Biological Potential, Gastrointestinal Digestion, Absorption, and Bioavailability of Algae-Derived Compounds with Neuroprotective Activity: A Comprehensive Review
Abstract
:1. Introduction
1.1. Overview of Neurodegenerative Diseases
1.1.1. Protein Aggregates
1.1.2. Oxidative and Nitrosative Stress
1.1.3. Metal Dyshomeostasis
1.1.4. Neuroinflammation
1.1.5. Mitochondrial Dysfunction
1.1.6. Neurotransmitters
1.1.7. Neurotransmitter Receptors and Other Straightly Related to Neurodegenerative Diseases
2. Methods
3. Compounds with Potential Neuroprotective Activity Extracted from Macroalgae
3.1. Polysaccharides
Compound | Concentration Tested | Macroalgae | Bioactivity | Type of Model | Experimental Model | Reference |
---|---|---|---|---|---|---|
Ulvan | 20–333.33 µg/mL | U. lactuca | Antioxidant | In vitro | ABTS•+, DPPH•, •OH scavenging, and metal chelating activity | [203] |
33–133 µg/mL | U. lactuca | Inhibition AChE and BChE | In vitro | In vitro assay | [203] | |
Fucoidan | 1–50 µg/mL | F. vesiculosus | Mitochondria biogenesis/energy production | In vitro | PD-induced by MPP+ in SH-SY5Y (parameters assessed: cell viability, apoptosis, oxidative stress, and mitochondrial dysfunction) | [232] |
Fucoidan | 25–100 µg/mL | F. vesiculosus | Anti-inflammatory | In vitro | LPS -induced inflammation in BV2 microglia cells (parameters assessed: cell viability, levels of •NO and PGE2, and expression of pro- and anti-inflammatory mediators) | [234] |
Fucoidan | 3.125–100 µg/mL | F. vesiculosus | Anti-aggregation Aβ1–42 | In vitro | H2O2 or Aβ1–42 treated PC-12 cells (parameters assessed: cell viability, apoptosis, and neurite outgrowth) | [236] |
Fucoidan | 3.125–100 µg/mL | U. pinnatifida | Anti-aggregation Aβ1–42 | In vitro | H2O2 or Aβ1–42 treated PC-12 cells (parameters assessed: cell viability, apoptosis, and neurite outgrowth) | [236] |
Fucoidan | S. hemiphyllum | Antioxidant | In vitro | ABTS•+, DPPH•, FRAP | [242] | |
Porphyran | 25 and 50 mg/kg | P. capensis | Anti-apoptotic | In vivo | Male C57BL6 mice model of PD induced by MPTP (parameters assessed: body weight ratio and behavioural patterns) | [244] |
Sulphated agaran | 15–60 µg | Gracilaria cornea | Antioxidant | In vivo | PD rat model induced by 6-OHDA (parameters assessed: behavioural, neurochemical, and transcriptional analyses) | [246] |
K-carrageenan | 0.01–1.0 mg/mL | H. musciformis | Anti-apoptotic | In vitro | SH-SY5Y cells treated by 6-OHDA (parameters assessed: cell viability, apoptosis, mitochondrial potential, and H2O2 levels) | [247] |
3.2. Aminoacids, Peptides, and Protein Hydrolysates
Compound | Concentration Tested | Macroalgae | Bioactivity | Type of Model | Experimental Model | Reference |
---|---|---|---|---|---|---|
Glycoprotein (UPGP, 10 KDa) | 5–100 µg/mL (cell viability) 50–500 µg/mL (COX inhibition) 0–5 mg/mL (SOD and xanthine oxidase inhibition) | U. pinnatifida | Inhibition of BACE1, AChE, and BChE and anti-inflammatory activity | In vitro | Inhibition of BACE1, AChE, BChE, COX-1, COX-2, SOD, and xanthine oxidase; assessment of •NO level and cell viability of LPS-treated RAW 264.7 cells; determination of cell viability of primary hippocampal neurons | [204] |
Ser-Asp-Ile-Thr-Arg-Pro-Gly-Gly-Gln-Met | P. palmata | Antioxidant | In vitro | ORAC and FRAP | [284] | |
Glu-Leu-Trp-Lys-Thr-Phe (ELWKTF) | 2 and 4 mg/mL | G. lemaneiformis | Antioxidant | In vitro | DPPH• scavenging activity | [285] |
KAQAD | 250–1000 ng/mL | P. yezoensis | Anti-inflammatory | In vitro | RAW 264.7 treated by LPS (parameters assessed: cell viability, levels of •NO and ROS, and expression of pro- and anti-inflammatory mediators) | [286] |
H9EHL5 | C. taxifolia | Proteolysis activator | In silico | In silico assays | [287] | |
Glycoprotein (LJGP) | 25–100 µg/mL | L. japonica | Anti-inflammatory | In vitro | LPS-induced proinflammation in BV2 microglial cells (parameters assessed: cell viability, levels of •NO, PGE2, TNF-α, and IL-1β, expression of pro- and anti-inflammatory mediators, and activation of anti-inflammatory pathways) | [288] |
3.3. Polyunsaturated Fatty Acids
3.4. Photosynthetic Pigments
Compound | Concentration Tested | Macroalgae | Bioactivity | Type of Model | Experimental Model | Reference |
---|---|---|---|---|---|---|
Fucoxanthin | 50–200 mg/kg | S. horneri | Inhibition of AChE and animal behaviour | In vitro and in vivo | In vitro AChE inhibition and scopolamine-induced cognitive impairment in ICR mice (parameters assessed: locomotor activity, recognition impairment, spatial learning and memory impairments, expression of neurotropic factors, and ChAT and AChE activity) | [205] |
Fucoxanthin | 2–100 µM | U. pinnatifida | Inhibition of BACE1 | In vitro | In vitro assay | [208] |
Fucoxanthin | 2–100 µM | E. stolonifera | Inhibition of BACE1 | In vitro | In vitro assay | [208] |
Fucoxanthin | 100–400 µM | E. bicyclis | Inhibition of hMAOs | In vitro | In vitro assay | [211] |
Fucoxanthin | 100–400 µM | U. pinnatifida | Inhibition of hMAOs | In vitro | In vitro assay | [211] |
Extract and fractions containing phycobiliproteins and chlorophyll a | 100–500 µg/mL | P. palmata | Anti-inflammatory | In vitro | LPS-stimulated RAW 264.7 cells (parameters assessed: Levels of •NO, TNF-α, and IL-6) | [310] |
Ethanol extract, fucoxanthin, and fucoxanthinol | Extract (5–30 µg/mL) Fucoxanthin (25–250 ng/mL) Fucoxanthinol (50–100 ng/mL) | U. pinnatifida | Antioxidant | In vitro | Primary cultures of rat hippocampal neurons (parameters assessed: cell viability, apoptosis, mitochondrial integrity, intracellular ROS, and total length of primary neurites) | [312] |
Fucoxanthin | 0.1–30 µM (in vitro) 50–200 mg/kg (in vivo) | S. horneri | Inhibition of Aβ assembly | In vitro and in vivo | In vitro inhibition of Aβ1–42 oligomers formation; SH-SY5Y cells treated with Aβ1–42 oligomers (parameters assessed: cell survival); Aβ1–42 oligomer-treated mice (parameters assessed: locomotor activity, and recognition performance) | [313] |
Ethyl acetate fraction containing fucoxanthin, canthaxanthin, and violaxanthin, among other compounds | 10–100 µg/mL | E. prolifera | Antioxidant and anti-apoptotic | In vitro | HT-22 cells treated with glutamate (parameters assessed: cell viability, intracellular ROS, apoptosis, expression of antioxidant activities, and neurotropic factors) | [314] |
Fucoxanthin | 0.3–3 µM | S. horneri | Antioxidant and Inhibition of Aβ assembly | In vitro | SH-SY5Y cells treated with Aβ oligomers (parameters assessed: cell viability, apoptosis, intracellular ROS, and activation of signalling pathways) | [343] |
Fucoxanthin | 0.3–3 µM | S. horneri | Antioxidant | In vitro | H2O2-induced toxicity in SH-SY5Y cells and in primary cerebellar granule neurons (parameters assessed: cell viability, apoptosis, intracellular ROS, and signalling pathways activation) | [344] |
3.5. Phlorotannins and Other Phenols
Compound | Tested Concentration | Macroalgae | Bioactivity | Type of Model | Experimental Model | Reference |
---|---|---|---|---|---|---|
Dioxinodehydroeckol, eckol, phlorofurofucoeckol-A | E. bicyclis | Inhibition of BACE1 | In vitro | In vitro assay | [209] | |
Fucofuroeckol-b | 25–100 µg/mL | E. bicyclis | Inhibition of β-secretase | In vitro | Aβ-induced toxicity on SH-SY5Y cells overexpressing APP695swe (parameters assessed: cell viability and expression levels of sAPPβ and Aβ42) | [210] |
Eckol and dieckol | E. bicyclis | Inhibition of hMAOs | In vitro | In vitro assay | [212] | |
Phlorofucofuroeckol-A | E. stolonifera | Inhibition of hMAOs | In vitro | In vitro assay | [213] | |
6, 6′-Bieckol | 10–40 µM | E. stolonifera | Anti-inflammatory | In vitro | LPS-stimulated BV2 and murine primary microglial cells (parameters assessed: cell viability, intracellular ROS, levels of pro-inflammatory mediators, activation of signalling pathways) | [364] |
Diphlorethohydroxycarmalol | 0.5–50 µM | I. okamurae | Antioxidant | In vitro | HT22 cells treated by H2O2 (parameters assessed: cell viability, apoptosis, intracellular ROS, lipid peroxidation inhibitory activity, and intracellular Ca2+ level) | [367] |
Different extracts containing phloroglucinol and other phenolic compounds | H. elongata | Antioxidant | In vitro | DPPH• scavenging activity | [369] |
3.6. Other Compounds
4. Gastrointestinal Digestion, Absorption, and Bioavailability of Algae-Derived Compounds
5. Macroalgae as Potential Prebiotics and the Gut–Brain Axis
6. Clinical Studies
7. Safety of Consumption of Seaweeds
8. Conclusions and Future Prospective
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kim, S.K.; Wijesekara, I. Development and biological activities of marine-derived bioactive peptides: A review. J. Funct. Foods 2010, 2, 1–9. [Google Scholar] [CrossRef]
- Rengasamy, K.R.; Mahomoodally, M.F.; Aumeeruddy, M.Z.; Zengin, G.; Xiao, J.; Kim, D.H. Bioactive compounds in seaweeds: An overview of their biological properties and safety. Food Chem. Toxicol. 2020, 135, 111013. [Google Scholar] [CrossRef]
- Barzkar, N.; Jahromi, S.T.; Poorsaheli, H.B.; Vianello, F. Vianello Metabolites from Marine Microorganisms, Micro, and Macroalgae: Immense Scope for Pharmacology. Mar. Drugs 2019, 17, 464. [Google Scholar] [CrossRef] [Green Version]
- Circuncisão, A.; Catarino, M.; Cardoso, S.; Silva, A. Minerals from Macroalgae Origin: Health Benefits and Risks for Consumers. Mar. Drugs 2018, 16, 400. [Google Scholar] [CrossRef] [Green Version]
- Vieira, E.F.; Soares, C.; Machado, S.; Correia, M.; Ramalhosa, M.J.; Oliva-teles, M.T.; Paula Carvalho, A.; Domingues, V.F.; Antunes, F.; Oliveira, T.A.C.; et al. Seaweeds from the Portuguese coast as a source of proteinaceous material: Total and free amino acid composition profile. Food Chem. 2018, 269, 264–275. [Google Scholar] [CrossRef] [Green Version]
- Sá Monteiro, M.; Sloth, J.; Holdt, S.; Hansen, M. Analysis and Risk Assessment of Seaweed. EFSA J. 2019, 17, e170915. [Google Scholar] [CrossRef] [Green Version]
- Lorenzo, J.M.; Agregán, R.; Munekata, P.E.S.; Franco, D.; Carballo, J.; Şahin, S.; Lacomba, R.; Barba, F.J. Proximate composition and nutritional value of three macroalgae: Ascophyllum nodosum, Fucus vesiculosus and Bifurcaria bifurcata. Mar. Drugs 2017, 15, 360. [Google Scholar] [CrossRef] [Green Version]
- Gupta, S.; Abu-Ghannam, N. Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci. Technol. 2011, 22, 315–326. [Google Scholar] [CrossRef] [Green Version]
- Rosa, G.P.; Tavares, W.R.; Sousa, P.M.C.; Pagès, A.K.; Seca, A.M.L.; Pinto, D.C.G.A. Seaweed Secondary Metabolites with Beneficial Health Effects: An Overview of Successes in In Vivo Studies and Clinical Trials. Mar. Drugs 2019, 18, 8. [Google Scholar] [CrossRef] [Green Version]
- Alghazwi, M.; Kan, Y.Q.; Zhang, W.; Gai, W.P.; Garson, M.J.; Smid, S. Neuroprotective activities of natural products from marine macroalgae during 1999–2015. J. Appl. Phycol. 2016, 28, 3599–3616. [Google Scholar] [CrossRef]
- Cruz, L.J.; Luque-Ortega, J.R.; Rivas, L.; Albericio, F. Kahalalide F, an Antitumor Depsipeptide in Clinical Trials, and Its Analogues as Effective Antileishmanial Agents. Mol. Pharm. 2009, 6, 813–824. [Google Scholar] [CrossRef]
- Hitoe, S.; Shimoda, H. Seaweed Fucoxanthin Supplementation Improves Obesity Parameters in Mild Obese Japanese Subjects. Funct. Foods Health Dis. 2017, 7, 246. [Google Scholar] [CrossRef]
- Cai, Y.; Xu, W.; Gu, C.; Cai, X.; Qu, D.; Lu, L.; Xie, Y.; Jiang, S. Griffithsin with A Broad-Spectrum Antiviral Activity by Binding Glycans in Viral Glycoprotein Exhibits Strong Synergistic Effect in Combination with A Pan-Coronavirus Fusion Inhibitor Targeting SARS-CoV-2 Spike S2 Subunit. Virol. Sin. 2020, 35, 857–860. [Google Scholar] [CrossRef]
- Aisen, P.S.; Gauthier, S.; Ferris, S.H.; Saumier, D.; Haine, D.; Garceau, D.; Duong, A.; Suhy, J.; Oh, J.; Lau, W.C.; et al. Tramiprosate in mild-to-moderate Alzheimer’s disease—A randomized, double-blind, placebo-controlled, multi-centre study (the alphase study). Arch. Med. Sci. 2011, 7, 102–111. [Google Scholar] [CrossRef] [Green Version]
- Wang, T.; Kuang, W.; Chen, W.; Xu, W.; Zhang, L.; Li, Y.; Li, H.; Peng, Y.; Chen, Y.; Wang, B.; et al. A phase II randomized trial of sodium oligomannate in Alzheimer’s dementia. Alzheimer’s Res. Ther. 2020, 12, 110. [Google Scholar] [CrossRef]
- Tierney, M.S.; Croft, A.K.; Hayes, M. A review of antihypertensive and antioxidant activities in macroalgae. Bot. Mar. 2010, 53, 387–408. [Google Scholar] [CrossRef]
- Cian, R.; Drago, S.; de Medina, F.; Martínez-Augustin, O. Proteins and Carbohydrates from Red Seaweeds: Evidence for Beneficial Effects on Gut Function and Microbiota. Mar. Drugs 2015, 13, 5358–5383. [Google Scholar] [CrossRef] [Green Version]
- Pérez, M.J.; Falqué, E.; Domínguez, H. Antimicrobial action of compounds from marine seaweed. Mar. Drugs 2016, 14, 52. [Google Scholar] [CrossRef] [Green Version]
- Adrien, A.; Dufour, D.; Baudouin, S.; Maugard, T.; Bridiau, N. Evaluation of the anticoagulant potential of polysaccharide-rich fractions extracted from macroalgae. Nat. Prod. Res. 2017, 31, 2126–2136. [Google Scholar] [CrossRef]
- Schmid, M.; Kraft, L.G.K.; van der Loos, L.M.; Kraft, G.T.; Virtue, P.; Nichols, P.D.; Hurd, C.L. Southern Australian seaweeds: A promising resource for omega-3 fatty acids. Food Chem. 2018, 265, 70–77. [Google Scholar] [CrossRef]
- Zaharudin, N.; Salmeán, A.A.; Dragsted, L.O. Inhibitory effects of edible seaweeds, polyphenolics and alginates on the activities of porcine pancreatic α-amylase. Food Chem. 2018, 245, 1196–1203. [Google Scholar] [CrossRef]
- Saeed, A.M.; Abotaleb, S.I.; Alam, N.G.; Elmehalawy, A.A.; Gheda, S.F. In vitro assessment of antimicrobial, antioxidant and anticancer activities of some marine macroalgae. Egypt. J. Bot. 2020, 60, 81–96. [Google Scholar] [CrossRef]
- Chin, Y.X.; Chen, X.; Cao, W.X.; Sharifuddin, Y.; Green, B.D.; Lim, P.E.; Xue, C.H.; Tang, Q.J. Characterization of seaweed hypoglycemic property with integration of virtual screening for identification of bioactive compounds. J. Funct. Foods 2020, 64, 103656. [Google Scholar] [CrossRef]
- Barbosa, M.; Valentão, P.; Andrade, P. Bioactive Compounds from Macroalgae in the New Millennium: Implications for Neurodegenerative Diseases. Mar. Drugs 2014, 12, 4934–4972. [Google Scholar] [CrossRef]
- Jeyakumar, M.; Sathya, S.; Gandhi, S.; Tharra, P.; Suryanarayanan, V.; Singh, S.K.; Baire, B.; Pandima Devi, K. α-bisabolol β-D-fucopyranoside as a potential modulator of β-amyloid peptide induced neurotoxicity: An in vitro & in silico study. Bioorg. Chem. 2019, 88, 102935. [Google Scholar] [CrossRef]
- Olasehinde, T.A.; Mabinya, L.V.; Olaniran, A.O.; Okoh, A.I. Chemical characterization, antioxidant properties, cholinesterase inhibitory and anti-amyloidogenic activities of sulfated polysaccharides from some seaweeds. Bioact. Carbohydrates Diet. Fibre 2019, 18, 100182. [Google Scholar] [CrossRef]
- Shanmuganathan, B.; Sathya, S.; Balasubramaniam, B.; Balamurugan, K.; Devi, K.P. Amyloid-β induced neuropathological actions are suppressed by Padina gymnospora (Phaeophyceae) and its active constituent α-bisabolol in Neuro2a cells and transgenic Caenorhabditis elegans Alzheimer’s model. Nitric Oxide-Biol. Chem. 2019, 91, 52–66. [Google Scholar] [CrossRef]
- Alghazwi, M.; Charoensiddhi, S.; Smid, S.; Zhang, W. Impact of Ecklonia radiata extracts on the neuroprotective activities against amyloid beta (Aβ1-42) toxicity and aggregation. J. Funct. Foods 2020, 68, 103893. [Google Scholar] [CrossRef]
- Barbosa, M.; Valentão, P.; Ferreres, F.; Gil-Izquierdo, Á.; Andrade, P.B. In vitro multifunctionality of phlorotannin extracts from edible Fucus species on targets underpinning neurodegeneration. Food Chem. 2020, 333, 127456. [Google Scholar] [CrossRef]
- Maiese, K. Targeting molecules to medicine with mTOR, autophagy and neurodegenerative disorders. Br. J. Clin. Pharmacol. 2016, 82, 1245–1266. [Google Scholar] [CrossRef] [Green Version]
- Sosa-Ortiz, A.L.; Acosta-Castillo, I.; Prince, M.J. Epidemiology of Dementias and Alzheimer’s Disease. Arch. Med. Res. 2012, 43, 600–608. [Google Scholar] [CrossRef]
- Erdö, F.; Denes, L.; De Lange, E. Age-associated physiological and pathological changes at the blood-brain barrier: A review. J. Cereb. Blood Flow Metab. 2017, 37, 4–24. [Google Scholar] [CrossRef] [Green Version]
- Brown, R.C.; Lockwood, A.H.; Sonawane, B.R. Neurodegenerative Diseases: An Overview of Environmental Risk Factors. Environ. Health Perspect. 2005, 113, 1250–1256. [Google Scholar] [CrossRef] [Green Version]
- Jomova, K.; Vondrakova, D.; Lawson, M.; Valko, M. Metals, oxidative stress and neurodegenerative disorders. Mol. Cell. Biochem. 2010, 345, 91–104. [Google Scholar] [CrossRef]
- Lai, T.W.; Zhang, S.; Wang, Y.T. Excitotoxicity and stroke: Identifying novel targets for neuroprotection. Prog. Neurobiol. 2014, 115, 157–188. [Google Scholar] [CrossRef] [Green Version]
- Chaturvedi, M.; Kaczmarek, L. MMP-9 Inhibition: A Therapeutic Strategy in Ischemic Stroke. Mol. Neurobiol. 2014, 49, 563–573. [Google Scholar] [CrossRef] [Green Version]
- Baune, B.T. Inflammation and neurodegenerative disorders. Curr. Opin. Psychiatry 2015, 28, 148–154. [Google Scholar] [CrossRef]
- Barbalace, M.C.; Malaguti, M.; Giusti, L.; Lucacchini, A.; Hrelia, S.; Angeloni, C. Anti-Inflammatory Activities of Marine Algae in Neurodegenerative Diseases. Int. J. Mol. Sci. 2019, 20, 3061. [Google Scholar] [CrossRef] [Green Version]
- Hannan, M.A.; Dash, R.; Haque, M.N.; Mohibbullah, M.; Sohag, A.A.M.; Rahman, M.A.; Uddin, M.J.; Alam, M.; Moon, I.S. Neuroprotective Potentials of Marine Algae and Their Bioactive Metabolites: Pharmacological Insights and Therapeutic Advances. Mar. Drugs 2020, 18, 347. [Google Scholar] [CrossRef]
- Schepers, M.; Martens, N.; Tiane, A.; Vanbrabant, K.; Liu, H.B.; Lütjohann, D.; Mulder, M.; Vanmierlo, T. Edible seaweed-derived constituents: An undisclosed source of neuroprotective compounds. Neural Regen. Res. 2020, 15, 790–795. [Google Scholar] [CrossRef]
- Syed, Y.Y. Sodium Oligomannate: First Approval. Drugs 2020, 80, 441–444. [Google Scholar] [CrossRef]
- McIsaac, T.L.; Fritz, N.E.; Quinn, L.; Muratori, L.M. Cognitive-motor interference in neurodegenerative disease: A narrative review and implications for clinical management. Front. Psychol. 2018, 9, 2061. [Google Scholar] [CrossRef]
- Höglund, K.; Salter, H. Molecular biomarkers of neurodegeneration. Expert Rev. Mol. Diagn. 2013, 13, 845–861. [Google Scholar] [CrossRef]
- Skovronsky, D.M.; Lee, V.M.-Y.; Trojanowski, J.Q. NEURODEGENERATIVE DISEASES: New Concepts of Pathogenesis and Their Therapeutic Implications. Annu. Rev. Pathol. Mech. Dis. 2006, 1, 151–170. [Google Scholar] [CrossRef]
- Kraft, A.D.; Jean Harry, G. Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int. J. Environ. Res. Public Health 2011, 8, 2980–3018. [Google Scholar] [CrossRef] [Green Version]
- Liu, Z.; Zhou, T.; Ziegler, A.C.; Dimitrion, P.; Zuo, L. Oxidative Stress in Neurodegenerative Diseases: From Molecular Mechanisms to Clinical Applications. Oxid. Med. Cell. Longev. 2017, 2017, 2525967. [Google Scholar] [CrossRef]
- Foti, S.C.; Hargreaves, I.; Carrington, S.; Kiely, A.P.; Houlden, H.; Holton, J.L. Cerebral mitochondrial electron transport chain dysfunction in multiple system atrophy and Parkinson’s disease. Sci. Rep. 2019, 9, 6559. [Google Scholar] [CrossRef] [Green Version]
- Acevedo, K.; Masaldan, S.; Opazo, C.M.; Bush, A.I. Redox active metals in neurodegenerative diseases. JBIC J. Biol. Inorg. Chem. 2019, 24, 1141–1157. [Google Scholar] [CrossRef]
- Bae, J.R.; Kim, S.H. Synapses in neurodegenerative diseases. BMB Rep. 2017, 50, 237–246. [Google Scholar] [CrossRef] [Green Version]
- Sheikh, S.; Safia; Haque, E.; Mir, S.S. Neurodegenerative Diseases: Multifactorial Conformational Diseases and Their Therapeutic Interventions. J. Neurodegener. Dis. 2013, 2013, 563481. [Google Scholar] [CrossRef] [Green Version]
- Dong, X.X.; Wang, Y.; Qin, Z.H. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol. Sin. 2009, 30, 379–387. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, Z.; Chan, C.H.; Ma, Q.; Xu, X.; Xiao, Z.; Tan, E.-K. The roles of amyloid precursor protein (APP) in neurogenesis. Cell Adh. Migr. 2011, 5, 280–292. [Google Scholar] [CrossRef] [Green Version]
- West, S.; Bhugra, P. Emerging drug targets for A β and tau in Alzheimer’s disease: A systematic review. Br. J. Clin. Pharmacol. 2015, 80, 221–234. [Google Scholar] [CrossRef] [Green Version]
- Jevtic, S.; Provias, J. The Amyloid Precursor Protein: More than Just Amyloid- Beta. J. Neurol. Exp. Neurosci. 2019, 5, 1–11. [Google Scholar] [CrossRef]
- Kandalepas, P.C.; Vassar, R. Identification and biology of β-secretase. J. Neurochem. 2012, 120, 55–61. [Google Scholar] [CrossRef] [PubMed]
- Gao, C.M.; Yam, A.Y.; Wang, X.; Magdangal, E.; Salisbury, C.; Peretz, D.; Zuckermann, R.N.; Connolly, M.D.; Hansson, O.; Minthon, L.; et al. Aβ40 oligomers identified as a potential biomarker for the diagnosis of alzheimer’s disease. PLoS ONE 2010, 5, e0015725. [Google Scholar] [CrossRef] [PubMed]
- Wolfe, M.S. Tau mutations in neurodegenerative diseases. J. Biol. Chem. 2009, 284, 6021–6025. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hernández, F.; Gómez de Barreda, E.; Fuster-Matanzo, A.; Lucas, J.J.; Avila, J. GSK3: A possible link between beta amyloid peptide and tau protein. Exp. Neurol. 2010, 223, 322–325. [Google Scholar] [CrossRef]
- Lauretti, E.; Dincer, O.; Praticò, D. Glycogen synthase kinase-3 signaling in Alzheimer’s disease. Biochim. Biophys. Acta—Mol. Cell Res. 2020, 1867, 118664. [Google Scholar] [CrossRef]
- Rudrabhatla, P.; Jaffe, H.; Pant, H.C. Direct evidence of phosphorylated neuronal intermediate filament proteins in neurofibrillary tangles (NFTs): Phosphoproteomics of Alzheimer’s NFTs. FASEB J. 2011, 25, 3896–3905. [Google Scholar] [CrossRef]
- Kopeikina, K.; Hyman, B.; Spires-Jones, T. Soluble forms of tau are toxic in Alzheimer’s disease. Transl. Neurosci. 2012, 3, 223–233. [Google Scholar] [CrossRef]
- Snead, D.; Eliezer, D. Alpha-Synuclein Function and Dysfunction on Cellular Membranes. Exp. Neurobiol. 2014, 23, 292–313. [Google Scholar] [CrossRef] [Green Version]
- Butler, B.; Sambo, D.; Khoshbouei, H. Alpha-synuclein modulates dopamine neurotransmission. J. Chem. Neuroanat. 2017, 83–84, 41–49. [Google Scholar] [CrossRef]
- Bellucci, A.; Mercuri, N.B.; Venneri, A.; Faustini, G.; Longhena, F.; Pizzi, M.; Missale, C.; Spano, P. Review: Parkinson’s disease: From synaptic loss to connectome dysfunction. Neuropathol. Appl. Neurobiol. 2016, 42, 77–94. [Google Scholar] [CrossRef] [Green Version]
- Colosimo, C. Lewy body cortical involvement may not always predict dementia in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 2003, 74, 852–856. [Google Scholar] [CrossRef] [Green Version]
- Parkkinen, L.; O’Sullivan, S.S.; Collins, C.; Petrie, A.; Holton, J.L.; Revesz, T.; Lees, A.J. Disentangling the Relationship between Lewy Bodies and Nigral Neuronal Loss in Parkinson’s Disease. J. Parkinsons. Dis. 2011, 1, 277–286. [Google Scholar] [CrossRef] [Green Version]
- Strand, A.D.; Aragaki, A.K.; Shaw, D.; Bird, T.; Holton, J.; Turner, C.; Tapscott, S.J.; Tabrizi, S.J.; Schapira, A.H.; Kooperberg, C.; et al. Gene expression in Huntington’s disease skeletal muscle: A potential biomarker. Hum. Mol. Genet. 2005, 14, 1863–1876. [Google Scholar] [CrossRef] [Green Version]
- Xiao, G.; Fan, Q.; Wang, X.; Zhou, B. Huntington disease arises from a combinatory toxicity of polyglutamine and copper binding. Proc. Natl. Acad. Sci. USA 2013, 110, 14995–15000. [Google Scholar] [CrossRef] [Green Version]
- Novak, M.J.U.; Tabrizi, S.J. Clinical Review Huntington ’ s disease. Br. Med. J. 2010, 341, 34–40. [Google Scholar] [CrossRef] [Green Version]
- Miller, J.; Arrasate, M.; Shaby, B.A.; Mitra, S.; Masliah, E.; Finkbeiner, S. Quantitative relationships between huntingtin levels, polyglutamine length, inclusion body formation, and neuronal death provide novel insight into huntington’s disease molecular pathogenesis. J. Neurosci. 2010, 30, 10541–10550. [Google Scholar] [CrossRef] [Green Version]
- Hübers, A.; Hildebrandt, V.; Petri, S.; Kollewe, K.; Hermann, A.; Storch, A.; Hanisch, F.; Zierz, S.; Rosenbohm, A.; Ludolph, A.C.; et al. Clinical features and differential diagnosis of flail arm syndrome. J. Neurol. 2016, 263, 390–395. [Google Scholar] [CrossRef]
- Ramesh, N.; Pandey, U.B. Autophagy dysregulation in ALS: When protein aggregates get out of hand. Front. Mol. Neurosci. 2017, 10, 263. [Google Scholar] [CrossRef] [Green Version]
- Thellung, S.; Corsaro, A.; Nizzari, M.; Barbieri, F.; Florio, T. Autophagy activator drugs: A new opportunity in neuroprotection from misfolded protein toxicity. Int. J. Mol. Sci. 2019, 20, 901. [Google Scholar] [CrossRef] [Green Version]
- Sarkar, S.; Rubinsztein, D.C. Huntington’s disease: Degradation of mutant huntingtin by autophagy. FEBS J. 2008, 275, 4263–4270. [Google Scholar] [CrossRef]
- Schapira, A.H.; Jenner, P. Etiology and pathogenesis of Parkinson’s disease. Mov. Disord. 2011, 26, 1049–1055. [Google Scholar] [CrossRef]
- Cecarini, V.; Bonfili, L.; Cuccioloni, M.; Mozzicafreddo, M.; Rossi, G.; Buizza, L.; Uberti, D.; Angeletti, M.; Eleuteri, A.M. Crosstalk between the ubiquitin-proteasome system and autophagy in a human cellular model of Alzheimer’s disease. Biochim. Biophys. Acta—Mol. Basis Dis. 2012, 1822, 1741–1751. [Google Scholar] [CrossRef]
- Hara, T.; Nakamura, K.; Matsui, M.; Yamamoto, A.; Nakahara, Y.; Suzuki-Migishima, R.; Yokoyama, M.; Mishima, K.; Saito, I.; Okano, H.; et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441, 885–889. [Google Scholar] [CrossRef]
- Schönfeld, P.; Reiser, G. Brain energy metabolism spurns fatty acids as fuel due to their inherent mitotoxicity and potential capacity to unleash neurodegeneration. Neurochem. Int. 2017, 109, 68–77. [Google Scholar] [CrossRef]
- Milatovic, D.; Gupta, R.C. Antioxidants in Prevention and Treatment of Diseases and Toxicity. In Nutraceuticals in Veterinary Medicine; Springer International Publishing: Cham, Switzerland, 2019; pp. 205–213. ISBN 9783030046248. [Google Scholar]
- Xiang, W.; Schlachetzki, J.C.M.; Helling, S.; Bussmann, J.C.; Berlinghof, M.; Schäffer, T.E.; Marcus, K.; Winkler, J.; Klucken, J.; Becker, C.-M. Oxidative stress-induced posttranslational modifications of alpha-synuclein: Specific modification of alpha-synuclein by 4-hydroxy-2-nonenal increases dopaminergic toxicity. Mol. Cell. Neurosci. 2013, 54, 71–83. [Google Scholar] [CrossRef]
- Scudamore, O.; Ciossek, T. Increased Oxidative Stress Exacerbates α-Synuclein Aggregation In Vivo. J. Neuropathol. Exp. Neurol. 2018, 77, 443–453. [Google Scholar] [CrossRef]
- Goswami, A.; Dikshit, P.; Mishra, A.; Mulherkar, S.; Nukina, N.; Jana, N.R. Oxidative stress promotes mutant huntingtin aggregation and mutant huntingtin-dependent cell death by mimicking proteasomal malfunction. Biochem. Biophys. Res. Commun. 2006, 342, 184–190. [Google Scholar] [CrossRef]
- Swomley, A.M.; Förster, S.; Keeney, J.T.; Triplett, J.; Zhang, Z.; Sultana, R.; Butterfield, D.A. Abeta, oxidative stress in Alzheimer disease: Evidence based on proteomics studies. Biochim. Biophys. Acta—Mol. Basis Dis. 2014, 1842, 1248–1257. [Google Scholar] [CrossRef] [Green Version]
- Cheignon, C.; Tomas, M.; Bonnefont-Rousselot, D.; Faller, P.; Hureau, C.; Collin, F. Oxidative stress and the amyloid beta peptide in Alzheimer’s disease. Redox Biol. 2018, 14, 450–464. [Google Scholar] [CrossRef]
- Di Meo, S.; Reed, T.T.; Venditti, P.; Victor, V.M. Role of ROS and RNS Sources in Physiological and Pathological Conditions. Oxid. Med. Cell. Longev. 2016, 2016, 1245049. [Google Scholar] [CrossRef]
- Goyal, S.; Kaur, T.J. Antioxidants: Dietary scavengers in lifestyle diseases. J. Pharmacogn. Phytochem. 2019, 8, 96–102. [Google Scholar]
- Li, Y.R.; Trush, M. Defining ROS in Biology and Medicine. React. Oxyg. Species 2016, 1, 803. [Google Scholar] [CrossRef] [Green Version]
- Al-Dalaen, S.M. Review Article: Oxidative Stress Versus Antioxidants. Am. J. Biosci. Bioeng. 2014, 2, 60. [Google Scholar] [CrossRef] [Green Version]
- Rahal, A.; Kumar, A.; Singh, V.; Yadav, B.; Tiwari, R.; Chakraborty, S.; Dhama, K. Oxidative stress, prooxidants, and antioxidants: The interplay. BioMed Res. Int. 2014, 2014, 761264. [Google Scholar] [CrossRef] [Green Version]
- Gandhi, S.; Abramov, A.Y. Mechanism of Oxidative Stress in Neurodegeneration. Oxid. Med. Cell. Longev. 2012, 2012, 428010. [Google Scholar] [CrossRef] [Green Version]
- Salim, S. Oxidative Stress and the Central Nervous System. J. Pharmacol. Exp. Ther. 2017, 360, 201–205. [Google Scholar] [CrossRef]
- Dias, V.; Junn, E.; Mouradian, M.M. The role of oxidative stress in parkinson’s disease. J. Parkinsons. Dis. 2013, 3, 461–491. [Google Scholar] [CrossRef] [Green Version]
- Chang, K.-H.; Cheng, M.-L.; Chiang, M.-C.; Chen, C.-M. Lipophilic antioxidants in neurodegenerative diseases. Clin. Chim. Acta 2018, 485, 79–87. [Google Scholar] [CrossRef]
- Surh, Y.J.; Kundu, J.K.; Li, M.H.; Na, H.K.; Cha, Y.N. Role of Nrf2-mediated heme oxygenase-1 upregulation in adaptive survival response to nitrosative stress. Arch. Pharm. Res. 2009, 32, 1163–1176. [Google Scholar] [CrossRef]
- Tsang, A.H.K.; Chung, K.K.K. Oxidative and nitrosative stress in Parkinson’s disease. Biochim. Biophys. Acta—Mol. Basis Dis. 2009, 1792, 643–650. [Google Scholar] [CrossRef] [Green Version]
- Duce, J.A.; Bush, A.I. Biological metals and Alzheimer’s disease: Implications for therapeutics and diagnostics. Prog. Neurobiol. 2010, 92, 1–18. [Google Scholar] [CrossRef]
- Maret, W. The metals in the biological periodic system of the elements: Concepts and conjectures. Int. J. Mol. Sci. 2016, 17, 66. [Google Scholar] [CrossRef] [Green Version]
- Opazo, C.M.; Greenough, M.A.; Bush, A.I. Copper: From neurotransmission to neuroproteostasis. Front. Aging Neurosci. 2014, 6, 143. [Google Scholar] [CrossRef] [Green Version]
- Braidy, N.; Poljak, A.; Marjo, C.; Rutlidge, H.; Rich, A.; Jugder, B.E.; Jayasena, T.; Inestrosa, N.C.; Sachdev, P.S. Identification of cerebral metal ion imbalance in the brain of aging Octodon degus. Front. Aging Neurosci. 2017, 9, 66. [Google Scholar] [CrossRef]
- Liu, Y.; Nguyen, M.; Robert, A.; Meunier, B. Metal Ions in Alzheimer’s Disease: A Key Role or Not? Acc. Chem. Res. 2019, 52, 2026–2035. [Google Scholar] [CrossRef]
- Genoud, S.; Senior, A.M.; Hare, D.J.; Double, K.L. Meta-Analysis of Copper and Iron in Parkinson’s Disease Brain and Biofluids. Mov. Disord. 2020, 35, 662–671. [Google Scholar] [CrossRef]
- Schrag, M.; Mueller, C.; Oyoyo, U.; Smith, M.A.; Kirsch, W.M. Iron, zinc and copper in the Alzheimer’s disease brain: A quantitative meta-analysis. Some insight on the influence of citation bias on scientific opinion. Prog. Neurobiol. 2011, 94, 296–306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bucossi, S.; Ventriglia, M.; Panetta, V.; Salustri, C.; Pasqualetti, P.; Mariani, S.; Siotto, M.; Rossini, P.M.; Squitti, R. Copper in alzheimer’s disease: A meta-analysis of serum, plasma, and cerebrospinal fluid studies. J. Alzheimer’s Dis. 2011, 24, 175–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szewczyk, B. Zinc homeostasis and neurodegenerative disorders. Front. Aging Neurosci. 2013, 5, 33. [Google Scholar] [CrossRef] [Green Version]
- Manto, M. Abnormal copper homeostasis: Mechanisms and roles in neurodegeneration. Toxics 2014, 2, 327–345. [Google Scholar] [CrossRef]
- Li, K.; Reichmann, H. Role of iron in neurodegenerative diseases. J. Neural Transm. 2016, 123, 389–399. [Google Scholar] [CrossRef]
- Arena, G.; Bellia, F.; Frasca, G.; Grasso, G.; Lanza, V.; Rizzarelli, E.; Tabbì, G.; Zito, V.; Milardi, D. Inorganic stressors of ubiquitin. Inorg. Chem. 2013, 52, 9567–9573. [Google Scholar] [CrossRef]
- Tahmasebinia, F.; Emadi, S. Effect of metal chelators on the aggregation of beta-amyloid peptides in the presence of copper and iron. BioMetals 2017, 30, 285–293. [Google Scholar] [CrossRef]
- Yang, G.J.; Liu, H.; Ma, D.L.; Leung, C.H. Rebalancing metal dyshomeostasis for Alzheimer’s disease therapy. J. Biol. Inorg. Chem. 2019, 24, 1159–1170. [Google Scholar] [CrossRef]
- Lee, H.J.; Lee, Y.G.; Kang, J.; Yang, S.H.; Kim, J.H.; Ghisaidoobe, A.B.T.; Kang, H.J.; Lee, S.R.; Lim, M.H.; Chung, S.J. Monitoring metal-amyloid-β complexation by a FRET-based probe: Design, detection, and inhibitor screening. Chem. Sci. 2019, 10, 1000–1007. [Google Scholar] [CrossRef] [Green Version]
- Strodel, B.; Coskuner-Weber, O. Transition Metal Ion Interactions with Disordered Amyloid-β Peptides in the Pathogenesis of Alzheimer’s Disease: Insights from Computational Chemistry Studies. J. Chem. Inf. Model. 2019, 59, 1782–1805. [Google Scholar] [CrossRef]
- Wang, L.; Yin, Y.L.; Liu, X.Z.; Shen, P.; Zheng, Y.G.; Lan, X.R.; Lu, C.B.; Wang, J.Z. Current understanding of metal ions in the pathogenesis of Alzheimer’s disease. Transl. Neurodegener. 2020, 9, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodríguez-Rodríguez, C.; Telpoukhovskaia, M.; Orvig, C. The art of building multifunctional metal-binding agents from basic molecular scaffolds for the potential application in neurodegenerative diseases. Coord. Chem. Rev. 2012, 256, 2308–2332. [Google Scholar] [CrossRef]
- Robert, A.; Liu, Y.; Nguyen, M.; Meunier, B. Regulation of copper and Iron homeostasis by metal chelators: A possible chemotherapy for alzheimers disease. Acc. Chem. Res. 2015, 48, 1332–1339. [Google Scholar] [CrossRef] [PubMed]
- August, A.; Schmidt, N.; Klingler, J.; Baumkötter, F.; Lechner, M.; Klement, J.; Eggert, S.; Vargas, C.; Wild, K.; Keller, S.; et al. Copper and zinc ions govern the trans-directed dimerization of APP family members in multiple ways. J. Neurochem. 2019, 151, 626–641. [Google Scholar] [CrossRef]
- Banerjee, P.; Sahoo, A.; Anand, S.; Ganguly, A.; Righi, G.; Bovicelli, P.; Saso, L.; Chakrabarti, S. Multiple Mechanisms of Iron-Induced Amyloid Beta-Peptide Accumulation in SHSY5Y Cells: Protective Action of Negletein. NeuroMolecular Med. 2014, 16, 787–798. [Google Scholar] [CrossRef]
- Guo, C.; Wang, P.; Zhong, M.L.; Wang, T.; Huang, X.S.; Li, J.Y.; Wang, Z.Y. Deferoxamine inhibits iron induced hippocampal tau phosphorylation in the Alzheimer transgenic mouse brain. Neurochem. Int. 2013, 62, 165–172. [Google Scholar] [CrossRef]
- Myhre, O.; Utkilen, H.; Duale, N.; Brunborg, G.; Hofer, T. Metal Dyshomeostasis and Inflammation in Alzheimer’s and Parkinson’s Diseases: Possible Impact of Environmental Exposures. Oxid. Med. Cell. Longev. 2013, 2013, 726954. [Google Scholar] [CrossRef] [Green Version]
- Gkouvatsos, K.; Papanikolaou, G.; Pantopoulos, K. Regulation of iron transport and the role of transferrin. Biochim. Biophys. Acta—Gen. Subj. 2012, 1820, 188–202. [Google Scholar] [CrossRef]
- Wang, B.; Wang, X.-P. Does Ceruloplasmin Defend Against Neurodegenerative Diseases? Curr. Neuropharmacol. 2018, 17, 539–549. [Google Scholar] [CrossRef]
- Linder, M.C. Ceruloplasmin and other copper binding components of blood plasma and their functions: An update. Metallomics 2016, 8, 887–905. [Google Scholar] [CrossRef]
- De Riccardis, L.; Buccolieri, A.; Muci, M.; Pitotti, E.; De Robertis, F.; Trianni, G.; Manno, D.; Maffia, M. Copper and ceruloplasmin dyshomeostasis in serum and cerebrospinal fluid of multiple sclerosis subjects. Biochim. Biophys. Acta—Mol. Basis Dis. 2018, 1864, 1828–1838. [Google Scholar] [CrossRef] [PubMed]
- Barbariga, M.; Zanardi, A.; Curnis, F.; Conti, A.; Boselli, D.; Di Terlizzi, S.; Alessio, M. Ceruloplasmin oxidized and deamidated by Parkinson’s disease cerebrospinal fluid induces epithelial cells proliferation arrest and apoptosis. Sci. Rep. 2020, 10, 15507. [Google Scholar] [CrossRef] [PubMed]
- Savelieff, M.G.; Lee, S.; Liu, Y.; Lim, M.H. Untangling Amyloid-β, Tau, and Metals in Alzheimer’s Disease. ACS Chem. Biol. 2013, 8, 856–865. [Google Scholar] [CrossRef] [PubMed]
- Kempuraj, D.; Thangavel, R.; Natteru, P.A.; Selvakumar, G.P.; Saeed, D.; Zahoor, H.; Zaheer, S.; Iyer, S.S.; Zaheer, A. Neuroinflammation Induces Neurodegeneration. J. Neurol. Neurosurg. Spine 2016, 1, 1003. [Google Scholar]
- Shabab, T.; Khanabdali, R.; Moghadamtousi, S.Z.; Kadir, H.A.; Mohan, G. Neuroinflammation pathways: A general review. Int. J. Neurosci. 2017, 127, 624–633. [Google Scholar] [CrossRef]
- Heneka, M.T.; Carson, M.J.; Khoury, J.E.; Gary, E.; Brosseron, F.; Feinstein, D.L.; Jacobs, A.H.; Wyss-coray, T.; Vitorica, J.; Ransohoff, R.M. Neuroinflammation in Alzheimer’ s Disease. Lancet Neurol 2015, 14, 388–405. [Google Scholar] [CrossRef] [Green Version]
- Hickman, S.; Izzy, S.; Sen, P.; Morsett, L.; El Khoury, J. Microglia in neurodegeneration. Nat. Neurosci. 2018, 21, 1359–1369. [Google Scholar] [CrossRef]
- Chamidah, A.; Hardoko, H.; Awaludin Prihanto, A. Prebiotics Activity of Laminaran Derived From Sargassum crassifolium. Res. J. Life Sci. 2016, 3, 160–165. [Google Scholar] [CrossRef] [Green Version]
- Ransohoff, R.M. A polarizing question: Do M1 and M2 microglia exist? Nat. Neurosci. 2016, 19, 987–991. [Google Scholar] [CrossRef]
- Zeng, W.X.; Han, Y.L.; Zhu, G.F.; Huang, L.Q.; Deng, Y.Y.; Wang, Q.S.; Jiang, W.Q.; Wen, M.Y.; Han, Q.P.; Xie, D.; et al. Hypertonic saline attenuates expression of Notch signaling and proinflammatory mediators in activated microglia in experimentally induced cerebral ischemia and hypoxic BV-2 microglia. BMC Neurosci. 2017, 18, 32. [Google Scholar] [CrossRef] [Green Version]
- Zhou, S.; Du, X.; Xie, J.; Wang, J. Interleukin-6 regulates iron-related proteins through c-Jun N-terminal kinase activation in BV2 microglial cell lines. PLoS ONE 2017, 12, e0180464. [Google Scholar] [CrossRef] [PubMed]
- Koppula, S.; Kumar, H.; Kim, I.S.; Choi, D.K. Reactive oxygen species and inhibitors of inflammatory enzymes, NADPH oxidase, and iNOS in experimental models of parkinsons disease. Mediators Inflamm. 2012, 2012, 823902. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cianciulli, A.; Porro, C.; Calvello, R.; Trotta, T.; Lofrumento, D.D.; Panaro, M.A. Microglia Mediated Neuroinflammation: Focus on PI3K Modulation. Biomolecules 2020, 10, 137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teismann, P.; Sathe, K.; Bierhaus, A.; Leng, L.; Martin, H.L.; Bucala, R.; Weigle, B.; Nawroth, P.P.; Schulz, J.B. Receptor for advanced glycation endproducts (RAGE) deficiency protects against MPTP toxicity. Neurobiol. Aging 2012, 33, 2478–2490. [Google Scholar] [CrossRef] [Green Version]
- Saponaro, C.; Cianciulli, A.; Calvello, R.; Dragone, T.; Iacobazzi, F.; Panaro, M.A. The PI3K/Akt pathway is required for LPS activation of microglial cells. Immunopharmacol. Immunotoxicol. 2012, 34, 858–865. [Google Scholar] [CrossRef]
- von Bernhardi, R.; Eugenín, J. Microglial reactivity to β-amyloid is modulated by astrocytes and proinflammatory factors. Brain Res. 2004, 1025, 186–193. [Google Scholar] [CrossRef]
- Joshi, P.; Turola, E.; Ruiz, A.; Bergami, A.; Libera, D.D.; Benussi, L.; Giussani, P.; Magnani, G.; Comi, G.; Legname, G.; et al. Microglia convert aggregated amyloid-β into neurotoxic forms through the shedding of microvesicles. Cell Death Differ. 2014, 21, 582–593. [Google Scholar] [CrossRef] [Green Version]
- Navarro, V.; Sanchez-Mejias, E.; Jimenez, S.; Muñoz-Castro, C.; Sanchez-Varo, R.; Davila, J.C.; Vizuete, M.; Gutierrez, A.; Vitorica, J. Microglia in Alzheimer’s Disease: Activated, Dysfunctional or Degenerative. Front. Aging Neurosci. 2018, 10, 140. [Google Scholar] [CrossRef] [Green Version]
- Perea, J.R.; Llorens-Martín, M.; Ávila, J.; Bolós, M. The role of microglia in the spread of Tau: Relevance for tauopathies. Front. Cell. Neurosci. 2018, 12, 172. [Google Scholar] [CrossRef] [Green Version]
- Španić, E.; Langer Horvat, L.; Hof, P.R.; Šimić, G. Role of Microglial Cells in Alzheimer’s Disease Tau Propagation. Front. Aging Neurosci. 2019, 11, 271. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Wang, T.; Pei, Z.; Miller, D.S.; Wu, X.; Block, M.L.; Wilson, B.; Zhang, W.; Zhou, Y.; Hong, J.-S.; et al. Aggregated α-synuclein activates microglia: A process leading to disease progression in Parkinson’s disease. FASEB J. 2005, 19, 533–542. [Google Scholar] [CrossRef] [PubMed]
- Sapp, E.; Kegel, K.B.; Aronin, N.; Hashikawa, T.; Uchiyama, Y.; Tohyama, K.; Bhide, P.G.; Vonsattel, J.P.; Difiglia, M. Early and Progressive Accumulation of Reactive Microglia in the Huntington Disease Brain. J. Neuropathol. Exp. Neurol. 2001, 60, 161–172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Markaki, M.; Tavernarakis, N. Mitochondrial turnover and homeostasis in ageing and neurodegeneration. FEBS Lett. 2020, 594, 2370–2379. [Google Scholar] [CrossRef] [PubMed]
- Aufschnaiter, A.; Kohler, V.; Diessl, J.; Peselj, C.; Carmona-Gutierrez, D.; Keller, W.; Büttner, S. Mitochondrial lipids in neurodegeneration. Cell Tissue Res. 2017, 367, 125–140. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Golpich, M.; Amini, E.; Mohamed, Z.; Azman Ali, R.; Mohamed Ibrahim, N.; Ahmadiani, A. Mitochondrial Dysfunction and Biogenesis in Neurodegenerative diseases: Pathogenesis and Treatment. CNS Neurosci. Ther. 2017, 23, 5–22. [Google Scholar] [CrossRef] [PubMed]
- Lou, G.; Palikaras, K.; Lautrup, S.; Scheibye-Knudsen, M.; Tavernarakis, N.; Fang, E.F. Mitophagy and Neuroprotection. Trends Mol. Med. 2020, 26, 8–20. [Google Scholar] [CrossRef] [PubMed]
- Cummins, N.; Tweedie, A.; Zuryn, S.; Bertran-Gonzalez, J.; Götz, J. Disease-associated tau impairs mitophagy by inhibiting Parkin translocation to mitochondria. EMBO J. 2019, 38, e99360. [Google Scholar] [CrossRef]
- Agarwal, S.; Yadav, A.; Chaturvedi, R.K. Peroxisome proliferator-activated receptors (PPARs) as therapeutic target in neurodegenerative disorders. Biochem. Biophys. Res. Commun. 2017, 483, 1166–1177. [Google Scholar] [CrossRef]
- Britti, E.; Delaspre, F.; Tamarit, J.; Ros, J. Mitochondrial calcium signalling and neurodegenerative diseases. Neuronal Signal. 2018, 2, NS20180061. [Google Scholar] [CrossRef] [Green Version]
- Hajieva, P.; Baeken, M.W.; Moosmann, B. The role of Plasma Membrane Calcium ATPases (PMCAs) in neurodegenerative disorders. Neurosci. Lett. 2018, 663, 29–38. [Google Scholar] [CrossRef]
- Wenk, G.L. Neuropathologic changes in Alzheimer’s disease: Potential targets for treatment. J. Clin. Psychiatry 2006, 67, 3–7. [Google Scholar] [PubMed]
- Fan, M.; Raymond, L. N-Methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington’s disease. Prog. Neurobiol. 2007, 81, 272–293. [Google Scholar] [CrossRef] [PubMed]
- Bonuccelli, U.; Del Dotto, P. New pharmacologic horizons in the treatment of Parkinson disease. Neurology 2006, 67, S30–S38. [Google Scholar] [CrossRef] [PubMed]
- Gauthier, S. Use of memantine to treat Alzheimer’s disease. Can. Med. Assoc. J. 2006, 175, 501–502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Y.; Lin, H.; Zhu, J.; Gu, K.; Li, Q.; He, S.; Lu, X.; Tan, R.; Pei, Y.; Wu, L.; et al. Design, synthesis, in vitro and in vivo evaluation of tacrine-cinnamic acid hybrids as multi-target acetyl- and butyrylcholinesterase inhibitors against Alzheimer’s disease. RSC Adv. 2017, 7, 33851–33867. [Google Scholar] [CrossRef] [Green Version]
- Hampel, H.; Mesulam, M.M.; Cuello, A.C.; Farlow, M.R.; Giacobini, E.; Grossberg, G.T.; Khachaturian, A.S.; Vergallo, A.; Cavedo, E.; Snyder, P.J.; et al. The cholinergic system in the pathophysiology and treatment of Alzheimer’s disease. Brain 2018, 141, 1917–1933. [Google Scholar] [CrossRef]
- Sharma, K. Cholinesterase inhibitors as Alzheimer’s therapeutics (Review). Mol. Med. Rep. 2019, 20, 1479–1487. [Google Scholar] [CrossRef] [Green Version]
- Hampel, H.; Mesulam, M.M.; Cuello, A.C.; Khachaturian, A.S.; Farlow, M.R.; Snyder, P.J.; Giacobini, E.; Khachaturian, Z.S. WITHDRAWN: Revisiting the cholinergic hypothesis in Alzheimer’s disease: Emerging evidence from translational and clinical research. Alzheimer’s Dement. 2017, 6, 1–14. [Google Scholar] [CrossRef]
- García-Ayllón, M.S.; Riba-Llena, I.; Serra-Basante, C.; Alom, J.; Boopathy, R.; Sáez-Valero, J. Altered levels of acetylcholinesterase in Alzheimer plasma. PLoS ONE 2010, 5, 0008701. [Google Scholar] [CrossRef] [Green Version]
- Gabriel, A.J.; Almeida, M.R.; Ribeiro, M.H.; Durães, J.; Tábuas-Pereira, M.; Pinheiro, A.C.; Pascoal, R.; Santana, I.; Baldeiras, I. Association between butyrylcholinesterase and cerebrospinal fluid biomarkers in Alzheimer’s disease patients. Neurosci. Lett. 2017, 641, 101–106. [Google Scholar] [CrossRef]
- Ayano, G. Dopamine: Receptors, Functions, Synthesis, Pathways, Locations and Mental Disorders: Review of Literatures. J. Ment. Disord. Treat. 2016, 2, 2–5. [Google Scholar] [CrossRef]
- Finberg, J.P.M. Update on the pharmacology of selective inhibitors of MAO-A and MAO-B: Focus on modulation of CNS monoamine neurotransmitter release. Pharmacol. Ther. 2014, 143, 133–152. [Google Scholar] [CrossRef] [PubMed]
- Noorulla, M. Histochemical localization of monoamine oxidase and glucose 6 phosphatase dehydrogenase and their probable role in guinea pigs with experimental allergic encephalomyelitis. Eur. J. Biomed. Pharm. Sci. 2017, 4, 470–479. [Google Scholar]
- Finberg, J.P.M.; Rabey, J.M. Inhibitors of MAO-A and MAO-B in psychiatry and neurology. Front. Pharmacol. 2016, 7, 340. [Google Scholar] [CrossRef] [Green Version]
- Riederer, P.; Müller, T. Monoamine oxidase-B inhibitors in the treatment of Parkinson’s disease: Clinical–pharmacological aspects. J. Neural Transm. 2018, 125, 1751–1757. [Google Scholar] [CrossRef]
- Alborghetti, M.; Nicoletti, F. Different Generations of Type-B Monoamine Oxidase Inhibitors in Parkinson’s Disease: From Bench to Bedside. Curr. Neuropharmacol. 2018, 17, 861–873. [Google Scholar] [CrossRef]
- Mishra, A.; Singh, S.; Shukla, S. Physiological and Functional Basis of Dopamine Receptors and Their Role in Neurogenesis: Possible Implication for Parkinson’s disease. J. Exp. Neurosci. 2018, 12, 1179069518779829. [Google Scholar] [CrossRef] [Green Version]
- Karrer, T.M.; Josef, A.K.; Mata, R.; Morris, E.D.; Samanez-Larkin, G.R. Reduced dopamine receptors and transporters but not synthesis capacity in normal aging adults: A meta-analysis. Neurobiol. Aging 2017, 57, 36–46. [Google Scholar] [CrossRef]
- Pan, X.; Kaminga, A.C.; Wen, S.W.; Wu, X.; Acheampong, K.; Liu, A. Dopamine and dopamine receptors in Alzheimer’s disease: A systematic review and network meta-analysis. Front. Aging Neurosci. 2019, 10, 175. [Google Scholar] [CrossRef] [Green Version]
- Lester, D.B.; Rogers, T.D.; Blaha, C.D. Acetylcholine-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci. Ther. 2010, 16, 137–162. [Google Scholar] [CrossRef]
- Tritsch, N.X.; Sabatini, B.L. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 2012, 76, 33–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hisahara, S.; Shimohama, S. Dopamine Receptors and Parkinson’s Disease. Int. J. Med. Chem. 2011, 2011, 403039. [Google Scholar] [CrossRef] [PubMed]
- Hassan, M.N.; Thakar, J.H. Dopamine receptors in Parkinson’s disease. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 1988, 12, 173–182. [Google Scholar] [CrossRef]
- Rowley, N.M.; Madsen, K.K.; Schousboe, A.; Steve White, H. Glutamate and GABA synthesis, release, transport and metabolism as targets for seizure control. Neurochem. Int. 2012, 61, 546–558. [Google Scholar] [CrossRef]
- A Rahn, K.; S Slusher, B.; I Kaplin, A. Glutamate in CNS Neurodegeneration and Cognition and its Regulation by GCPII Inhibition. Curr. Med. Chem. 2012, 19, 1335–1345. [Google Scholar] [CrossRef]
- Ribeiro, F.M.; Vieira, L.B.; Pires, R.G.W.; Olmo, R.P.; Ferguson, S.S.G. Metabotropic glutamate receptors and neurodegenerative diseases. Pharmacol. Res. 2017, 115, 179–191. [Google Scholar] [CrossRef]
- Fazio, F.; Ulivieri, M.; Volpi, C.; Gargaro, M.; Fallarino, F. Targeting metabotropic glutamate receptors for the treatment of neuroinflammation. Curr. Opin. Pharmacol. 2018, 38, 16–23. [Google Scholar] [CrossRef]
- Spampinato, S.F.; Copani, A.; Nicoletti, F.; Sortino, M.A.; Caraci, F. Metabotropic glutamate receptors in glial cells: A new potential target for neuroprotection? Front. Mol. Neurosci. 2018, 11, 414. [Google Scholar] [CrossRef] [Green Version]
- Twomey, E.C.; Yelshanskaya, M.V.; Grassucci, R.A.; Frank, J.; Sobolevsky, A.I. Channel opening and gating mechanism in AMPA-subtype glutamate receptors. Nature 2017, 549, 60–65. [Google Scholar] [CrossRef] [Green Version]
- Wang, Q.; Yu, S.; Simonyi, A.; Sun, G.Y.; Sun, A.Y. Kainic Acid-Mediated Excitotoxicity as a Model for Neurodegeneration. Mol. Neurobiol. 2005, 31, 003–016. [Google Scholar] [CrossRef]
- Shaye, H.; Ishchenko, A.; Lam, J.H.; Han, G.W.; Xue, L.; Rondard, P.; Pin, J.P.; Katritch, V.; Gati, C.; Cherezov, V. Structural basis of the activation of a metabotropic GABA receptor. Nature 2020, 584, 298–303. [Google Scholar] [CrossRef] [PubMed]
- Błaszczyk, J.W. Parkinson’s disease and neurodegeneration: GABA-collapse hypothesis. Front. Neurosci. 2016, 10, 269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luchetti, S.; Huitinga, I.; Swaab, D.F. Neurosteroid and GABA-A receptor alterations in Alzheimer’s disease, Parkinson’s disease and multiple sclerosis. Neuroscience 2011, 191, 6–21. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.S.; Yoon, B.-E. Altered GABAergic Signaling in Brain Disease at Various Stages of Life. Exp. Neurobiol. 2017, 26, 122–131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meldolesi, J. Neurotrophin receptors in the pathogenesis, diagnosis and therapy of neurodegenerative diseases. Pharmacol. Res. 2017, 121, 129–137. [Google Scholar] [CrossRef]
- Gupta, V.K.; You, Y.; Gupta, V.B.; Klistorner, A.; Graham, S.L. TrkB receptor signalling: Implications in neurodegenerative, psychiatric and proliferative disorders. Int. J. Mol. Sci. 2013, 14, 10122–10142. [Google Scholar] [CrossRef] [PubMed]
- Kowiański, P.; Lietzau, G.; Czuba, E.; Waśkow, M.; Steliga, A.; Moryś, J. BDNF: A Key Factor with Multipotent Impact on Brain Signaling and Synaptic Plasticity. Cell. Mol. Neurobiol. 2018, 38, 579–593. [Google Scholar] [CrossRef]
- Wang, Z.; Xiang, J.; Liu, X.; Yu, S.P.; Manfredsson, F.P.; Ivette, M.; Wu, S.; Wang, J.; Ye, K.; Rapids, G. Deficiency in BDNF/TrkB Neurotrophic Activity Stimulates δ- Secretase by Upregulating C/EBPβ in Alzheimer’s Disease Zhi-Hao. Cell Rep. 2019, 28, 655–669. [Google Scholar] [CrossRef] [Green Version]
- Sabaghi, A.; Heirani, A.; Mahmoodi, H.; Sabaghi, S. High-intensity interval training prevents cognitive-motor impairment and serum BDNF level reduction in parkinson mice model. Sport Sci. Health 2019, 15, 681–687. [Google Scholar] [CrossRef]
- Huang, Y.; Huang, C.; Yun, W. Peripheral BDNF/TrkB protein expression is decreased in Parkinson’s disease but not in Essential tremor. J. Clin. Neurosci. 2019, 63, 176–181. [Google Scholar] [CrossRef]
- Zhao, X.; Chen, X.Q.; Han, E.; Hu, Y.; Paik, P.; Ding, Z.; Overman, J.; Lau, A.L.; Shahmoradian, S.H.; Chiu, W.; et al. TRiC subunits enhance BDNF axonal transport and rescue striatal atrophy in Huntington’s disease. Proc. Natl. Acad. Sci. USA 2016, 113, 5655–5664. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okun, E.; Griffioen, K.J.; Lathia, J.D.; Tang, S.C.; Mattson, M.P.; Arumugam, T.V. Toll-like receptors in neurodegeneration. Brain Res. Rev. 2009, 59, 278–292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arroyo, D.S.; Soria, J.A.; Gaviglio, E.A.; Rodriguez-Galan, M.C.; Iribarren, P. Toll-like receptors are key players in neurodegeneration Daniela. Int. Immunopharmacol. 2011, 11, 1415–1421. [Google Scholar] [CrossRef] [Green Version]
- Momtazmanesh, S.; Perry, G.; Rezaei, N. Toll-like receptors in Alzheimer’s disease. J. Neuroimmunol. 2020, 348, 137–153. [Google Scholar] [CrossRef] [PubMed]
- Kouli, A.; Horne, C.B.; Williams-Gray, C.H. Toll-like receptors and their therapeutic potential in Parkinson’s disease and α-synucleinopathies. Brain. Behav. Immun. 2019, 81, 41–51. [Google Scholar] [CrossRef] [PubMed]
- Griffioen, K.; Mattson, M.P.; Okun, E. Deficiency of Toll-like receptors 2, 3 or 4 extends life expectancy in Huntington’s disease mice. Heliyon 2018, 4, e00508. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holdt, S.L.; Kraan, S. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 2011, 23, 543–597. [Google Scholar] [CrossRef]
- Bocanegra, A.; Bastida, S.; Benedí, J.; Ródenas, S.; Sánchez-Muniz, F.J. Characteristics and Nutritional and Cardiovascular-Health Properties of Seaweeds. J. Med. Food 2009, 12, 236–258. [Google Scholar] [CrossRef]
- Pereira, H.; Polo, C.; Rešek, E.; Engelen, A. Polyunsaturated Fatty Acids of Marine Macroalgae: Potential for Nutritional and Pharmaceutical Applications. Marine Drugs 2012, 10, 1920–1935. [Google Scholar] [CrossRef] [Green Version]
- Osório, C.; Machado, S.; Peixoto, J.; Bessada, S.; Pimentel, F.B.; Alves, R.C.; Oliveira, M.B.P.P. Pigments content (Chlorophylls, fucoxanthin and phycobiliproteins) of different commercial dried algae. Separations 2020, 7, 33. [Google Scholar] [CrossRef]
- Balboa, E.M.; Conde, E.; Moure, A.; Falqué, E.; Domínguez, H. In vitro antioxidant properties of crude extracts and compounds from brown algae. Food Chem. 2013, 138, 1764–1785. [Google Scholar] [CrossRef] [PubMed]
- Olasehinde, T.A.; Mabinya, L.V.; Olaniran, A.O.; Okoh, A.I. Chemical characterization of sulfated polysaccharides from Gracilaria gracilis and Ulva lactuca and their radical scavenging, metal chelating, and cholinesterase inhibitory activities. Int. J. Food Prop. 2019, 22, 100–110. [Google Scholar] [CrossRef] [Green Version]
- Rafiquzzaman, S.M.; Kim, E.Y.; Lee, J.M.; Mohibbullah, M.; Alam, M.B.; Soo Moon, I.; Kim, J.M.; Kong, I.S. Anti-Alzheimers and anti-inflammatory activities of a glycoprotein purified from the edible brown alga Undaria pinnatifida. Food Res. Int. 2015, 77, 118–124. [Google Scholar] [CrossRef]
- Lin, J.; Huang, L.; Yu, J.; Xiang, S.; Wang, J.; Zhang, J.; Yan, X.; Cui, W.; He, S.; Wang, Q. Fucoxanthin, a marine carotenoid, reverses scopolamine-induced cognitive impairments in mice and inhibits acetylcholinesterase in vitro. Mar. Drugs 2016, 14, 67. [Google Scholar] [CrossRef] [Green Version]
- Choi, J.S.; Haulader, S.; Karki, S.; Jung, H.J.; Kim, H.R.; Jung, H.A. Acetyl- and butyryl-cholinesterase inhibitory activities of the edible brown alga Eisenia bicyclis. Arch. Pharm. Res. 2015, 38, 1477–1487. [Google Scholar] [CrossRef]
- Fang, Z.; Jeong, S.Y.; Jung, H.A.; Choi, J.S.; Min, B.S.; Woo, M.H. Anticholinesterase and Antioxidant Constituents from Gloiopeltis furcata. Chem. Pharm. Bull. 2010, 58, 1236–1239. [Google Scholar] [CrossRef] [Green Version]
- Jung, H.A.; Ali, M.Y.; Choi, R.J.; Jeong, H.O.; Chung, H.Y.; Choi, J.S. Kinetics and molecular docking studies of fucosterol and fucoxanthin, BACE1 inhibitors from brown algae Undaria pinnatifida and Ecklonia stolonifera. Food Chem. Toxicol. 2016, 89, 104–111. [Google Scholar] [CrossRef]
- Jung, H.A.; Oh, S.H.; Choi, J.S. Molecular docking studies of phlorotannins from Eisenia bicyclis with BACE1 inhibitory activity. Bioorganic Med. Chem. Lett. 2010, 20, 3211–3215. [Google Scholar] [CrossRef]
- Lee, J.K.; Byun, H.G. A novel BACE inhibitor isolated from Eisenia bicyclis exhibits neuroprotective activity against β-amyloid toxicity. Fish. Aquat. Sci. 2018, 21, 38. [Google Scholar] [CrossRef] [Green Version]
- Jung, H.A.; Roy, A.; Choi, J.S. In vitro monoamine oxidase A and B inhibitory activity and molecular docking simulations of fucoxanthin. Fish. Sci. 2017, 83, 123–132. [Google Scholar] [CrossRef]
- Jung, H.A.; Roy, A.; Jung, J.H.; Choi, J.S. Evaluation of the inhibitory effects of eckol and dieckol isolated from edible brown alga Eisenia bicyclis on human monoamine oxidases A and B. Arch. Pharm. Res. 2017, 40, 480–491. [Google Scholar] [CrossRef] [PubMed]
- Seong, S.H.; Paudel, P.; Choi, J.W.; Ahn, D.H.; Nam, T.J.; Jung, H.A.; Choi, J.S. Probing multi-target action of phlorotannins as new monoamine oxidase inhibitors and dopaminergic receptor modulators with the potential for treatment of neuronal disorders. Mar. Drugs 2019, 17, 377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghazali, F.C.; Aroyehun, A.Q.B.; Razak, S.A. Acknowledging Sulfated Polysaccharides from Marine Macroalgae Multi- Functional Properties. Haya Saudi J. Life Sci. 2017, 2, 269–283. [Google Scholar] [CrossRef]
- Choi, J.I.; Kim, H.J.; Kim, J.H.; Byun, M.W.; Soo Chun, B.; Hyun Ahn, D.; Hwang, Y.J.; Kim, D.J.; Kim, G.H.; Lee, J.W. Application of gamma irradiation for the enhanced physiological properties of polysaccharides from seaweeds. Appl. Radiat. Isot. 2009, 67, 1277–1281. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Hu, S.; Nie, S.; Yu, Q.; Xie, M. Reviews on Mechanisms of In Vitro Antioxidant Activity of Polysaccharides. Oxid. Med. Cell. Longev. 2016, 2016, 5692852. [Google Scholar] [CrossRef] [Green Version]
- Nordgård, C.T.; Rao, S.V.; Draget, K.I. The potential of marine oligosaccharides in pharmacy. Bioact. Carbohydrates Diet. Fibre 2019, 18, 100178. [Google Scholar] [CrossRef]
- Ganesan, A.R.; Tiwari, U.; Rajauria, G. Seaweed nutraceuticals and their therapeutic role in disease prevention. Food Sci. Hum. Wellness 2019, 8, 252–263. [Google Scholar] [CrossRef]
- Fletcher, H.R.; Biller, P.; Ross, A.B.; Adams, J.M.M. The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res. 2017, 22, 79–86. [Google Scholar] [CrossRef] [Green Version]
- Saravana Guru, M.M.; Vasanthi, M.; Achary, A. Antioxidant and free radical scavenging potential of crude sulphated polysaccharides from Turbinaria ornata. Biologia 2015, 70, 27–33. [Google Scholar] [CrossRef]
- Zhang, Z.; Wang, X.; Mo, X.; Qi, H. Degradation and the antioxidant activity of polysaccharide from Enteromorpha linza. Carbohydr. Polym. 2013, 92, 2084–2087. [Google Scholar] [CrossRef]
- Pozharitskaya, O.N.; Obluchinskaya, E.D.; Shikov, A.N. Mechanisms of bioactivities of fucoidan from the brown seaweed fucus vesiculosus L. Of the barents sea. Mar. Drugs 2020, 18, 275. [Google Scholar] [CrossRef] [PubMed]
- Obluchinskaya, E.D.; Pozharitskaya, O.N.; Zakharov, D.V.; Flisyuk, E.V.; Terninko, I.I.; Generalova, Y.E.; Smekhova, I.E.; Shikov, A.N. The Biochemical Composition and Antioxidant Properties of Fucus vesiculosus from the Arctic Region. Mar. Drugs 2022, 20, 193. [Google Scholar] [CrossRef] [PubMed]
- Olasehinde, T.A.; Olaniran, A.O.; Okoh, A.I. Sulfated polysaccharides of some seaweeds exhibit neuroprotection via mitigation of oxidative stress, cholinergic dysfunction and inhibition of Zn—Induced neuronal damage in HT-22 cells. BMC Complement. Med. Ther. 2020, 20, 251. [Google Scholar] [CrossRef] [PubMed]
- Jin, W.; Zhang, W.; Wang, J.; Yao, J.; Xie, E.; Liu, D.; Duan, D.; Zhang, Q. A study of neuroprotective and antioxidant activities of heteropolysaccharides from six Sargassum species. Int. J. Biol. Macromol. 2014, 67, 336–342. [Google Scholar] [CrossRef]
- Liang, Z.; Liu, Z.; Sun, X.; Tao, M.; Xiao, X.; Yu, G.; Wang, X. The effect of fucoidan on cellular oxidative stress and the CATD-Bax signaling axis in MN9D cells damaged by 1-methyl-4-phenypyridinium. Front. Aging Neurosci. 2019, 11, 429. [Google Scholar] [CrossRef] [Green Version]
- Winslow, A.R.; Rubinsztein, D.C. Autophagy in neurodegeneration and development. Biochim. Biophys. Acta—Mol. Basis Dis. 2008, 1782, 723–729. [Google Scholar] [CrossRef]
- Liu, J.; Yang, L.; Tian, H.; Ma, Q. Cathepsin D is involved in the oxygen and glucose deprivation/reperfusion-induced apoptosis of astrocytes. Int. J. Mol. Med. 2016, 38, 1257–1263. [Google Scholar] [CrossRef]
- Hu, P.; Li, Z.; Chen, M.; Sun, Z.; Ling, Y.; Jiang, J.; Huang, C. Structural elucidation and protective role of a polysaccharide from Sargassum fusiforme on ameliorating learning and memory deficiencies in mice. Carbohydr. Polym. 2016, 139, 150–158. [Google Scholar] [CrossRef]
- Zhang, L.; Hao, J.; Zheng, Y.; Su, R.; Liao, Y.; Gong, X.; Liu, L.; Wang, X. Fucoidan protects dopaminergic neurons by enhancing the mitochondrial function in a rotenone-induced rat model of parkinson’s disease. Aging Dis. 2018, 9, 590–604. [Google Scholar] [CrossRef] [Green Version]
- Dinkova-Kostova, A.T.; Kostov, R.V.; Kazantsev, A.G. The role of Nrf2 signaling in counteracting neurodegenerative diseases. FEBS J. 2018, 285, 3576–3590. [Google Scholar] [CrossRef] [Green Version]
- Han, Y.S.; Lee, J.H.; Lee, S.H. Fucoidan suppresses mitochondrial dysfunction and cell death against 1-methyl-4-phenylpyridinum-induced neuronal cytotoxicity via regulation of PGC-1α expression. Mar. Drugs 2019, 17, 518. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peixoto, C.A.; de Oliveira, W.H.; da Racho Araújo, S.M.; Nunes, A.K.S. AMPK activation: Role in the signaling pathways of neuroinflammation and neurodegeneration. Exp. Neurol. 2017, 298, 31–41. [Google Scholar] [CrossRef] [PubMed]
- Park, H.Y.; Han, M.H.; Park, C.; Jin, C.Y.; Kim, G.Y.; Choi, I.W.; Kim, N.D.; Nam, T.J.; Kwon, T.K.; Choi, Y.H. Anti-inflammatory effects of fucoidan through inhibition of NF-κB, MAPK and Akt activation in lipopolysaccharide-induced BV2 microglia cells. Food Chem. Toxicol. 2011, 49, 1745–1752. [Google Scholar] [CrossRef] [PubMed]
- Peng, Z.; Luchtman, D.W.; Wang, X.; Zhang, Y.; Song, C. Activation of microglia synergistically enhances neurodegeneration caused by MPP+ in human SH-SY5Y cells. Eur. J. Pharmacol. 2019, 850, 64–74. [Google Scholar] [CrossRef]
- Alghazwi, M.; Smid, S.; Karpiniec, S.; Zhang, W. Comparative study on neuroprotective activities of fucoidans from Fucus vesiculosus and Undaria pinnatifida. Int. J. Biol. Macromol. 2019, 122, 255–264. [Google Scholar] [CrossRef]
- Wang, X.; Yi, K.; Zhao, Y. Fucoidan inhibits amyloid-β-induced toxicity in transgenic: Caenorhabditis elegans by reducing the accumulation of amyloid-β and decreasing the production of reactive oxygen species. Food Funct. 2018, 9, 552–560. [Google Scholar] [CrossRef]
- Wei, H.; Gao, Z.; Zheng, L.; Zhang, C.; Liu, Z.; Yang, Y.; Teng, H.; Hou, L.; Yin, Y.; Zou, X. Protective effects of fucoidan on Aβ25-35 and D-gal-induced neurotoxicity in PC12 cells and D-gal-induced cognitive dysfunction in mice. Mar. Drugs 2017, 15, 77. [Google Scholar] [CrossRef] [Green Version]
- Kim, H.; Ahn, J.H.; Song, M.; Kim, D.W.; Lee, T.K.; Lee, J.C.; Kim, Y.M.; Kim, J.D.; Cho, J.H.; Hwang, I.K.; et al. Pretreated fucoidan confers neuroprotection against transient global cerebral ischemic injury in the gerbil hippocampal CA1 area via reducing of glial cell activation and oxidative stress. Biomed. Pharmacother. 2019, 109, 1718–1727. [Google Scholar] [CrossRef]
- Ahn, J.H.; Shin, M.C.; Kim, D.W.; Kim, H.; Song, M.; Lee, T.K.; Lee, J.C.; Kim, H.; Cho, J.H.; Kim, Y.M.; et al. Antioxidant properties of fucoidan alleviate acceleration and exacerbation of hippocampal neuronal death following transient global cerebral ischemia in high-fat diet-induced obese gerbils. Int. J. Mol. Sci. 2019, 20, 554. [Google Scholar] [CrossRef] [Green Version]
- Hsieh, C.H.; Lu, C.H.; Kuo, Y.Y.; Lin, G.B.; Chao, C.Y. The protective effect of non-invasive low intensity pulsed electric field and fucoidan in preventing oxidative stress-induced motor neuron death via ROCK/Akt pathway. PLoS ONE 2019, 14, e0214100. [Google Scholar] [CrossRef]
- Huang, C.Y.; Kuo, C.H.; Chen, P.W. Compressional-puffing pretreatment enhances neuroprotective effects of fucoidans from the brown seaweed sargassum hemiphyllum on 6-hydroxydopamine-induced apoptosis in SH-SY5Y cells. Molecules 2018, 23, 78. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Hou, Y.; Duan, D.; Zhang, Q. The structure and nephroprotective activity of oligo-porphyran on glycerol-induced acute renal failure in rats. Mar. Drugs 2017, 15, 135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.; Geng, L.; Zhang, J.; Wang, J.; Zhang, Q.; Duan, D.; Zhang, Q. Oligo-porphyran ameliorates neurobehavioral deficits in parkinsonian mice by regulating the PI3K/Akt/Bcl-2 pathway. Mar. Drugs 2018, 16, 82. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rai, S.N.; Dilnashin, H.; Birla, H.; Singh, S.S.; Zahra, W.; Rathore, A.S.; Singh, B.K.; Singh, S.P. The Role of PI3K/Akt and ERK in Neurodegenerative Disorders. Neurotox. Res. 2019, 35, 775–795. [Google Scholar] [CrossRef] [PubMed]
- Souza, R.B.; Frota, A.F.; Sousa, R.S.; Cezario, N.A.; Santos, T.B.; Souza, L.M.F.; Coura, C.O.; Monteiro, V.S.; Cristino Filho, G.; Vasconcelos, S.M.M.; et al. Neuroprotective Effects of Sulphated Agaran from Marine Alga Gracilaria cornea in Rat 6-Hydroxydopamine Parkinson’s Disease Model: Behavioural, Neurochemical and Transcriptional Alterations. Basic Clin. Pharmacol. Toxicol. 2017, 120, 159–170. [Google Scholar] [CrossRef]
- Souza, R.B.; Frota, A.F.; Silva, J.; Alves, C.; Neugebauer, A.Z.; Pinteus, S.; Rodrigues, J.A.G.; Cordeiro, E.M.S.; de Almeida, R.R.; Pedrosa, R.; et al. In vitro activities of kappa-carrageenan isolated from red marine alga Hypnea musciformis: Antimicrobial, anticancer and neuroprotective potential. Int. J. Biol. Macromol. 2018, 112, 1248–1256. [Google Scholar] [CrossRef]
- Kidgell, J.T.; Magnusson, M.; de Nys, R.; Glasson, C.R.K. Ulvan: A systematic review of extraction, composition and function. Algal Res. 2019, 39, 101422. [Google Scholar] [CrossRef]
- Kadam, S.U.; Tiwari, B.K.; O’Donnell, C.P. Extraction, structure and biofunctional activities of laminarin from brown algae. Int. J. Food Sci. Technol. 2015, 50, 24–31. [Google Scholar] [CrossRef]
- Park, J.H.; Ahn, J.H.; Lee, T.K.; Park, C.W.; Kim, B.; Lee, J.C.; Kim, D.W.; Shin, M.C.; Cho, J.H.; Lee, C.H.; et al. Laminarin pretreatment provides neuroprotection against forebrain ischemia/reperfusion injury by reducing oxidative stress and neuroinflammation in aged gerbils. Mar. Drugs 2020, 18, 213. [Google Scholar] [CrossRef] [Green Version]
- Lee, T.K.; Ahn, J.H.; Park, C.W.; Kim, B.; Park, Y.E.; Lee, J.C.; Park, J.H.; Yang, G.E.; Shin, M.C.; Cho, J.H.; et al. Pre-treatment with laminarin protects hippocampal CA1 pyramidal neurons and attenuates reactive gliosis following transient forebrain ischemia in gerbils. Mar. Drugs 2020, 18, 52. [Google Scholar] [CrossRef] [Green Version]
- Zhou, R.; Shi, X.Y.; Bi, D.C.; Fang, W.S.; Wei, G.B.; Xu, X. Alginate-derived oligosaccharide inhibits neuroinflammation and promotes microglial phagocytosis of β-amyloid. Mar. Drugs 2015, 13, 5828–5846. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hung, C.C.; Lin, C.H.; Chang, H.; Wang, C.Y.; Lin, S.H.; Hsu, P.C.; Sun, Y.Y.; Lin, T.N.; Shie, F.S.; Kao, L.S.; et al. Astrocytic GAP43 induced by the TLR4/NF-κB/STAT3 axis attenuates astrogliosis-mediated microglial activation and neurotoxicity. J. Neurosci. 2016, 36, 2027–2043. [Google Scholar] [CrossRef] [PubMed]
- Bi, D.; Li, X.; Li, T.; Li, X.; Lin, Z.; Yao, L.; Li, H.; Xu, H.; Hu, Z.; Zhang, Z.; et al. Characterization and Neuroprotection Potential of Seleno-Polymannuronate. Front. Pharmacol. 2020, 11, 21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Das, B.; Yan, R. Role of BACE1 in Alzheimer’s synaptic function. Transl. Neurodegener. 2017, 6, 4–11. [Google Scholar] [CrossRef]
- Mohd Fauziee, N.A.; Chang, L.S.; Wan Mustapha, W.A.; Md Nor, A.R.; Lim, S.J. Functional polysaccharides of fucoidan, laminaran and alginate from Malaysian brown seaweeds (Sargassum polycystum, Turbinaria ornata and Padina boryana). Int. J. Biol. Macromol. 2021, 167, 1135–1145. [Google Scholar] [CrossRef]
- Hu, J.; Geng, M.; Li, J.; Xin, X.; Wang, J.; Tang, M.; Zhang, J.; Zhang, X.; Ding, J. Acidic Oligosaccharide Sugar Chain, a Marine-Derived Acidic Oligosaccharide, Inhibits the Cytotoxicity and Aggregation of Amyloid Beta Protein. J. Pharmacol. Sci. 2004, 95, 248–255. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Sun, G.; Feng, T.; Zhang, J.; Huang, X.; Wang, T.; Xie, Z.; Chu, X.; Yang, J.; Wang, H.; et al. Sodium oligomannate therapeutically remodels gut microbiota and suppresses gut bacterial amino acids-shaped neuroinflammation to inhibit Alzheimer’s disease progression. Cell Res. 2019, 29, 787. [Google Scholar] [CrossRef]
- Harnedy, P.A.; Fitzgerald, R.J. Bioactive proteins, peptides, and amino acids from macroalgae. J. Phycol. 2011, 47, 218–232. [Google Scholar] [CrossRef]
- Katayama, S.; Nakamura, S. Emerging roles of bioactive peptides on brain health promotion. Int. J. Food Sci. Technol. 2019, 54, 1949–1955. [Google Scholar] [CrossRef] [Green Version]
- Hernández-Benítez, R.; Vangipuram, S.D.; Ramos-Mandujano, G.; Lyman, W.D.; Pasantes-Morales, H. Taurine enhances the growth of neural precursors derived from fetal human brain and promotes neuronal specification. Dev. Neurosci. 2013, 35, 40–49. [Google Scholar] [CrossRef]
- Mohibbullah, M.; Bhuiyan, M.M.H.; Hannan, M.A.; Getachew, P.; Hong, Y.K.; Choi, J.S.; Choi, I.S.; Moon, I.S. The Edible Red Alga Porphyra yezoensis Promotes Neuronal Survival and Cytoarchitecture in Primary Hippocampal Neurons. Cell. Mol. Neurobiol. 2016, 36, 669–682. [Google Scholar] [CrossRef] [PubMed]
- Pangestuti, R.; Kim, S.K. Marine-derived bioactive materials for neuroprotection. Food Sci. Biotechnol. 2013, 22, 1–12. [Google Scholar] [CrossRef]
- Cotas, J.; Leandro, A.; Pacheco, D.; Gonçalves, A.M.M.; Pereira, L. A Comprehensive Review of the Nutraceutical and Therapeutic Applications of Red Seaweeds (Rhodophyta). Life 2020, 10, 19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kazir, M.; Abuhassira, Y.; Robin, A.; Nahor, O.; Luo, J.; Israel, A.; Golberg, A.; Livney, Y.D. Extraction of proteins from two marine macroalgae, Ulva sp. and Gracilaria sp., for food application, and evaluating digestibility, amino acid composition and antioxidant properties of the protein concentrates. Food Hydrocoll. 2019, 87, 194–203. [Google Scholar] [CrossRef]
- Øverland, M.; Mydland, L.T.; Skrede, A. Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. J. Sci. Food Agric. 2019, 99, 13–24. [Google Scholar] [CrossRef] [Green Version]
- Ripps, H.; Shen, W. Review: Taurine: A “very essential” amino acid. Mol. Vis. 2012, 18, 2673–2686. [Google Scholar]
- Li, X.W.; Gao, H.Y.; Liu, J. The role of taurine in improving neural stem cells proliferation and differentiation. Nutr. Neurosci. 2017, 20, 409–415. [Google Scholar] [CrossRef]
- Garcia-Vaquero, M.; Hayes, M. Red and green macroalgae for fish and animal feed and human functional food development. Food Rev. Int. 2016, 32, 15–45. [Google Scholar] [CrossRef]
- Che, Y.; Hou, L.; Sun, F.; Zhang, C.; Liu, X.; Piao, F.; Zhang, D.; Li, H.; Wang, Q. Taurine protects dopaminergic neurons in a mouse Parkinson’s disease model through inhibition of microglial M1 polarization. Cell Death Dis. 2018, 9, 435. [Google Scholar] [CrossRef] [Green Version]
- Hou, L.; Che, Y.; Sun, F.; Wang, Q. Taurine protects noradrenergic locus coeruleus neurons in a mouse Parkinson’s disease model by inhibiting microglial M1 polarization. Amino Acids 2018, 50, 547–556. [Google Scholar] [CrossRef]
- Tang, Y.; Le, W. Differential Roles of M1 and M2 Microglia in Neurodegenerative Diseases. Mol. Neurobiol. 2016, 53, 1181–1194. [Google Scholar] [CrossRef] [PubMed]
- Terriente-Palacios, C.; Castellari, M. Levels of taurine, hypotaurine and homotaurine, and amino acids profiles in selected commercial seaweeds, microalgae, and algae-enriched food products. Food Chem. 2022, 368, 130770. [Google Scholar] [CrossRef] [PubMed]
- Manzano, S.; Agüera, L.; Aguilar, M.; Olazarán, J. A Review on Tramiprosate (Homotaurine) in Alzheimer’s Disease and Other Neurocognitive Disorders. Front. Neurol. 2020, 11, 614. [Google Scholar] [CrossRef] [PubMed]
- Caltagirone, C.; Ferrannini, L.; Marchionni, N.; Nappi, G.; Scapagnini, G.; Trabucchi, M. The potential protective effect of tramiprosate (homotaurine) against Alzheimer’s disease: A review. Aging Clin. Exp. Res. 2012, 24, 580–587. [Google Scholar]
- Bellia, F.; Vecchio, G.; Rizzarelli, E. Carnosine derivatives: New multifunctional drug-like molecules. Amino Acids 2012, 43, 153–163. [Google Scholar] [CrossRef]
- Ouyang, L.; Tian, Y.; Bao, Y.; Xu, H.; Cheng, J.; Wang, B.; Shen, Y.; Chen, Z.; Lyu, J. Carnosine decreased neuronal cell death through targeting glutamate system and astrocyte mitochondrial bioenergetics in cultured neuron/astrocyte exposed to OGD/recovery. Brain Res. Bull. 2016, 124, 76–84. [Google Scholar] [CrossRef]
- Xie, R.X.; Li, D.W.; Liu, X.C.; Yang, M.F.; Fang, J.; Sun, B.L.; Zhang, Z.Y.; Yang, X. yi Carnosine Attenuates Brain Oxidative Stress and Apoptosis After Intracerebral Hemorrhage in Rats. Neurochem. Res. 2017, 42, 541–551. [Google Scholar] [CrossRef]
- Pawlik-Skowrońska, B.; Pirszel, J.; Brown, M.T. Concentrations of phytochelatins and glutathione found in natural assemblages of seaweeds depend on species and metal concentrations of the habitat. Aquat. Toxicol. 2007, 83, 190–199. [Google Scholar] [CrossRef]
- Ulrich, K.; Jakob, U. The role of thiols in antioxidant systems. Free Radic. Biol. Med. 2019, 140, 14–27. [Google Scholar] [CrossRef]
- Aoyama, K.; Nakaki, T. Glutathione in Cellular Redox Homeostasis: Association with the Excitatory Amino Acid Carrier 1 (EAAC1). Molecules 2015, 20, 8742–8758. [Google Scholar] [CrossRef] [Green Version]
- Gould, R.L.; Pazdro, R. Impact of supplementary amino acids, micronutrients, and overall diet on glutathione homeostasis. Nutrients 2019, 11, 1056. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, B.L.; Norhaizan, M.E.; Liew, W.P.P.; Rahman, H.S. Antioxidant and oxidative stress: A mutual interplay in age-related diseases. Front. Pharmacol. 2018, 9, 1162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harnedy, P.A.; O’Keeffe, M.B.; FitzGerald, R.J. Fractionation and identification of antioxidant peptides from an enzymatically hydrolysed Palmaria palmata protein isolate. Food Res. Int. 2017, 100, 416–422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, X.; Cao, D.; Sun, X.; Sun, S.; Xu, N. Preparation and identification of antioxidant peptides from protein hydrolysate of marine alga Gracilariopsis lemaneiformis. J. Appl. Phycol. 2019, 31, 2585–2596. [Google Scholar] [CrossRef]
- Lee, H.A.; Kim, I.H.; Nam, T.J. Bioactive peptide from Pyropia yezoensis and its anti-inflammatory activities. Int. J. Mol. Med. 2015, 36, 1701–1706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agirbasli, Z.; Cavas, L. In silico evaluation of bioactive peptides from the green algae Caulerpa. J. Appl. Phycol. 2017, 29, 1635–1646. [Google Scholar] [CrossRef]
- Park, H.Y.; Han, M.H.; Kim, G.Y.; Kim, N.D.; Nam, T.J.; Choi, Y.H. Inhibitory Effects of Glycoprotein Isolated fromLaminaria japonicaon Lipopolysaccharide-Induced Pro-Inflammatory Mediators in BV2 Microglial Cells. J. Food Sci. 2011, 76, 156–162. [Google Scholar] [CrossRef]
- Shahidi, F.; Ambigaipalan, P. Omega-3 Polyunsaturated Fatty Acids and Their Health Benefits. Annu. Rev. Food Sci. Technol. 2018, 9, 345–381. [Google Scholar] [CrossRef]
- Shanab, S.M.M.; Hafez, R.M.; Fouad, A.S. A review on algae and plants as potential source of arachidonic acid. J. Adv. Res. 2018, 11, 3–13. [Google Scholar] [CrossRef]
- Layé, S.; Nadjar, A.; Joffre, C.; Bazinet, R.P. Anti-inflammatory effects of omega-3 fatty acids in the brain: Physiological mechanisms and relevance to pharmacology. Pharmacol. Rev. 2018, 70, 12–38. [Google Scholar] [CrossRef]
- Lange, K.W.; Hauser, J.; Lange, K.M.; Makulska-Gertruda, E.; Nakamura, Y.; Reissmann, A.; Sakaue, Y.; Takano, T.; Takeuchi, Y. The Role of Nutritional Supplements in the Treatment of ADHD: What the Evidence Says. Curr. Psychiatry Rep. 2017, 19, 8. [Google Scholar] [CrossRef] [PubMed]
- Van Ginneken, V.J.T.; Helsper, J.P.F.G.; De Visser, W.; Van Keulen, H.; Brandenburg, W.A. Polyunsaturated fatty acids in various macroalgal species from north Atlantic and tropical seas. Lipids Health Dis. 2011, 10, 4–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Biancarosa, I.; Belghit, I.; Bruckner, C.G.; Liland, N.S.; Waagbø, R.; Amlund, H.; Heesch, S.; Lock, E.J. Chemical characterization of 21 species of marine macroalgae common in Norwegian waters: Benefits of and limitations to their potential use in food and feed. J. Sci. Food Agric. 2018, 98, 2035–2042. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Da Costa, E.; Domingues, P.; Melo, T.; Coelho, E.; Pereira, R.; Calado, R.; Abreu, M.H.; Domingues, M.R. Lipidomic signatures reveal seasonal shifts on the relative abundance of high-valued lipids from the brown algae fucus vesiculosus. Mar. Drugs 2019, 17, 335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, Y.-Q.; Dang, R.-L.; Tang, M.-M.; Cai, H.-L.; Li, H.-D.; Liao, D.-H.; He, X.; Cao, L.-J.; Xue, Y.; Jiang, P. Long Chain Omega-3 Polyunsaturated Fatty Acid Supplementation Alleviates Doxorubicin-Induced Depressive-Like Behaviors and Neurotoxicity in Rats: Involvement of Oxidative Stress and Neuroinflammation. Nutrients 2016, 8, 243. [Google Scholar] [CrossRef] [Green Version]
- Devassy, J.G.; Leng, S.; Gabbs, M.; Monirujjaman, M.; Aukema, H.M. Omega-3 Polyunsaturated Fatty Acids and Oxylipins in Neuroinflammation and Management of Alzheimer Disease. Adv. Nutr. 2016, 7, 905–916. [Google Scholar] [CrossRef]
- Scaioli, E.; Liverani, E.; Belluzzi, A. The Imbalance between n-6/n-3 Polyunsaturated Fatty Acids and Inflammatory Bowel Disease: A Comprehensive Review and Future Therapeutic Perspectives. Int. J. Mol. Sci. 2017, 18, 2619. [Google Scholar] [CrossRef] [Green Version]
- Dong, Y.; Xu, M.; Kalueff, A.V.; Song, C. Dietary eicosapentaenoic acid normalizes hippocampal omega-3 and 6 polyunsaturated fatty acid profile, attenuates glial activation and regulates BDNF function in a rodent model of neuroinflammation induced by central interleukin-1β administration. Eur. J. Nutr. 2018, 57, 1781–1791. [Google Scholar] [CrossRef]
- Huang, T.L.; Wen, Y.T.; Ho, Y.C.; Wang, J.K.; Lin, K.H.; Tsai, R.K. Algae oil treatment protects retinal ganglion cells (RGCs) via ERK signaling pathway in experimental optic nerve ischemia. Mar. Drugs 2020, 18, 83. [Google Scholar] [CrossRef] [Green Version]
- Clementi, M.E.; Lazzarino, G.; Sampaolese, B.; Brancato, A.; Tringali, G. DHA protects PC12 cells against oxidative stress and apoptotic signals through the activation of the NFE2L2/HO-1 axis. Int. J. Mol. Med. 2019, 43, 2523–2531. [Google Scholar] [CrossRef]
- Vaamonde-Garcia, C.; Courties, A.; Pigenet, A.; Laiguillon, M.C.; Sautet, A.; Houard, X.; Kerdine-Römer, S.; Meijide, R.; Berenbaum, F.; Sellam, J. The nuclear factor-erythroid 2-related factor/heme oxygenase-1 axis is critical for the inflammatory features of type 2 diabetes–associated osteoarthritis. J. Biol. Chem. 2017, 292, 14505–14515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Habtemariam, S. The Nrf2/HO-1 Axis as Targets for Flavanones: Neuroprotection by Pinocembrin, Naringenin, and Eriodictyol. Oxid. Med. Cell. Longev. 2019, 2019, 4724920. [Google Scholar] [CrossRef] [PubMed]
- de Oliveira Souza, A.; Couto-Lima, C.A.; Catalão, C.H.R.; Santos-Júnior, N.N.; dos Santos, J.F.; da Rocha, M.J.A.; Alberici, L.C. Neuroprotective action of Eicosapentaenoic (EPA) and Docosahexaenoic (DHA) acids on Paraquat intoxication in Drosophila melanogaster. Neurotoxicology 2019, 70, 154–160. [Google Scholar] [CrossRef] [PubMed]
- Cutuli, D.; de Bartolo, P.; Caporali, P.; Laricchiuta, D.; Foti, F.; Ronci, M.; Rossi, C.; Neri, C.; Spalletta, G.; Caltagirone, C.; et al. N-3 Polyunsaturated Fatty Acids Supplementation Enhances Hippocampal Functionality in Aged Mice. Front. Aging Neurosci. 2014, 6, 220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohibbullah, M.; Hannan, M.A.; Choi, J.Y.; Bhuiyan, M.M.H.; Hong, Y.K.; Choi, J.S.; Choi, I.S.; Moon, I.S. The Edible Marine Alga Gracilariopsis chorda Alleviates Hypoxia/Reoxygenation-Induced Oxidative Stress in Cultured Hippocampal Neurons. J. Med. Food 2015, 18, 960–971. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schain, M.; Kreisl, W.C. Neuroinflammation in Neurodegenerative Disorders—A Review. Curr. Neurol. Neurosci. Rep. 2017, 17, 25. [Google Scholar] [CrossRef]
- Pangestuti, R.; Kim, S.K. Biological activities and health benefit effects of natural pigments derived from marine algae. J. Funct. Foods 2011, 3, 255–266. [Google Scholar] [CrossRef]
- Saluri, M.; Kaldmäe, M.; Tuvikene, R. Extraction and quantification of phycobiliproteins from the red alga Furcellaria lumbricalis. Algal Res. 2019, 37, 115–123. [Google Scholar] [CrossRef]
- Lee, D.; Nishizawa, M.; Shimizu, Y.; Saeki, H. Anti-inflammatory effects of dulse (Palmaria palmata) resulting from the simultaneous water-extraction of phycobiliproteins and chlorophyll a. Food Res. Int. 2017, 100, 514–521. [Google Scholar] [CrossRef]
- Macedo, D.; Bertolin, T.E.; Oro, T.; Backes, L.T.H.; Brás, I.C.; Santos, C.N.; Tenreiro, S.; Outeiro, T.F. Phycocyanin protects against Alpha-Synuclein toxicity in yeast. J. Funct. Foods 2017, 38, 553–560. [Google Scholar] [CrossRef]
- Mohibbullah, M.; Haque, M.N.; Khan, M.N.A.; Park, I.S.; Moon, I.S.; Hong, Y.K. Neuroprotective effects of fucoxanthin and its derivative fucoxanthinol from the phaeophyte Undaria pinnatifida attenuate oxidative stress in hippocampal neurons. J. Appl. Phycol. 2018, 30, 3243–3252. [Google Scholar] [CrossRef]
- Xiang, S.; Liu, F.; Lin, J.; Chen, H.; Huang, C.; Chen, L.; Zhou, Y.; Ye, L.; Zhang, K.; Jin, J.; et al. Fucoxanthin Inhibits β-Amyloid Assembly and Attenuates β-Amyloid Oligomer-Induced Cognitive Impairments. J. Agric. Food Chem. 2017, 65, 4092–4102. [Google Scholar] [CrossRef] [PubMed]
- Baek, S.Y.; Kim, M.R. Neuroprotective Effect of Carotenoid-Rich Enteromorpha prolifera Extract via TrkB/Akt Pathway against Oxidative Stress in Hippocampal Neuronal Cells. Mar. Drugs 2020, 18, 372. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.; Yu, J.; Zhao, J.; Zhang, K.; Zheng, J.; Wang, J.; Huang, C.; Zhang, J.; Yan, X.; Gerwick, W.H.; et al. Fucoxanthin, a Marine Carotenoid, Attenuates β-Amyloid Oligomer-Induced Neurotoxicity Possibly via Regulating the PI3K/Akt and the ERK Pathways in SH-SY5Y Cells. Oxid. Med. Cell. Longev. 2017, 2017, 6792543. [Google Scholar] [CrossRef] [Green Version]
- Yu, J.; Lin, J.-J.; Yu, R.; He, S.; Wang, Q.-W.; Cui, W.; Zhang, J.-R. Fucoxanthin prevents H2O2-induced neuronal apoptosis via concurrently activating the PI3-K/Akt cascade and inhibiting the ERK pathway. Food Nutr. Res. 2017, 61, 1304678. [Google Scholar] [CrossRef] [Green Version]
- Krishnaraj, R.N.; Kumari, S.S.S.; Mukhopadhyay, S.S. Antagonistic molecular interactions of photosynthetic pigments with molecular disease targets: A new approach to treat AD and ALS. J. Recept. Signal Transduct. 2016, 36, 67–71. [Google Scholar] [CrossRef]
- Goldshmit, Y.; Spanevello, M.D.; Tajouri, S.; Li, L.; Rogers, F.; Pearse, M.; Galea, M.; Bartlett, P.F.; Boyd, A.W.; Turnley, A.M. EphA4 blockers promote axonal regeneration and functional recovery following spinal cord injury in mice. PLoS ONE 2011, 6, e0024636. [Google Scholar] [CrossRef] [Green Version]
- Shukla, S.; Tekwani, B.L. Histone Deacetylases Inhibitors in Neurodegenerative Diseases, Neuroprotection and Neuronal Differentiation. Front. Pharmacol. 2020, 11, 537. [Google Scholar] [CrossRef]
- Nisar, N.; Li, L.; Lu, S.; Khin, N.C.; Pogson, B.J. Carotenoid metabolism in plants. Mol. Plant 2015, 8, 68–82. [Google Scholar] [CrossRef] [Green Version]
- Maoka, T. Carotenoids in marine animals. Mar. Drugs 2011, 9, 278–293. [Google Scholar] [CrossRef]
- Christaki, E.; Bonos, E.; Giannenas, I.; Florou-Paneri, P. Functional properties of carotenoids originating from algae. J. Sci. Food Agric. 2013, 93, 5–11. [Google Scholar] [CrossRef] [PubMed]
- Yatsunami, R.; Ando, A.; Yang, Y.; Takaichi, S.; Kohno, M.; Matsumura, Y.; Ikeda, H.; Fukui, T.; Nakasone, K.; Fujita, N.; et al. Identification of carotenoids from the extremely halophilic archaeon Haloarcula japonica. Front. Microbiol. 2014, 5, 100. [Google Scholar] [CrossRef] [PubMed]
- Lakey-Beitia, J.; Jagadeesh Kumar, D.; Hegde, M.L.; Rao, K.S. Carotenoids as novel therapeutic molecules against neurodegenerative disorders: Chemistry and molecular docking analysis. Int. J. Mol. Sci. 2019, 20, 5553. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mein, J.R.; Dolnikowski, G.G.; Ernst, H.; Russell, R.M.; Wang, X.D. Enzymatic formation of apo-carotenoids from the xanthophyll carotenoids lutein, zeaxanthin and β-cryptoxanthin by ferret carotene-9′,10′-monooxygenase. Arch. Biochem. Biophys. 2011, 506, 109–121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Novoveská, L.; Ross, M.E.; Stanley, M.S.; Pradelles, R.; Wasiolek, V.; Sassi, J.F. Microalgal carotenoids: A review of production, current markets, regulations, and future direction. Mar. Drugs 2019, 17, 640. [Google Scholar] [CrossRef] [Green Version]
- Del Campo, J.A.; García-González, M.; Guerrero, M.G. Outdoor cultivation of microalgae for carotenoid production: Current state and perspectives. Appl. Microbiol. Biotechnol. 2007, 74, 1163–1174. [Google Scholar] [CrossRef]
- Toti, E.; Chen, C.-Y.O.; Palmery, M.; Villaño Valencia, D.; Peluso, I. Non-Provitamin A and Provitamin A Carotenoids as Immunomodulators: Recommended Dietary Allowance, Therapeutic Index, or Personalized Nutrition? Oxid. Med. Cell. Longev. 2018, 2018, 4637861. [Google Scholar] [CrossRef]
- Chuyen, H.V.; Eun, J.-B. Marine carotenoids: Bioactivities and potential benefits to human health. Crit. Rev. Food Sci. Nutr. 2017, 57, 2600–2610. [Google Scholar] [CrossRef]
- Shaish, A.; Harari, A.; Kamari, Y.; Soudant, E.; Harats, D.; Ben-Amotz, A. A carotenoid algal preparation containing phytoene and phytofluene inhibited LDL oxidation in vitro. Plant Foods Hum. Nutr. 2008, 63, 83–86. [Google Scholar] [CrossRef]
- Linnewiel-Hermoni, K.; Khanin, M.; Danilenko, M.; Zango, G.; Amosi, Y.; Levy, J.; Sharoni, Y. The anti-cancer effects of carotenoids and other phytonutrients resides in their combined activity. Arch. Biochem. Biophys. 2015, 572, 28–35. [Google Scholar] [CrossRef]
- Cho, K.S.; Shin, M.; Kim, S.; Lee, S.B. Recent Advances in Studies on the Therapeutic Potential of Dietary Carotenoids in Neurodegenerative Diseases. Oxid. Med. Cell. Longev. 2018, 2018, 4120458. [Google Scholar] [CrossRef] [PubMed]
- Galasso, C.; Orefice, I.; Pellone, P.; Cirino, P.; Miele, R.; Ianora, A.; Brunet, C.; Sansone, C. On the neuroprotective role of astaxanthin: New perspectives? Mar. Drugs 2018, 16, 247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pangestuti, R.; Wibowo, S. Prospects and Health Promoting Effects of Brown Algal-derived Natural Pigments. Squalen Bull. Mar. Fish. Postharvest Biotechnol. 2013, 8, 37. [Google Scholar] [CrossRef] [Green Version]
- Hira, S.; Saleem, U.; Anwar, F.; Sohail, M.F.; Raza, Z.; Ahmad, B. β-Carotene: A Natural Compound Improves Cognitive Impairment and Oxidative Stress in a Mouse Model of Streptozotocin-Induced Alzheimer’s Disease. Biomolecules 2019, 9, 441. [Google Scholar] [CrossRef] [Green Version]
- Min, J.Y.; Min, K.B. Serum lycopene, lutein and zeaxanthin, and the risk of Alzheimer’s disease mortality in older adults. Dement. Geriatr. Cogn. Disord. 2014, 37, 246–256. [Google Scholar] [CrossRef] [PubMed]
- Jung, H.A.; Islam, M.N.; Lee, C.M.; Jeong, H.O.; Chung, H.Y.; Woo, H.C.; Choi, J.S. Promising antidiabetic potential of fucoxanthin isolated from the edible brown algae Eisenia bicyclis and Undaria pinnatifida. Fish. Sci. 2012, 78, 1321–1329. [Google Scholar] [CrossRef]
- Peng, J.; Yuan, J.P.; Wu, C.F.; Wang, J.H. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: Metabolism and bioactivities relevant to human health. Mar. Drugs 2011, 9, 1806–1828. [Google Scholar] [CrossRef]
- Sachindra, N.M.; Sato, E.; Maeda, H.; Hosokawa, M.; Niwano, Y.; Kohno, M.; Miyashita, K. Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J. Agric. Food Chem. 2007, 55, 8516–8522. [Google Scholar] [CrossRef]
- Zhang, L.; Wang, H.; Fan, Y.; Gao, Y.; Li, X.; Hu, Z.; Ding, K.; Wang, Y.; Wang, X. Fucoxanthin provides neuroprotection in models of traumatic brain injury via the Nrf2-ARE and Nrf2-autophagy pathways. Sci. Rep. 2017, 7, 46763. [Google Scholar] [CrossRef] [Green Version]
- Hu, L.; Chen, W.; Tian, F.; Yuan, C.; Wang, H.; Yue, H. Neuroprotective role of fucoxanthin against cerebral ischemic/reperfusion injury through activation of Nrf2/HO-1 signaling. Biomed. Pharmacother. 2018, 106, 1484–1489. [Google Scholar] [CrossRef]
- Zhao, D.; Kwon, S.H.; Chun, Y.S.; Gu, M.Y.; Yang, H.O. Anti-Neuroinflammatory Effects of Fucoxanthin via Inhibition of Akt/NF-κB and MAPKs/AP-1 Pathways and Activation of PKA/CREB Pathway in Lipopolysaccharide-Activated BV-2 Microglial Cells. Neurochem. Res. 2017, 42, 667–677. [Google Scholar] [CrossRef] [PubMed]
- Li, P.A.; Hou, X.; Hao, S. Mitochondrial biogenesis in neurodegeneration. J. Neurosci. Res. 2017, 95, 2025–2029. [Google Scholar] [CrossRef] [PubMed]
- Jiang, X.; Wang, G.; Lin, Q.; Tang, Z.; Yan, Q.; Yu, X. Fucoxanthin prevents lipopolysaccharide-induced depressive-like behavior in mice via AMPK- NF-κB pathway. Metab. Brain Dis. 2019, 34, 431–442. [Google Scholar] [CrossRef] [PubMed]
- Alghazwi, M.; Smid, S.; Musgrave, I.; Zhang, W. In vitro studies of the neuroprotective activities of astaxanthin and fucoxanthin against amyloid beta (Aβ 1-42) toxicity and aggregation. Neurochem. Int. 2019, 124, 215–224. [Google Scholar] [CrossRef] [Green Version]
- Paudel, P.; Seong, S.H.; Jung, H.A.; Choi, J.S. Characterizing fucoxanthin as a selective dopamine D3/D4 receptor agonist: Relevance to Parkinson’s disease. Chem. Biol. Interact. 2019, 310, 108757. [Google Scholar] [CrossRef]
- Ambati, R.; Phang, S.-M.; Ravi, S.; Aswathanarayana, R. Astaxanthin: Sources, Extraction, Stability, Biological Activities and Its Commercial Applications—A Review. Mar. Drugs 2014, 12, 128–152. [Google Scholar] [CrossRef]
- Jiang, X.; Chen, L.; Shen, L.; Chen, Z.; Xu, L.; Zhang, J.; Yu, X. Trans-astaxanthin attenuates lipopolysaccharide-induced neuroinflammation and depressive-like behavior in mice. Brain Res. 2016, 1649, 30–37. [Google Scholar] [CrossRef]
- Zhang, X.S.; Zhang, X.; Wu, Q.; Li, W.; Wang, C.X.; Xie, G.B.; Zhou, X.M.; Shi, J.X.; Zhou, M.L. Astaxanthin offers neuroprotection and reduces neuroinflammation in experimental subarachnoid hemorrhage. J. Surg. Res. 2014, 192, 206–213. [Google Scholar] [CrossRef]
- Wen, X.; Huang, A.; Hu, J.; Zhong, Z.; Liu, Y.; Li, Z.; Pan, X.; Liu, Z. Neuroprotective effect of astaxanthin against glutamate-induced cytotoxicity in HT22 cells: Involvement of the Akt/GSK-3β pathway. Neuroscience 2015, 303, 558–568. [Google Scholar] [CrossRef]
- Beurel, E.; Grieco, S.F.; Jope, R.S. Glycogen synthase kinase-3 (GSK3): Regulation, actions, and diseases. Pharmacol. Ther. 2015, 148, 114–131. [Google Scholar] [CrossRef] [Green Version]
- Chang, C.S.; Chang, C.L.; Lai, G.H. Reactive oxygen species scavenging activities in a chemiluminescence model and neuroprotection in rat pheochromocytoma cells by astaxanthin, beta-carotene, and canthaxanthin. Kaohsiung J. Med. Sci. 2013, 29, 412–421. [Google Scholar] [CrossRef] [PubMed]
- Nolan, J.M.; Mulcahy, R.; Power, R.; Moran, R.; Howard, A.N. Nutritional Intervention to Prevent Alzheimer’s Disease: Potential Benefits of Xanthophyll Carotenoids and Omega-3 Fatty Acids Combined. J. Alzheimer’s Dis. 2018, 64, 367–378. [Google Scholar] [CrossRef] [Green Version]
- Li, S.Y.; Yang, D.; Fu, Z.J.; Woo, T.; Wong, D.; Lo, A.C.Y. Lutein enhances survival and reduces neuronal damage in a mouse model of ischemic stroke. Neurobiol. Dis. 2012, 45, 624–632. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.X.; Liu, T.; Dai, X.L.; Zheng, Q.S.; Hui, B.D.; Jiang, Z.F. Treatment with lutein provides neuroprotection in mice subjected to transient cerebral ischemia. J. Asian Nat. Prod. Res. 2014, 16, 1084–1093. [Google Scholar] [CrossRef] [PubMed]
- Chen, P.; Li, L.; Gao, Y.; Xie, Z.; Zhang, Y.; Pan, Z.; Tu, Y.; Wang, H.; Han, Q.; Hu, X.; et al. β -carotene provides neuro protection after experimental traumatic brain injury via the Nrf2-ARE pathway. J. Integr. Neurosci. 2019, 18, 153–161. [Google Scholar] [CrossRef] [Green Version]
- Ribeiro, D.; Freitas, M.; Silva, A.M.S.; Carvalho, F.; Fernandes, E. Antioxidant and pro-oxidant activities of carotenoids and their oxidation products. Food Chem. Toxicol. 2018, 120, 681–699. [Google Scholar] [CrossRef] [PubMed]
- Barbosa, M.; Lopes, G.; Andrade, P.B.; Valentão, P. Bioprospecting of brown seaweeds for biotechnological applications: Phlorotannin actions in inflammation and allergy network. Trends Food Sci. Technol. 2019, 86, 153–171. [Google Scholar] [CrossRef]
- Isaza Martínez, J.H.; Torres Castañeda, H.G. Preparation and chromatographic analysis of phlorotannins. J. Chromatogr. Sci. 2013, 51, 825–838. [Google Scholar] [CrossRef] [Green Version]
- Heffernan, N.; Brunton, N.P.; FitzGerald, R.J.; Smyth, T.J. Profiling of the molecular weight and structural isomer abundance of macroalgae-derived phlorotannins. Mar. Drugs 2015, 13, 509–528. [Google Scholar] [CrossRef]
- Shanura Fernando, I.P.; Kim, M.; Son, K.T.; Jeong, Y.; Jeon, Y.J. Antioxidant Activity of Marine Algal Polyphenolic Compounds: A Mechanistic Approach. J. Med. Food 2016, 19, 615–628. [Google Scholar] [CrossRef]
- Rajauria, G.; Jaiswal, A.K.; Abu-Gannam, N.; Gupta, S. Antimicrobial, antioxidant and free radical-scavenging capacity of brown seaweed himanthalia elongata from western coast of Ireland. J. Food Biochem. 2013, 37, 322–335. [Google Scholar] [CrossRef]
- Gager, L.; Connan, S.; Molla, M.; Couteau, C.; Arbona, J.-F.; Coiffard, L.; Cérantola, S.; Stiger-Pouvreau, V. Active phlorotannins from seven brown seaweeds commercially harvested in Brittany (France) detected by 1H NMR and in vitro assays: Temporal variation and potential valorization in cosmetic applications. J. Appl. Phycol. 2020, 32, 2375–2386. [Google Scholar] [CrossRef]
- Kim, A.R.; Lee, B.; Joung, E.J.; Gwon, W.G.; Utsuki, T.; Kim, N.G.; Kim, H.R. 6,6′-Bieckol suppresses inflammatory responses by down-regulating nuclear factor-κB activation via Akt, JNK, and p38 MAPK in LPS-stimulated microglial cells. Immunopharmacol. Immunotoxicol. 2016, 38, 244–252. [Google Scholar] [CrossRef] [PubMed]
- Manandhar, B.; Wagle, A.; Seong, S.H.; Paudel, P.; Kim, H.R.; Jung, H.A.; Choi, J.S. Phlorotannins with potential anti-tyrosinase and antioxidant activity isolated from the marine seaweed ecklonia stolonifera. Antioxidants 2019, 8, 240. [Google Scholar] [CrossRef] [Green Version]
- Ahn, B.R.; Moon, H.E.; Kim, H.R.; Jung, H.A.; Choi, J.S. Neuroprotective effect of edible brown alga Eisenia bicyclis on amyloid beta peptide-induced toxicity in PC12 cells. Arch. Pharm. Res. 2012, 35, 1989–1998. [Google Scholar] [CrossRef]
- Heo, S.J.; Cha, S.H.; Kim, K.N.; Lee, S.H.; Ahn, G.; Kang, D.H.; Oh, C.; Choi, Y.U.; Affan, A.; Kim, D.; et al. Neuroprotective effect of phlorotannin isolated from Ishige okamurae against H2O2-induced oxidative stress in murine hippocampal neuronal cells, HT22. Appl. Biochem. Biotechnol. 2012, 166, 1520–1532. [Google Scholar] [CrossRef]
- Bogolitsyn, K.; Druzhinina, A.; Kaplitsin, P.; Ovchinnikov, D.; Parshina, A.; Kuznetsova, M. Relationship between radical scavenging activity and polymolecular properties of brown algae polyphenols. Chem. Pap. 2019, 73, 2377–2385. [Google Scholar] [CrossRef]
- Belda, M.; Sanchez, D.; Bover, E.; Prieto, B.; Padrón, C.; Cejalvo, D.; Lloris, J.M. Extraction of polyphenols in Himanthalia elongata and determination by high performance liquid chromatography with diode array detector prior to its potential use against oxidative stress. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2016, 1033–1034, 334–341. [Google Scholar] [CrossRef]
- Olasehinde, T.A.; Olaniran, A.O.; Okoh, A.I. Neuroprotective effects of some seaweeds against Zn—Induced neuronal damage in HT-22 cells via modulation of redox imbalance, inhibition of apoptosis and acetylcholinesterase activity. Metab. Brain Dis. 2019, 34, 1615–1627. [Google Scholar] [CrossRef]
- Yonekura-Sakakibara, K.; Higashi, Y.; Nakabayashi, R. The Origin and Evolution of Plant Flavonoid Metabolism. Front. Plant Sci. 2019, 10, 943. [Google Scholar] [CrossRef] [Green Version]
- Davies, K.M.; Jibran, R.; Zhou, Y.; Albert, N.W.; Brummell, D.A.; Jordan, B.R.; Bowman, J.L.; Schwinn, K.E. The Evolution of Flavonoid Biosynthesis: A Bryophyte Perspective. Front. Plant Sci. 2020, 11, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chauhan, B.S.; Kumar, R.; Kumar, P.; Kumar, P.; Sinha, S.; Mishra, S.K.; Tiwari, K.N.; Critchley, A.T.; Prithiviraj, B.; Srikrishna, S. Neuroprotective potential of flavonoid rich Ascophyllum nodosum (FRAN) fraction from the brown seaweed on an Aβ42 induced Alzheimer’s model of Drosophila. Phytomedicine 2022, 95, 153872. [Google Scholar] [CrossRef] [PubMed]
- Machu, L.; Misurcova, L.; Ambrozova, J.V.; Orsavova, J.; Mlcek, J.; Sochor, J.; Jurikova, T. Phenolic content and antioxidant capacity in algal food products. Molecules 2015, 20, 1118–1133. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shay, J.; Elbaz, H.A.; Lee, I.; Zielske, S.P.; Malek, M.H.; Hüttemann, M. Molecular Mechanisms and Therapeutic Effects of (−)-Epicatechin and Other Polyphenols in Cancer, Inflammation, Diabetes, and Neurodegeneration. Oxid. Med. Cell. Longev. 2015, 2015, 181260. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shaki, F.; Shayeste, Y.; Karami, M.; Akbari, E.; Rezaei, M.; Ataee, R. The effect of epicatechin on oxidative stress and mitochondrial damage induced by homocycteine using isolated rat hippocampus mitochondria. Res. Pharm. Sci. 2017, 12, 119–127. [Google Scholar] [CrossRef] [Green Version]
- Mohamed, R.H.; Karam, R.A.; Amer, M.G. Epicatechin attenuates doxorubicin-induced brain toxicity: Critical role of TNF-α, iNOS and NF-κB. Brain Res. Bull. 2011, 86, 22–28. [Google Scholar] [CrossRef]
- Wong, C.H.; Gan, S.Y.; Tan, S.C.; Gany, S.A.; Ying, T.; Gray, A.I.; Igoli, J.; Chan, E.W.L.; Phang, S.M. Fucosterol inhibits the cholinesterase activities and reduces the release of pro-inflammatory mediators in lipopolysaccharide and amyloid-induced microglial cells. J. Appl. Phycol. 2018, 30, 3261–3270. [Google Scholar] [CrossRef]
- Hannan, M.A.; Dash, R.; Mamun Sohag, A.A.; Moon, I.S. Deciphering molecular mechanism of the neuropharmacological action of fucosterol through integrated system pharmacology and in silico analysis. Mar. Drugs 2019, 17, 639. [Google Scholar] [CrossRef] [Green Version]
- Motaghinejad, M.; Motevalian, M.; Fatima, S.; Hashemi, H.; Gholami, M. Curcumin confers neuroprotection against alcohol-induced hippocampal neurodegeneration via CREB-BDNF pathway in rats. Biomed. Pharmacother. 2017, 87, 721–740. [Google Scholar] [CrossRef]
- Castro-Silva, E.S.; Bello, M.; Rosales-Hernández, M.C.; Correa-Basurto, J.; Hernández-Rodríguez, M.; Villalobos-Acosta, D.; Méndez-Méndez, J.V.; Estrada-Pérez, A.; Murillo-Álvarez, J.; Muñoz-Ochoa, M. Fucosterol from Sargassum horridum as an amyloid-beta (Aβ1-42) aggregation inhibitor: In vitro and in silico studies. J. Biomol. Struct. Dyn. 2021, 39, 1271–1283. [Google Scholar] [CrossRef]
- Oh, J.H.; Choi, J.S.; Nam, T.J. Fucosterol from an edible brown alga ecklonia stolonifera prevents soluble amyloid beta-induced cognitive dysfunction in aging rats. Mar. Drugs 2018, 16, 368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silva, J.; Alves, C.; Pinteus, S.; Susano, P.; Simões, M.; Guedes, M.; Martins, A.; Rehfeldt, S.; Gaspar, H.; Goettert, M.; et al. Disclosing the potential of eleganolone for Parkinson’s disease therapeutics: Neuroprotective and anti-inflammatory activities. Pharmacol. Res. 2021, 168, 105589. [Google Scholar] [CrossRef] [PubMed]
- Sangha, J.S.; Wally, O.; Banskota, A.H.; Stefanova, R.; Hafting, J.T.; Critchley, A.T.; Prithiviraj, B.; Perry, G. A cultivated form of a red seaweed (Chondrus crispus), suppresses β-amyloid-induced paralysis in caenorhabditis elegans. Mar. Drugs 2015, 13, 6407–6424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.; Banskota, A.H.; Critchley, A.T.; Hafting, J.; Prithiviraj, B. Neuroprotective effects of the cultivated Chondrus crispus in a C. elegans model of Parkinson’s disease. Mar. Drugs 2015, 13, 2250–2266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tullet, J.M.A.; Green, J.W.; Au, C.; Benedetto, A.; Thompson, M.A.; Clark, E.; Gilliat, A.F.; Young, A.; Schmeisser, K.; Gems, D. The SKN-1/Nrf2 transcription factor can protect against oxidative stress and increase lifespan in C. elegans by distinct mechanisms. Aging Cell 2017, 16, 1191–1194. [Google Scholar] [CrossRef] [Green Version]
- de Oliveira, B.F.; Veloso, C.A.; Nogueira-Machado, J.A.; de Moraes, E.N.; dos Santos, R.R.; Cintra, M.T.G.; Chaves, M.M. Ascorbic acid, alpha-tocopherol, and betacarotene reduce oxidative stress and proinflammatory cytokines in mononuclear cells of Alzheimer’s disease patients. Nutr. Neurosci. 2012, 15, 244–251. [Google Scholar] [CrossRef]
- Khanna, S.; Heigel, M.; Weist, J.; Gnyawali, S.; Teplitsky, S.; Roy, S.; Sen, C.K.; Rink, C. Excessive α-tocopherol exacerbates microglial activation and brain injury caused by acute ischemic stroke. FASEB J. 2015, 29, 828–836. [Google Scholar] [CrossRef] [Green Version]
- Ding, H.; Wang, H.; Zhu, L.; Wei, W. Ursolic Acid Ameliorates Early Brain Injury After Experimental Traumatic Brain Injury in Mice by Activating the Nrf2 Pathway. Neurochem. Res. 2017, 42, 337–346. [Google Scholar] [CrossRef]
- Rai, S.N.; Yadav, S.K.; Singh, D.; Singh, S.P. Ursolic acid attenuates oxidative stress in nigrostriatal tissue and improves neurobehavioral activity in MPTP-induced Parkinsonian mouse model. J. Chem. Neuroanat. 2016, 71, 41–49. [Google Scholar] [CrossRef]
- Liu, D.Q.; Mao, S.C.; Zhang, H.Y.; Yu, X.Q.; Feng, M.T.; Wang, B.; Feng, L.H.; Guo, Y.W. Racemosins A and B, two novel bisindole alkaloids from the green alga Caulerpa racemosa. Fitoterapia 2013, 91, 15–20. [Google Scholar] [CrossRef]
- Shikov, A.N.; Flisyuk, E.V.; Obluchinskaya, E.D.; Pozharitskaya, O.N. Pharmacokinetics of Marine-Derived Drugs. Mar. Drugs 2020, 18, 557. [Google Scholar] [CrossRef] [PubMed]
- Karaś, M.; Jakubczyk, A.; Szymanowska, U.; Złotek, U.; Zielińska, E. Digestion and bioavailability of bioactive phytochemicals. Int. J. Food Sci. Technol. 2017, 52, 291–305. [Google Scholar] [CrossRef]
- Ribas-Agustí, A.; Martín-Belloso, O.; Soliva-Fortuny, R.; Elez-Martínez, P. Food processing strategies to enhance phenolic compounds bioaccessibility and bioavailability in plant-based foods. Crit. Rev. Food Sci. Nutr. 2018, 58, 2531–2548. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Xu, W.; Chen, D.; Chen, G.; Liu, J.; Zeng, X.; Shao, R.; Zhu, H. Digestibility of sulfated polysaccharide from the brown seaweed Ascophyllum nodosum and its effect on the human gut microbiota in vitro. Int. J. Biol. Macromol. 2018, 112, 1055–1061. [Google Scholar] [CrossRef] [PubMed]
- Sutapa, B.M.; Dhruti, A.; Priyanka, G.; Gopa, R.B. Absorption, distribution, metabolism and elimination (ADME) and toxicity profile of marine sulfated polysaccharides used in bionanotechnology. African J. Pharm. Pharmacol. 2018, 12, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Cunha, L.; Grenha, A. Sulfated Seaweed Polysaccharides as Multifunctional Materials in Drug Delivery Applications. Mar. Drugs 2016, 14, 42. [Google Scholar] [CrossRef]
- Rouzet, F.; Bachelet-Violette, L.; Alsac, J.M.; Suzuki, M.; Meulemans, A.; Louedec, L.; Petiet, A.; Jandrot-Perrus, M.; Chaubet, F.; Michel, J.B.; et al. Radiolabeled fucoidan as a P-selectin targeting agent for in vivo imaging of platelet-rich thrombus and endothelial activation. J. Nucl. Med. 2011, 52, 1433–1440. [Google Scholar] [CrossRef] [Green Version]
- Pozharitskaya, O.N.; Shikov, A.N.; Faustova, N.M.; Obluchinskaya, E.D.; Kosman, V.M.; Vuorela, H.; Makarov, V.G. Pharmacokinetic and tissue distribution of fucoidan from fucus vesiculosus after oral administration to rats. Mar. Drugs 2018, 16, 132. [Google Scholar] [CrossRef] [Green Version]
- van der Wielen, N.; Moughan, P.J.; Mensink, M. Amino acid absorption in the large intestine of humans and porcine models. J. Nutr. 2017, 147, 1493–1498. [Google Scholar] [CrossRef] [Green Version]
- Nakashima, E.M.N.; Kudo, A.; Iwaihara, Y.; Tanaka, M.; Matsumoto, K.; Matsui, T. Application of 13C stable isotope labeling liquid chromatography-multiple reaction monitoring-tandem mass spectrometry method for determining intact absorption of bioactive dipeptides in rats. Anal. Biochem. 2011, 414, 109–116. [Google Scholar] [CrossRef]
- Tanaka, M.; Dohgu, S.; Komabayashi, G.; Kiyohara, H.; Takata, F.; Kataoka, Y.; Nirasawa, T.; Maebuchi, M.; Matsui, T. Brain-transportable dipeptides across the blood-brain barrier in mice. Sci. Rep. 2019, 9, 5769. [Google Scholar] [CrossRef] [PubMed]
- Gow, R.V.; Hibbeln, J.R. Omega-3 Fatty Acid and Nutrient Deficits in Adverse Neurodevelopment and Childhood Behaviors. Child Adolesc. Psychiatr. Clin. N. Am. 2014, 23, 555–590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barceló-Coblijn, G.; Murphy, E.J. Alpha-linolenic acid and its conversion to longer chain n − 3 fatty acids: Benefits for human health and a role in maintaining tissue n − 3 fatty acid levels. Prog. Lipid Res. 2009, 48, 355–374. [Google Scholar] [CrossRef] [PubMed]
- Che, H.; Fu, X.; Zhang, L.; Gao, X.; Wen, M.; Du, L.; Xue, C.; Xu, J.; Wang, Y. Neuroprotective Effects of n-3 Polyunsaturated Fatty Acid-Enriched Phosphatidylserine Against Oxidative Damage in PC12 Cells. Cell. Mol. Neurobiol. 2018, 38, 657–668. [Google Scholar] [CrossRef] [PubMed]
- Francisco, J.; Horta, A.; Pedrosa, R.; Afonso, C.; Cardoso, C.; Bandarra, N.M.; Gil, M.M. Bioaccessibility of antioxidants and fatty acids from fucus spiralis. Foods 2020, 9, 440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moran, N.E.; Mohn, E.S.; Hason, N.; Erdman, J.W.; Johnson, E.J. Intrinsic and extrinsic factors impacting absorption, metabolism, and health effects of dietary carotenoids. Adv. Nutr. 2018, 9, 465–492. [Google Scholar] [CrossRef] [Green Version]
- Johnson, E.J.; Vishwanathan, R.; Johnson, M.A.; Hausman, D.B.; Davey, A.; Scott, T.M.; Green, R.C.; Miller, L.S.; Gearing, M.; Woodard, J.; et al. Relationship between serum and brain carotenoids, α -tocopherol, and retinol concentrations and cognitive performance in the oldest old from the georgia centenarian study. J. Aging Res. 2013, 2013, 951786. [Google Scholar] [CrossRef] [Green Version]
- Corona, G.; Ji, Y.; Anegboonlap, P.; Hotchkiss, S.; Gill, C.; Yaqoob, P.; Spencer, J.P.E.; Rowland, I. Gastrointestinal modifications and bioavailability of brown seaweed phlorotannins and effects on inflammatory markers. Br. J. Nutr. 2016, 115, 1240–1253. [Google Scholar] [CrossRef] [Green Version]
- Corona, G.; Coman, M.M.; Guo, Y.; Hotchkiss, S.; Gill, C.; Yaqoob, P.; Spencer, J.P.E.; Rowland, I. Effect of simulated gastrointestinal digestion and fermentation on polyphenolic content and bioactivity of brown seaweed phlorotannin-rich extracts. Mol. Nutr. Food Res. 2017, 61, 1700223. [Google Scholar] [CrossRef]
- Upadhyay, R.K. Drug Delivery Systems, CNS Protection, and the Blood Brain Barrier. BioMed Res. Int. 2014, 2014, 869269. [Google Scholar] [CrossRef] [Green Version]
- Liu, L.; Venkatraman, S.S.; Yang, Y.Y.; Guo, K.; Lu, J.; He, B.; Moochhala, S.; Kan, L. Polymeric micelles anchored with TAT for delivery of antibiotics across the blood-brain barrier. Biopolym.—Pept. Sci. Sect. 2008, 90, 617–623. [Google Scholar] [CrossRef] [PubMed]
- Guarnieri, D.; Falanga, A.; Muscetti, O.; Tarallo, R.; Fusco, S.; Galdiero, M.; Galdiero, S.; Netti, P.A. Shuttle-Mediated Nanoparticle Delivery to the Blood-Brain Barrier. Small 2013, 9, 853–862. [Google Scholar] [CrossRef] [PubMed]
- Neves, A.R.; Queiroz, J.F.; Lima, S.A.C.; Reis, S. Apo E-Functionalization of Solid Lipid Nanoparticles Enhances Brain Drug Delivery: Uptake Mechanism and Transport Pathways. Bioconjug. Chem. 2017, 28, 995–1004. [Google Scholar] [CrossRef] [PubMed]
- Sinnecker, H.; Krause, T.; Koelling, S.; Lautenschläger, I.; Frey, A. The gut wall provides an effective barrier against nanoparticle uptake. Beilstein J. Nanotechnol. 2014, 5, 2092–2101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Date, A.A.; Hanes, J.; Ensign, L.M. Nanoparticles for oral delivery: Design, evaluation and state-ofthe-art. J. Control Release 2016, 240, 504–526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bindels, L.B.; Delzenne, N.M.; Cani, P.D.; Walter, J. Towards a more comprehensive concept for prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 303–310. [Google Scholar] [CrossRef]
- Zhang, Y.J.; Li, S.; Gan, R.Y.; Zhou, T.; Xu, D.P.; Li, H. Bin Impacts of gut bacteria on human health and diseases. Int. J. Mol. Sci. 2015, 16, 7493–7519. [Google Scholar] [CrossRef]
- Kim, J.Y.; Kwon, Y.M.; Kim, I.S.; Kim, J.A.; Yu, D.Y.; Adhikari, B.; Lee, S.S.; Choi, I.S.; Cho, K.K. Effects of the Brown Seaweed Laminaria japonica Supplementation on Serum Concentrations of IgG, Triglycerides, and Cholesterol, and Intestinal Microbiota Composition in Rats. Front. Nutr. 2018, 5, 23. [Google Scholar] [CrossRef] [Green Version]
- Zhou, M.; Hünerberg, M.; Chen, Y.; Reuter, T.; McAllister, T.A.; Evans, F.; Critchley, A.T.; Guan, L.L. Air-Dried Brown Seaweed, Ascophyllum nodosum, Alters the Rumen Microbiome in a Manner That Changes Rumen Fermentation Profiles and Lowers the Prevalence of Foodborne Pathogens. mSphere 2018, 3, e00017-18. [Google Scholar] [CrossRef] [Green Version]
- Sommer, F.; Bäckhed, F. The gut microbiota-masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11, 227–238. [Google Scholar] [CrossRef]
- Rea, K.; Dinan, T.G.; Cryan, J.F. The microbiome: A key regulator of stress and neuroinflammation. Neurobiol. Stress 2016, 4, 23–33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Friedland, R.P.; Chapman, M.R. The role of microbial amyloid in neurodegeneration. PLoS Pathog. 2017, 13, e1006654. [Google Scholar] [CrossRef] [PubMed]
- Lin, C.H.; Chen, C.C.; Chiang, H.L.; Liou, J.M.; Chang, C.M.; Lu, T.P.; Chuang, E.Y.; Tai, Y.C.; Cheng, C.; Lin, H.Y.; et al. Altered gut microbiota and inflammatory cytokine responses in patients with Parkinson’s disease. J. Neuroinflamm. 2019, 16, 129. [Google Scholar] [CrossRef] [PubMed]
- Bercik, P.; Denou, E.; Collins, J.; Jackson, W.; Lu, J.; Jury, J.; Deng, Y.; Blennerhassett, P.; MacRi, J.; McCoy, K.D.; et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011, 141, 599–609. [Google Scholar] [CrossRef] [Green Version]
- Clarke, G.; Grenham, S.; Scully, P.; Fitzgerald, P.; Moloney, R.D.; Shanahan, F.; Dinan, T.G.; Cryan, J.F. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry 2013, 18, 666–673. [Google Scholar] [CrossRef] [Green Version]
- Neufeld, K.M.; Kang, N.; Bienenstock, J.; Foster, J.A. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 2011, 23, 255–265. [Google Scholar] [CrossRef]
- Menshova, R.V.; Shevchenko, N.M.; Imbs, T.I.; Zvyagintseva, T.N.; Malyarenko, O.S.; Zaporoshets, T.S.; Besednova, N.N.; Ermakova, S.P. Fucoidans from brown alga Fucus evanescens: Structure and biological activity. Front. Mar. Sci. 2016, 3, 129. [Google Scholar] [CrossRef] [Green Version]
- Kong, Q.; Dong, S.; Gao, J.; Jiang, C. In vitro fermentation of sulfated polysaccharides from E. prolifera and L. japonica by human fecal microbiota. Int. J. Biol. Macromol. 2016, 91, 867–871. [Google Scholar] [CrossRef]
- Bajury, D.M.; Rawi, M.H.; Sazali, I.H.; Abdullah, A.; Sarbini, S.R. Prebiotic evaluation of red seaweed (Kappaphycus alvarezii) using in vitro colon model. Int. J. Food Sci. Nutr. 2017, 68, 821–828. [Google Scholar] [CrossRef]
- Watson, H.; Mitra, S.; Croden, F.C.; Taylor, M.; Wood, H.M.; Perry, S.L.; Spencer, J.A.; Quirke, P.; Toogood, G.J.; Lawton, C.L.; et al. A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut 2018, 67, 1974–1983. [Google Scholar] [CrossRef]
- Menni, C.; Zierer, J.; Pallister, T.; Jackson, M.A.; Long, T.; Mohney, R.P.; Steves, C.J.; Spector, T.D.; Valdes, A.M. Omega-3 fatty acids correlate with gut microbiome diversity and production of N-carbamylglutamate in middle aged and elderly women. Sci. Rep. 2017, 7, 11079. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Charoensiddhi, S.; Conlon, M.A.; Vuaran, M.S.; Franco, C.M.M.; Zhang, W. Polysaccharide and phlorotannin-enriched extracts of the brown seaweed Ecklonia radiata influence human gut microbiota and fermentation in vitro. J. Appl. Phycol. 2017, 29, 2407–2416. [Google Scholar] [CrossRef]
- Honarpisheh, P.; Reynolds, C.R.; Blasco Conesa, M.P.; Moruno Manchon, J.F.; Putluri, N.; Bhattacharjee, M.B.; Urayama, A.; McCullough, L.D.; Ganesh, B.P. Dysregulated Gut Homeostasis Observed Prior to the Accumulation of the Brain Amyloid-β in Tg2576 Mice. Int. J. Mol. Sci. 2020, 21, 1711. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scheperjans, F.; Aho, V.; Pereira, P.A.B.; Koskinen, K.; Paulin, L.; Pekkonen, E.; Haapaniemi, E.; Kaakkola, S.; Eerola-Rautio, J.; Pohja, M.; et al. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov. Disord. 2015, 30, 350–358. [Google Scholar] [CrossRef] [PubMed]
- Peng, W.; Yi, P.; Yang, J.; Xu, P.; Wang, Y.; Zhang, Z.; Huang, S.; Wang, Z.; Zhang, C. Association of gut microbiota composition and function with a senescence-accelerated mouse model of Alzheimer’s Disease using 16S rRNA gene and metagenomic sequencing analysis. Aging 2018, 10, 4054–4065. [Google Scholar] [CrossRef]
- Bunney, P.E.; Zink, A.N.; Holm, A.A.; Billington, C.J.; Kotz, C.M. Orexin activation counteracts decreases in nonexercise activity thermogenesis (NEAT) caused by high-fat diet. Physiol. Behav. 2017, 176, 139–148. [Google Scholar] [CrossRef]
- Fang, X.; Wang, X.; Yang, S.; Meng, F.; Wang, X.; Wei, H.; Chen, T. Evaluation of the microbial diversity in amyotrophic lateral sclerosis using high-throughput sequencing. Front. Microbiol. 2016, 7, 1479. [Google Scholar] [CrossRef] [Green Version]
- Bailes, J.E.; Abusuwwa, R.; Arshad, M.; Chowdhry, S.A.; Schleicher, D.; Hempeck, N.; Gandhi, Y.N.; Jaffa, Z.; Bokhari, F.; Karahalios, D.; et al. Omega-3 fatty acid supplementation in severe brain trauma: Case for a large multicenter trial. J. Neurosurg. 2020, 133, 598–602. [Google Scholar] [CrossRef]
- Chang, J.P.-C.; Su, K.-P.; Mondelli, V.; Satyanarayanan, S.K.; Yang, H.-T.; Chiang, Y.-J.; Chen, H.-T.; Pariante, C.M. High-dose eicosapentaenoic acid (EPA) improves attention and vigilance in children and adolescents with attention deficit hyperactivity disorder (ADHD) and low endogenous EPA levels. Transl. Psychiatry 2019, 9, 303. [Google Scholar] [CrossRef]
- Quinn, J.F.; Raman, R.; Thomas, R.G.; Yurko-Mauro, K.; Nelson, E.B.; Van Dyck, C.; Galvin, J.E.; Emond, J.; Jack, C.R.; Weiner, M.; et al. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: A randomized trial. JAMA—J. Am. Med. Assoc. 2010, 304, 1903–1911. [Google Scholar] [CrossRef]
- Bazan, N.G.; Molina, M.F.; Gordon, W.C. Docosahexaenoic acid signalolipidomics in nutrition: Significance in aging, neuroinflammation, macular degeneration, Alzheimer’s, and other neurodegenerative diseases. Annu. Rev. Nutr. 2011, 31, 321–351. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zárate, R.; Jaber-Vazdekis, N.; Tejera, N.; Pérez, J.A.; Rodríguez, C. Significance of long chain polyunsaturated fatty acids in human health. Clin. Transl. Med. 2017, 6, e25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silva, G.C.R.; Reis, R.P.R.; Braga, S.C.A.; Lima, T.S.; de Souza, M.C.M. Optimization during the First Thousand Days of Child through Dietary Supplement with Lc-Pufas: Systematic Review of the Literature. Matern. Pediatr. Nutr. 2017, 3, 120. [Google Scholar] [CrossRef] [Green Version]
- Casañas-Sánchez, V.; Pérez, J.A.; Fabelo, N.; Quinto-Alemany, D.; Díaz, M.L. Docosahexaenoic (DHA) modulates phospholipid-hydroperoxide glutathione peroxidase (Gpx4) gene expression to ensure self-protection from oxidative damage in hippocampal cells. Front. Physiol. 2015, 6, 203. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grayson, D.S.; Kroenke, C.D.; Neuringer, M.; Fair, D.A. Dietary omega-3 fatty acids modulate large-scale systems organization in the rhesus macaque brain. J. Neurosci. 2014, 34, 2065–2074. [Google Scholar] [CrossRef]
- Martorana, A.; Motta, C.; Koch, G.; Massaia, M.; Mondino, S.; Raniero, I.; Vacca, A.; Di Lorenzo, F.; Cavallo, G.; Oddenino, E.; et al. Effect of homotaurine in patients with cognitive impairment: Results from an Italian observational retrospective study. J. Gerontol. Geriatr. 2018, 66, 15–20. [Google Scholar]
- Tolar, M.; Abushakra, S.; Hey, J.A.; Porsteinsson, A.; Sabbagh, M. Aducanumab, gantenerumab, BAN2401, and ALZ-801—The first wave of amyloid-targeting drugs for Alzheimer’s disease with potential for near term approval. Alzheimers. Res. Ther. 2020, 12, 95. [Google Scholar] [CrossRef]
- Ricciardi, L.; De Nigris, F.; Specchia, A.; Fasano, A. Homotaurine in Parkinson’s disease. Neurol. Sci. 2015, 36, 1581–1587. [Google Scholar] [CrossRef]
- Reid, S.N.S.; Ryu, J.; Kim, Y.; Jeon, B.H. The Effects of Fermented Laminaria japonica on Short-Term Working Memory and Physical Fitness in the Elderly. Evid.-Based Complement. Altern. Med. 2018, 2018, 8109621. [Google Scholar] [CrossRef] [Green Version]
- Xiao, S.; Chan, P.; Wang, T.; Hong, Z.; Wang, S.; Kuang, W.; He, J.; Pan, X.; Zhou, Y.; Ji, Y.; et al. A 36-week multicenter, randomized, double-blind, placebo-controlled, parallel-group, phase 3 clinical trial of sodium oligomannate for mild-to-moderate Alzheimer’s dementia. Alzheimer’s Res. Ther. 2021, 13, 62. [Google Scholar] [CrossRef]
- Haskell-Ramsay, C.F.; Jackson, P.A.; Dodd, F.L.; Forster, J.S.; Bérubé, J.; Levinton, C.; Kennedy, D.O. Acute post-prandial cognitive effects of Brown seaweed extract in humans. Nutrients 2018, 10, 85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Um, M.Y.; Kim, J.Y.; Han, J.K.; Kim, J.; Yang, H.; Yoon, M.; Kim, J.; Kang, S.W.; Cho, S. Phlorotannin supplement decreases wake after sleep onset in adults with self-reported sleep disturbance: A randomized, controlled, double-blind clinical and polysomnographic study. Phyther. Res. 2018, 32, 698–704. [Google Scholar] [CrossRef] [PubMed]
- Banach, J.L.; Hoek-van den Hil, E.F.; Fels-Klerx, H.J. Food safety hazards in the European seaweed chain. Compr. Rev. Food Sci. Food Saf. 2020, 19, 332–364. [Google Scholar] [CrossRef] [PubMed]
- Dadolahi-Sohrab, A.; Mohammad, S.; Nabavi, B.; Safahieh, A. Environmental Monitoring of Heavy Metals in Seaweed and Associated Sediment from the Strait of Hormuz, I.R. Iran Deep Eutectic Solvent View project Histopathological, biochemical and and hematological changes in yellowfin seabream (Acanthopagrus latus)fol. World J. Fish Mar. Sci. 2011, 3, 576–589. [Google Scholar]
- Roleda, M.Y.; Marfaing, H.; Desnica, N.; Jónsdóttir, R.; Skjermo, J.; Rebours, C.; Nitschke, U. Variations in polyphenol and heavy metal contents of wild-harvested and cultivated seaweed bulk biomass: Health risk assessment and implication for food applications. Food Control 2019, 95, 121–134. [Google Scholar] [CrossRef]
- Desideri, D.; Roselli, C.; Feduzi, L.; Ugolini, L.; Meli, M.A. Applicability of an in vitro gastrointestinal digestion method to evaluation of toxic elements bioaccessibility from algae for human consumption. J. Toxicol. Environ. Health—Part A Curr. Issues 2018, 81, 212–217. [Google Scholar] [CrossRef]
- Stévant, P.; Marfaing, H.; Duinker, A.; Fleurence, J.; Rustad, T.; Sandbakken, I.; Chapman, A. Biomass soaking treatments to reduce potentially undesirable compounds in the edible seaweeds sugar kelp (Saccharina latissima) and winged kelp (Alaria esculenta) and health risk estimation for human consumption. J. Appl. Phycol. 2018, 30, 2047–2060. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Y.; Shang, D.; Ning, J.; Zhai, Y. Arsenic and cadmium in the marine macroalgae (porphyra yezoensis and laminaria japonica)-forms and concentrations. Chem. Speciat. Bioavailab. 2012, 24, 197–203. [Google Scholar] [CrossRef] [Green Version]
- European Parliament EC no 629/2008. Off. J. Eur. Union 2008, 2008, 2006–2009.
- Ma, Z.; Lin, L.; Wu, M.; Yu, H.; Shang, T.; Zhang, T.; Zhao, M. Total and inorganic arsenic contents in seaweeds: Absorption, accumulation, transformation and toxicity. Aquaculture 2018, 497, 49–55. [Google Scholar] [CrossRef]
- Ender, E.; Subirana, M.A.; Raab, A.; Krupp, E.M.; Schaumlöffel, D.; Feldmann, J. Why is NanoSIMS elemental imaging of arsenic in seaweed (: Laminaria digitata) important for understanding of arsenic biochemistry in addition to speciation information? J. Anal. At. Spectrom. 2019, 34, 2295–2302. [Google Scholar] [CrossRef]
- Besada, V.; Andrade, J.M.; Schultze, F.; González, J.J. Heavy metals in edible seaweeds commercialised for human consumption. J. Mar. Syst. 2009, 75, 305–313. [Google Scholar] [CrossRef]
- Fuge, R.; Johnson, C.C. Iodine and human health, the role of environmental geochemistry and diet, a review. Appl. Geochemistry 2015, 63, 282–302. [Google Scholar] [CrossRef]
- EFSA Panel on Dietetic Products; Nutrition and Allergies (NDA). Scientific Opinion on Dietary Reference Values for iodine. EFSA J. 2014, 12, 3660. [Google Scholar] [CrossRef] [Green Version]
- Kumar, B.; Verma, V.K.; Kumar, S.; Sharma, C.S. Probabilistic health risk assessment of polycyclic aromatic hydrocarbons and polychlorinated biphenyls in urban soils from a tropical city of India. J. Environ. Sci. Health—Part A Toxic/Hazardous Subst. Environ. Eng. 2013, 48, 1253–1263. [Google Scholar] [CrossRef]
- dos Santos Fogaça, F.H.; Soares, C.; Oliveira, M.; Alves, R.N.; Maulvault, A.L.; Barbosa, V.L.; Anacleto, P.; Magalhães, J.A.; Bandarra, N.M.; Ramalhosa, M.J.; et al. Polycyclic aromatic hydrocarbons bioaccessibility in seafood: Culinary practices effects on dietary exposure. Environ. Res. 2018, 164, 165–172. [Google Scholar] [CrossRef] [Green Version]
- Net, S.; Henry, F.; Rabodonirina, S.; Diop, M.; Merhaby, D.; Mahfouz, C.; Amara, R.; Ouddane, B. Accumulation of PAHs, Me-PAHs, PCBs and total mercury in sediments and marine species in coastal areas of Dakar, Senegal: Contamination level and impact. Int. J. Environ. Res. 2015, 9, 419–432. [Google Scholar]
- Mohammad Bagher, A. Introduction to Radioactive Materials. Int. J. Renew. Sustain. Energy 2014, 3, 59. [Google Scholar] [CrossRef]
- Mittal, S.; Rani, A.; Mehra, R.; Ramola, R.C. Estimation of natural radionuclides in the soil samples and its radiological impact on human health. Radiat. Eff. Defects Solids 2018, 173, 673–682. [Google Scholar] [CrossRef]
- Kesäniemi, J.; Jernfors, T.; Lavrinienko, A.; Kivisaari, K.; Kiljunen, M.; Mappes, T.; Watts, P.C. Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent. Mol. Ecol. 2019, 28, 4620–4635. [Google Scholar] [CrossRef]
- Heldal, H.E.; Sjøtun, K. Technetium-99 (99Tc) in annual growth segments of knotted wrack (Ascophyllum nodosum). Sci. Total Environ. 2010, 408, 5575–5582. [Google Scholar] [CrossRef] [PubMed]
- Desideri, D.; Cantaluppi, C.; Ceccotto, F.; Meli, M.A.; Roselli, C.; Feduzi, L. Radiochemical characterization of algae products commercialized for human consumption. Health Phys. 2016, 111, 256–264. [Google Scholar] [CrossRef] [PubMed]
- Torres, P.; Santos, J.P.; Chow, F.; dos Santos, D.Y.A.C. A comprehensive review of traditional uses, bioactivity potential, and chemical diversity of the genus Gracilaria (Gracilariales, Rhodophyta). Algal Res. 2019, 37, 288–306. [Google Scholar] [CrossRef]
- Cagide, E.; Louzao, M.C.; Ares, I.R.; Vieytes, M.R.; Yotsu-Yamashita, M.; Paquette, L.A.; Yasumoto, T.; Botana, L.M. Effects of a synthetic analog of polycavernoside A on human neuroblastoma cells. Cell. Physiol. Biochem. 2007, 19, 185–194. [Google Scholar] [CrossRef] [PubMed]
- Kadari, S.; Yerrabelly, H.; Gogula, T.; Erukala, Y.G.; Yerrabelly, J.R.; Begari, P.K. Stereoselective Synthesis of γ-Butyrolactones Subunit of Polycavernoside A. J. Heterocycl. Chem. 2018, 55, 1986–1990. [Google Scholar] [CrossRef]
- Hammann, M.; Rempt, M.; Pohnert, G.; Wang, G.; Boo, S.M.; Weinberger, F. Increased potential for wound activated production of Prostaglandin E2 and related toxic compounds in non-native populations of Gracilaria vermiculophylla. Harmful Algae 2016, 51, 81–88. [Google Scholar] [CrossRef] [PubMed]
- De Almeida, C.L.F.; Falcão, D.S.; Lima, D.M.; Gedson, R.; Montenegro, D.A.; Lira, N.S.; Athayde-Filho, D.; Petrônio, F.; Rodrigues, L.C.; De Souza, M.D.F.V.; et al. Bioactivities from marine algae of the genus Gracilaria. Int. J. Mol. Sci. 2011, 12, 4550–4573. [Google Scholar] [CrossRef] [PubMed]
- Tamele, I.J.; Silva, M.; Vasconcelos, V. The incidence of marine toxins and the associated seafood poisoning episodes in the african countries of the indian ocean and the red sea. Toxins 2019, 11, 58. [Google Scholar] [CrossRef] [Green Version]
Compounds | IC50 Value | Reference |
---|---|---|
Cholinesterases Inhibition | ||
Sulfated polysaccharides extracted from Ulva lactuca L. | 106.93 µg/mL (AChE)/93.45 µg/mL (BChE) | [203] |
Glycoprotein isolated from U. pinnatifida | 63.56 μg/mL (AChE)/99.03 μg/mL (BChE) | [204] |
Fucoxanthin | 81.2 µM (AChE) | [205] |
Phlorotannin 974-B | 1.95 µM (AChE)/3.26 μM (BChE) | [206] |
α-Linolenic acid | 12.50 μg/mL (AChE)/15.89 μg/mL (BChE) | [207] |
BACE 1 Inhibition | ||
Glycoprotein isolated from U. pinnatifida | 73.35 μg/mL | [204] |
Fucoxanthin | 5.31 μM | [208] |
Fucosterol | 64.12 μM | [208] |
Dioxinodehydroeckol | 5.35 μM | [209] |
Eckol | 12.20 μM | [209] |
Phlorofurofucoeckol A | 2.13 μM | [209] |
Dieckol | 2.21 μM | [209] |
Triphloroethol A | 11.68 μM | [209] |
7-Phloroethol | 8.59 μM | [209] |
Fucofuroeckol-b | 16.1 μM | [210] |
MAO Inhibition | ||
Fucoxanthin | 197.41 μM (MAO-A)/211.12 μM (MAO-B) | [211] |
Eckol | 7.20 μM (MAO-A)/83.44 μM (MAO-B) | [212,213] |
Dieckol | 11.43 μM (MAO-A)/43.42 μM (MAO-B) | [212,213] |
Phlorofucofuroeckol-A | 9.22 μM (MAO-A)/4.89 μM (MAO-B) | [213] |
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Martins, B.; Vieira, M.; Delerue-Matos, C.; Grosso, C.; Soares, C. Biological Potential, Gastrointestinal Digestion, Absorption, and Bioavailability of Algae-Derived Compounds with Neuroprotective Activity: A Comprehensive Review. Mar. Drugs 2022, 20, 362. https://doi.org/10.3390/md20060362
Martins B, Vieira M, Delerue-Matos C, Grosso C, Soares C. Biological Potential, Gastrointestinal Digestion, Absorption, and Bioavailability of Algae-Derived Compounds with Neuroprotective Activity: A Comprehensive Review. Marine Drugs. 2022; 20(6):362. https://doi.org/10.3390/md20060362
Chicago/Turabian StyleMartins, Bruna, Mónica Vieira, Cristina Delerue-Matos, Clara Grosso, and Cristina Soares. 2022. "Biological Potential, Gastrointestinal Digestion, Absorption, and Bioavailability of Algae-Derived Compounds with Neuroprotective Activity: A Comprehensive Review" Marine Drugs 20, no. 6: 362. https://doi.org/10.3390/md20060362
APA StyleMartins, B., Vieira, M., Delerue-Matos, C., Grosso, C., & Soares, C. (2022). Biological Potential, Gastrointestinal Digestion, Absorption, and Bioavailability of Algae-Derived Compounds with Neuroprotective Activity: A Comprehensive Review. Marine Drugs, 20(6), 362. https://doi.org/10.3390/md20060362