Marine Natural Products: Promising Candidates in the Modulation of Gut-Brain Axis towards Neuroprotection
Abstract
:1. Introduction
2. Gut Microbiome and Gut-Brain Axis in Diseases
3. Gut-Brain Axis in Neurodegenerative Disease
4. Marine-Derived Natural Products and Associated Sources
5. Marine-Derived Natural Products against Diseases: Approaches to the Gut-Brain Axis
5.1. Carotenoids: Fucoxanthin, Astaxanthin, and Lycopene
5.2. Polysaccharides: Fucoidan, Chitosan, Alginate, and Laminarin
5.3. Macrolactins/Anthraquinones: Macrolactin A
5.4. Diterpenes/Sesquiterpenes: Lobocrasol, Excavatolide B, Crassumol E, and Zonarol
5.5. Phytosterols: Fucosterol and Solomonsterol A
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Gottlieb, M.G.V.; Closs, V.E.; Junges, V.M.; Schwanke, C.H.A. Impact of human aging and modern lifestyle on gut microbiota. Crit. Rev. Food Sci. Nutr. 2017, 58, 1557–1564. [Google Scholar] [CrossRef]
- Cryan, J.F.; O’Riordan, K.J.; Sandhu, K.; Peterson, V.; Dinan, T.G. The gut microbiome in neurological disorders. Lancet Neurol. 2020, 19, 179–194. [Google Scholar] [CrossRef]
- 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]
- Vaiserman, A.M.; Koliada, A.K.; Marotta, F. Gut microbiota: A player in aging and a target for anti-aging intervention. Ageing Res. Rev. 2017, 35, 36–45. [Google Scholar] [CrossRef]
- Rogers, G.B.; Keating, D.J.; Young, R.L.; Wong, M.-L.; Licinio, J.; Wesselingh, S. From gut dysbiosis to altered brain function and mental illness: Mechanisms and pathways. Mol. Psychiatry 2016, 21, 738–748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heiss, C.N.; Olofsson, L.E. The role of the gut microbiota in development, function and disorders of the central nervous system and the enteric nervous system. J. Neuroendocr. 2019, 31, e12684. [Google Scholar] [CrossRef]
- Grenham, S.; Clarke, G.; Cryan, J.F.; Dinan, T.G. Brain–gut–microbe communication in health and disease. Front. Physiol. 2011, 2, 94. [Google Scholar] [CrossRef] [Green Version]
- Xu, N.; Fan, W.; Zhou, X.; Liu, Y.; Ma, P.; Qi, S.; Gu, B. Probiotics decrease depressive behaviors induced by constipation via activating the AKT signaling pathway. Metab. Brain Dis. 2018, 33, 1625–1633. [Google Scholar] [CrossRef] [PubMed]
- Patterson, T.T.; Grandhi, R. Gut Microbiota and Neurologic Diseases and Injuries. Taurine 9 2020, 73–91. [Google Scholar] [CrossRef]
- Mukhtar, K.; Nawaz, H.; Abid, S. Functional gastrointestinal disorders and gut-brain axis: What does the future hold? World J. Gastroenterol. 2019, 25, 552–566. [Google Scholar] [CrossRef]
- Suganya, K.; Koo, B.-S. Gut–Brain Axis: Role of Gut Microbiota on Neurological Disorders and How Probiotics/Prebiotics Beneficially Modulate Microbial and Immune Pathways to Improve Brain Functions. Int. J. Mol. Sci. 2020, 21, 7551. [Google Scholar] [CrossRef]
- Tilocca, B.; Pieroni, L.; Soggiu, A.; Britti, D.; Bonizzi, L.; Roncada, P.; Greco, V. Gut–Brain Axis and Neurodegeneration: State-of-the-Art of Meta-Omics Sciences for Microbiota Characterization. Int. J. Mol. Sci. 2020, 21, 4045. [Google Scholar] [CrossRef] [PubMed]
- Abbaszadeh, F.; Fakhri, S.; Khan, H. Targeting apoptosis and autophagy following spinal cord injury: Therapeutic approaches to polyphenols and candidate phytochemicals. Pharmacol. Res. 2020, 160, 105069. [Google Scholar] [CrossRef]
- Renaud, J.; Martinoli, M.-G. Considerations for the Use of Polyphenols as Therapies in Neurodegenerative Diseases. Int. J. Mol. Sci. 2019, 20, 1883. [Google Scholar] [CrossRef] [Green Version]
- 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] [Green Version]
- Grochowska, M.; Laskus, T.; Radkowski, M. Gut Microbiota in Neurological Disorders. Arch. Immunol. Ther. Exp. 2019, 67, 375–383. [Google Scholar] [CrossRef] [Green Version]
- Guarner, F.; Malagelada, J.-R. Gut flora in health and disease. Lancet 2003, 361, 512–519. [Google Scholar] [CrossRef]
- Wang, Y.; Xu, E.; Musich, P.R.; Lin, F. Mitochondrial dysfunction in neurodegenerative diseases and the potential countermeasure. CNS Neurosci. Ther. 2019, 25, 816–824. [Google Scholar] [CrossRef] [Green Version]
- Dinan, T.G.; Cryan, J.F. Regulation of the stress response by the gut microbiota: Implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012, 37, 1369–1378. [Google Scholar] [CrossRef] [PubMed]
- Eckburg, P.B.; Bik, E.M.; Bernstein, C.N.; Purdom, E.; Dethlefsen, L.; Sargent, M.; Gill, S.R.; Nelson, K.E.; Relman, D.A. Diversity of the Human Intestinal Microbial Flora. Science 2005, 308, 1635–1638. [Google Scholar] [CrossRef] [Green Version]
- Konturek, S.J.; Konturek, J.W.; Pawlik, T.; Brzozowski, T. Brain-gut axis and its role in the control of food intake. J. Physiol. Pharmacol. 2004, 55, 137–154. [Google Scholar] [PubMed]
- Gubert, C.; Kong, G.; Renoir, T.; Hannan, A.J. Exercise, diet and stress as modulators of gut microbiota: Implications for neurodegenerative diseases. Neurobiol. Dis. 2020, 134, 104621. [Google Scholar] [CrossRef]
- Bălașa, A.F.; Chircov, C.; Grumezescu, A.M. Marine Biocompounds for Neuroprotection—A Review. Mar. Drugs 2020, 18, 290. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.K.; Shin, C. The Microbiota-Gut-Brain Axis in Neuropsychiatric Disorders: Pathophysiological Mechanisms and Novel Treatments. Curr. Neuropharmacol. 2018, 16, 559–573. [Google Scholar] [CrossRef] [PubMed]
- Rubio, C.A.; Huang, C.B. Quantification of the sulphomucin-producing cell population of the colonic mucosa during protracted stress in rats. In Vivo 1992, 6, 81–84. [Google Scholar] [PubMed]
- Nie, Y.; Luo, F.; Lin, Q. Dietary nutrition and gut microflora: A promising target for treating diseases. Trends Food Sci. Technol. 2018, 75, 72–80. [Google Scholar] [CrossRef]
- Mayer, E.A. Gut feelings: The emerging biology of gut–brain communication. Nat. Rev. Neurosci. 2011, 12, 453–466. [Google Scholar] [CrossRef]
- Neufeld, K.M.; Mao, Y.K.; Bienenstock, J.; Foster, J.A.; Kunze, W.A. The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse. Neurogastroenterol. Motil. 2013, 25, 183-e88. [Google Scholar] [CrossRef]
- Sudo, N.; Chida, Y.; Aiba, Y.; Sonoda, J.; Oyama, N.; Yu, X.-N.; Kubo, C.; Koga, Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 2004, 558, 263–275. [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.e3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Furness, J.B. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol. 2012, 9, 286–294. [Google Scholar] [CrossRef] [PubMed]
- Wehrwein, E.A.; Orer, H.S.; Barman, S.M. Overview of the Anatomy, Physiology, and Pharmacology of the Autonomic Nervous System. Compr. Physiol. 2016, 6, 1239–1278. [Google Scholar] [CrossRef]
- Rhee, S.H.; Pothoulakis, C.; Mayer, E.A. Principles and clinical implications of the brain–gut–enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 2009, 6, 306–314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alonso, C.; Guilarte, M.; Vicario, M.; Ramos, L.; Ramadan, Z.; Antolín, M.; Martínez, C.; Rezzi, S.; Saperas, E.; Kochhar, S.; et al. Maladaptive Intestinal Epithelial Responses to Life Stress May Predispose Healthy Women to Gut Mucosal Inflammation. Gastroenterology 2008, 135, 163–172. [Google Scholar] [CrossRef]
- Patrick, K.L.; Bell, S.L.; Weindel, C.G.; Watson, R.O. Exploring the “Multiple-Hit Hypothesis” of Neurodegenerative Disease: Bacterial Infection Comes Up to Bat. Front. Cell. Infect. Microbiol. 2019, 9, 138. [Google Scholar] [CrossRef] [Green Version]
- Pellegrini, C.; Antonioli, L.; Calderone, V.; Colucci, R.; Fornai, M.; Blandizzi, C. Microbiota-gut-brain axis in health and disease: Is NLRP3 inflammasome at the crossroads of microbiota-gut-brain communications? Prog. Neurobiol. 2020, 191, 101806. [Google Scholar] [CrossRef] [PubMed]
- Tolhurst, G.; Heffron, H.; Lam, Y.S.; Parker, H.E.; Habib, A.M.; Diakogiannaki, E.; Cameron, J.; Grosse, J.; Reimann, F.; Gribble, F.M. Short-Chain Fatty Acids Stimulate Glucagon-Like Peptide-1 Secretion via the G-Protein-Coupled Receptor FFAR2. Diabetes 2011, 61, 364–371. [Google Scholar] [CrossRef] [Green Version]
- Yano, J.M.; Yu, K.; Donaldson, G.P.; Shastri, G.G.; Ann, P.; Ma, L.; Nagler, C.R.; Ismagilov, R.F.; Mazmanian, S.K.; Hsiao, E.Y. Indigenous Bacteria from the Gut Microbiota Regulate Host Serotonin Biosynthesis. Cell 2015, 161, 264–276. [Google Scholar] [CrossRef] [Green Version]
- Williams, B.B.; Van Benschoten, A.H.; Cimermancic, P.; Donia, M.S.; Zimmermann, M.; Taketani, M.; Ishihara, A.; Kashyap, P.C.; Fraser, J.S.; Fischbach, M.A. Discovery and Characterization of Gut Microbiota Decarboxylases that Can Produce the Neurotransmitter Tryptamine. Cell Host Microbe 2014, 16, 495–503. [Google Scholar] [CrossRef] [Green Version]
- Jiang, C.; Li, G.; Huang, P.; Liu, Z.; Zhao, B. The Gut Microbiota and Alzheimer’s Disease. J. Alzheimer’s Dis. 2017, 58, 1–15. [Google Scholar] [CrossRef]
- Zhao, L.; Xiong, Q.; Stary, C.M.; Mahgoub, O.K.; Ye, Y.; Gu, L.; Xiong, X.; Zhu, S. Bidirectional gut-brain-microbiota axis as a potential link between inflammatory bowel disease and ischemic stroke. J. Neuroinflamm. 2018, 15, 139. [Google Scholar] [CrossRef]
- Barrett, E.; Ross, R.P.; O’Toole, P.W.; Fitzgerald, G.F.; Stanton, C. γ-Aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 2012, 113, 411–417. [Google Scholar] [CrossRef]
- Asano, Y.; Hiramoto, T.; Nishino, R.; Aiba, Y.; Kimura, T.; Yoshihara, K.; Koga, Y.; Sudo, N. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am. J. Physiol. Liver Physiol. Gastrointest. Liver Physiol. 2012, 303, G1288–G1295. [Google Scholar] [CrossRef] [Green Version]
- Zarneshan, S.N.; Fakhri, S.; Farzaei, M.H.; Khan, H.; Saso, L. Astaxanthin targets PI3K/Akt signaling pathway toward potential therapeutic applications. Food Chem. Toxicol. 2020, 145, 111714. [Google Scholar] [CrossRef] [PubMed]
- Haghikia, A.; Jörg, S.; Duscha, A.; Berg, J.; Manzel, A.; Waschbisch, A.; Hammer, A.; Lee, D.-H.; May, C.; Wilck, N.; et al. Dietary Fatty Acids Directly Impact Central Nervous System Autoimmunity via the Small Intestine. Immunity 2015, 43, 817–829. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- GBD 2015 Neurological Disorders Collaborator Group. Global, regional, and national burden of neurological disorders during 1990–2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet Neurol. 2017, 16, 877–897. [Google Scholar] [CrossRef] [Green Version]
- Endres, K.; Schäfer, K.-H. Influence of Commensal Microbiota on the Enteric Nervous System and Its Role in Neurodegenerative Diseases. J. Innate Immun. 2018, 10, 172–180. [Google Scholar] [CrossRef]
- Peterson, C.T. Dysfunction of the Microbiota-Gut-Brain Axis in Neurodegenerative Disease: The Promise of Therapeutic Modulation with Prebiotics, Medicinal Herbs, Probiotics, and Synbiotics. J. Evid. Based Integr. Med. 2020, 25, 2515690X20957225. [Google Scholar] [CrossRef] [PubMed]
- Zhuang, Z.-Q.; Shen, L.-L.; Li, W.-W.; Fu, X.; Zeng, F.; Gui, L.; Lü, Y.; Cai, M.; Zhu, C.; Tan, Y.-L.; et al. Gut Microbiota is Altered in Patients with Alzheimer’s Disease. J. Alzheimer’s Dis. 2018, 63, 1337–1346. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Minter, M.R.; Zhang, C.; Leone, V.; Ringus, D.L.; Zhang, X.; Oyler-Castrillo, P.; Musch, M.W.; Liao, F.; Ward, J.F.; Holtzman, D.M.; et al. Antibiotic-induced perturbations in gut microbial diversity influences neuro-inflammation and amyloidosis in a murine model of Alzheimer’s disease. Sci. Rep. 2016, 6, 30028. [Google Scholar] [CrossRef]
- Haran, J.P.; Bhattarai, S.K.; Foley, S.E.; Dutta, P.; Ward, D.V.; Bucci, V.; McCormick, B.A. Alzheimer’s Disease Microbiome Is Associated with Dysregulation of the Anti-Inflammatory P-Glycoprotein Pathway. mBio 2019, 10, e00632-19. [Google Scholar] [CrossRef] [Green Version]
- Tejera, D.; Mercan, D.; Sanchez-Caro, J.M.; Hanan, M.; Greenberg, D.; Soreq, H.; Latz, E.; Golenbock, D.; Heneka, M.T. Systemic inflammation impairs microglial Aβ clearance through NLRP 3 inflammasome. EMBO J. 2019, 38, e101064. [Google Scholar] [CrossRef] [PubMed]
- Domingues, C.; Silva, O.A.D.C.E.; Henriques, A.G. Impact of Cytokines and Chemokines on Alzheimer’s Disease Neuropathological Hallmarks. Curr. Alzheimer Res. 2017, 14, 870–882. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, C.; Zhao, S.; Zhu, Y.; Fan, Z.; Wang, J.; Zhang, B.; Chen, Y. Microbiota-gut-brain axis and toll-like receptors in Alzheimer’s disease. Comput. Struct. Biotechnol. J. 2019, 17, 1309–1317. [Google Scholar] [CrossRef]
- Hill, J.M.; Lukiw, W.J. Microbial-generated amyloids and Alzheimer’s disease (AD). Front. Aging Neurosci. 2015, 7, 9. [Google Scholar] [CrossRef] [Green Version]
- Adamczyk-Sowa, M.; Medrek, A.; Madej, P.; Michlicka, W.; Dobrakowski, P. Does the Gut Microbiota Influence Immunity and Inflammation in Multiple Sclerosis Pathophysiology? J. Immunol. Res. 2017, 2017, 1–14. [Google Scholar] [CrossRef]
- Gerhardt, S.; Mohajeri, M.H. Changes of Colonic Bacterial Composition in Parkinson’s Disease and Other Neurodegenerative Diseases. Nutrients 2018, 10, 708. [Google Scholar] [CrossRef] [Green Version]
- Mantovani, S.; Smith, S.S.; Gordon, R.; O’Sullivan, J.D. An overview of sleep and circadian dysfunction in Parkinson’s disease. J. Sleep Res. 2018, 27, e12673. [Google Scholar] [CrossRef] [Green Version]
- Pouclet, H.; Lebouvier, T.; Coron, E.; Varannes, S.B.D.; Neunlist, M.; Derkinderen, P. A comparison between colonic submucosa and mucosa to detect Lewy pathology in Parkinson’s disease. Neurogastroenterol. Motil. 2012, 24, e202–e205. [Google Scholar] [CrossRef] [PubMed]
- Scheperjans, F.; Aho, V.; Pereira, P.A.; 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]
- Bravo, J.A.; Forsythe, P.; Chew, M.V.; Escaravage, E.; Savignac, H.M.; Dinan, T.G.; Bienenstock, J.; Cryan, J.F. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. USA 2011, 108, 16050–16055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abildgaard, A.; Elfving, B.; Hokland, M.; Wegener, G.; Lund, S. Probiotic treatment reduces depressive-like behaviour in rats independently of diet. Psychoneuroendocrinology 2017, 79, 40–48. [Google Scholar] [CrossRef]
- Roy, A.; Karoum, F.; Pollack, S. Marked Reduction in Indexes of Dopamine Metabolism Among Patients with Depression Who Attempt Suicide. Arch. Gen. Psychiatry 1992, 49, 447–450. [Google Scholar] [CrossRef]
- Cheung, S.G.; Goldenthal, A.R.; Uhlemann, A.-C.; Mann, J.J.; Miller, J.M.; Sublette, M.E. Systematic Review of Gut Microbiota and Major Depression. Front. Psychiatry 2019, 10, 34. [Google Scholar] [CrossRef] [Green Version]
- Du, Y.; Gao, X.-R.; Peng, L.; Ge, J.-F. Crosstalk between the microbiota-gut-brain axis and depression. Heliyon 2020, 6, e04097. [Google Scholar] [CrossRef]
- Whitehead, W.E.; Palsson, O.; Jones, K.R. Systematic review of the comorbidity of irritable bowel syndrome with other disorders: What are the causes and implications? Gastroenterology 2002, 122, 1140–1156. [Google Scholar] [CrossRef] [PubMed]
- Neufeld, K.M.; Kang, N.; Bienenstock, J.; Foster, J.A. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol. Motil. 2010, 23, 255-e119. [Google Scholar] [CrossRef] [PubMed]
- Heijtz, R.D.; Wang, S.; Anuar, F.; Qian, Y.; Björkholm, B.; Samuelsson, A.; Hibberd, M.L.; Forssberg, H.; Pettersson, S. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. USA 2011, 108, 3047–3052. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zheng, P.; Zeng, B.; Zhou, C.; Liu, M.; Fang, Z.; Xu, X.; Zeng, L.; Chen, J.; Fan, S.; Du, X.; et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol. Psychiatry 2016, 21, 786–796. [Google Scholar] [CrossRef]
- Kunze, W.A.; Mao, Y.K.; Wang, B.; Huizinga, J.D.; Ma, X.; Forsythe, P.; Bienenstock, J. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J. Cell. Mol. Med. 2009, 13, 2261–2270. [Google Scholar] [CrossRef]
- Duca, F.A.; Swartz, T.D.; Sakar, Y.; Covasa, M. Increased Oral Detection, but Decreased Intestinal Signaling for Fats in Mice Lacking Gut Microbiota. PLoS ONE 2012, 7, e39748. [Google Scholar] [CrossRef] [Green Version]
- Di Gioia, D.; Cionci, N.B.; Baffoni, L.; Amoruso, A.; Pane, M.; Mogna, L.; Gaggìa, F.; Lucenti, M.A.; Bersano, E.; Cantello, R.; et al. A prospective longitudinal study on the microbiota composition in amyotrophic lateral sclerosis. BMC Med. 2020, 18, 153. [Google Scholar] [CrossRef]
- Wu, S.; Yi, J.; Zhang, Y.-G.; Zhou, J.; Sun, J. Leaky intestine and impaired microbiome in an amyotrophic lateral sclerosis mouse model. Physiol. Rep. 2015, 3, e12356. [Google Scholar] [CrossRef] [Green Version]
- 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] [PubMed] [Green Version]
- Erber, A.C.; Cetin, H.; Berry, D.; Schernhammer, E.S. The role of gut microbiota, butyrate and proton pump inhibitors in amyotrophic lateral sclerosis: A systematic review. Int. J. Neurosci. 2019, 130, 727–735. [Google Scholar] [CrossRef]
- Obrenovich, M.; Jaworski, H.; Tadimalla, T.; Mistry, A.; Sykes, L.; Perry, G.; Bonomo, R.A. The Role of the Microbiota–Gut–Brain Axis and Antibiotics in ALS and Neurodegenerative Diseases. Microorganisms 2020, 8, 784. [Google Scholar] [CrossRef] [PubMed]
- Farrokhi, V.; Nemati, R.; Nichols, F.C.; Yao, X.; Anstadt, E.; Fujiwara, M.; Grady, J.; Wakefield, D.; Castro, W.; Donaldson, J.; et al. Bacterial lipodipeptide, Lipid 654, is a microbiome-associated biomarker for multiple sclerosis. Clin. Transl. Immunol. 2013, 2, e8. [Google Scholar] [CrossRef] [PubMed]
- Uzal, F.A.; Kelly, W.R.; Morris, W.E.; Bermudez, J.; Baisón, M. The pathology of peracute experimental Clostridium perfringens type D enterotoxemia in sheep. J. Vet. Diagn. Investig. 2004, 16, 403–411. [Google Scholar] [CrossRef] [Green Version]
- Barnett, M.H.; Parratt, J.D.E.; Cho, E.-S.; Prineas, J.W. Immunoglobulins and complement in postmortem multiple sclerosis tissue. Ann. Neurol. 2009, 65, 32–46. [Google Scholar] [CrossRef]
- Park, A.M.; Omura, S.; Fujita, M.; Sato, F.; Tsunoda, I. Helicobacter pylori and gut microbiota in multiple sclerosis versus Alzheimer’s disease: 10 pitfalls of microbiome studies. Clin. Exp. Neuroimmunol. 2017, 8, 215–232. [Google Scholar] [CrossRef] [Green Version]
- Van Sadelhoff, J.H.J.; Pardo, P.P.; Wu, J.; Garssen, J.; Van Bergenhenegouwen, J.; Hogenkamp, A.; Hartog, A.; Kraneveld, A.D. The Gut-Immune-Brain Axis in Autism Spectrum Disorders; A Focus on Amino Acids. Front. Endocrinol. 2019, 10, 247. [Google Scholar] [CrossRef]
- Ochoa-Repáraz, J.; Mielcarz, D.W.; Ditrio, L.E.; Burroughs, A.R.; Foureau, D.M.; Haque-Begum, S.; Kasper, L.H. Role of Gut Commensal Microflora in the Development of Experimental Autoimmune Encephalomyelitis. J. Immunol. 2009, 183, 6041–6050. [Google Scholar] [CrossRef] [Green Version]
- Rao, A.V.; Bested, A.C.; Beaulne, T.M.; Katzman, A.M.; Iorio, C.; Berardi, J.M.; Logan, A.C. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 2009, 1, 6. [Google Scholar] [CrossRef] [Green Version]
- Pulikkan, J.; Maji, A.; Dhakan, D.B.; Saxena, R.; Mohan, B.; Anto, M.M.; Agarwal, N.; Grace, T.; Sharma, V.K. Gut Microbial Dysbiosis in Indian Children with Autism Spectrum Disorders. Microb. Ecol. 2018, 76, 1102–1114. [Google Scholar] [CrossRef] [PubMed]
- Fattorusso, A.; Di Genova, L.; Dell’Isola, G.B.; Mencaroni, E.; Esposito, S. Autism Spectrum Disorders and the Gut Microbiota. Nutrients 2019, 11, 521. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, T.; Fu, F.; Han, B.; Zhang, L.; Zhang, X. Danshensu ameliorates the cognitive decline in streptozotocin-induced diabetic mice by attenuating advanced glycation end product-mediated neuroinflammation. J. Neuroimmunol. 2012, 245, 79–86. [Google Scholar] [CrossRef]
- Ashwood, P.; Enstrom, A.; Krakowiak, P.; Hertz-Picciotto, I.; Hansen, R.L.; Croen, L.A.; Ozonoff, S.; Pessah, I.N.; DeWater, J.; Van De Water, J. Decreased transforming growth factor beta1 in autism: A potential link between immune dysregulation and impairment in clinical behavioral outcomes. J. Neuroimmunol. 2008, 204, 149–153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vitale, G.A.; Coppola, D.; Esposito, F.P.; Buonocore, C.; Ausuri, J.; Tortorella, E.; De Pascale, D. Antioxidant Molecules from Marine Fungi: Methodologies and Perspectives. Antioxidants 2020, 9, 1183. [Google Scholar] [CrossRef]
- Spitz, J.; Hecht, G.; Taveras, M.; Aoys, E.; Alverdy, J. The effect of dexamethasone administration on rat intestinal permeability: The role of bacterial adherence. Gastroenterology 1994, 106, 35–41. [Google Scholar] [CrossRef]
- Unsal, H.; Balkaya, M.; Unsal, C.; Biyik, H.; Başbülbül, G.; Poyrazoğlu, E. The short-term effects of different doses of dexamethasone on the numbers of some bacteria in the ileum. Dig. Dis. Sci. 2008, 53, 1842–1845. [Google Scholar] [CrossRef]
- Bengmark, S. Gut microbiota, immune development and function. Pharmacol. Res. 2013, 69, 87–113. [Google Scholar] [CrossRef] [PubMed]
- Daulatzai, M.A. Role of Stress, Depression, and Aging in Cognitive Decline and Alzheimer’s Disease. Curr. Top Behav. Neurobiol. 2014, 18, 265–296. [Google Scholar] [CrossRef]
- Maes, M.; Kubera, M.; Leunis, J.-C.; Berk, M. Increased IgA and IgM responses against gut commensals in chronic depression: Further evidence for increased bacterial translocation or leaky gut. J. Affect. Disord. 2012, 141, 55–62. [Google Scholar] [CrossRef] [PubMed]
- Julio-Pieper, M.; Bravo, J.A.; Aliaga, E.; Gotteland, M. Review article: Intestinal barrier dysfunction and central nervous system disorders—A controversial association. Aliment. Pharmacol. Ther. 2014, 40, 1187–1201. [Google Scholar] [CrossRef]
- Daulatzai, M.A. Chronic Functional Bowel Syndrome Enhances Gut-Brain Axis Dysfunction, Neuroinflammation, Cognitive Impairment, and Vulnerability to Dementia. Neurochem. Res. 2014, 39, 624–644. [Google Scholar] [CrossRef] [PubMed]
- Kelly, J.R.; Kennedy, P.J.; Cryan, J.F.; Dinan, T.G.; Clarke, G.; Hyland, N.P. Breaking down the barriers: The gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front. Cell. Neurosci. 2015, 9, 392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caesar, R.; Reigstad, C.S.; Bäckhed, H.K.; Reinhardt, C.; Ketonen, M.; Lundén, G.Ö.; Cani, P.; Bäckhed, F. Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 2012, 61, 1701–1707. [Google Scholar] [CrossRef] [Green Version]
- Hyland, N.P.; Cryan, J.F. Microbe-host interactions: Influence of the gut microbiota on the enteric nervous system. Dev. Biol. 2016, 417, 182–187. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.; Luan, X.; Liu, Q.; Wang, J.; Chang, X.; Snijders, A.M.; Mao, J.-H.; Secombe, J.; Dan, Z.; Chen, J.-H.; et al. Drosophila Histone Demethylase KDM5 Regulates Social Behavior through Immune Control and Gut Microbiota Maintenance. Cell Host Microbe 2019, 25, 537–552. [Google Scholar] [CrossRef] [Green Version]
- Caputi, V.; Marsilio, I.; Filpa, V.; Cerantola, S.; Orso, G.; Bistoletti, M.; Paccagnella, N.; De Martin, S.; Montopoli, M.; Dall’Acqua, S.; et al. Antibiotic-induced dysbiosis of the microbiota impairs gut neuromuscular function in juvenile mice. Br. J. Pharmacol. 2017, 174, 3623–3639. [Google Scholar] [CrossRef] [Green Version]
- Nikapitiya, C. Bioactive Secondary Metabolites from Marine Microbes for Drug Discovery. Adv. Food Nutr. Res. 2012, 65, 363–387. [Google Scholar] [CrossRef]
- Petersen, L.-E.; Kellermann, M.Y.; Schupp, P.J. Secondary Metabolites of Marine Microbes: From Natural Products Chemistry to Chemical Ecology. YOUMARES 9 Ocean Res. Future 2019, 159–180. [Google Scholar] [CrossRef] [Green Version]
- Mayer, A.M.; Hamann, M.T. Marine pharmacology in 1999: Compounds with antibacterial, anticoagulant, antifungal, anthelmintic, anti-inflammatory, antiplatelet, antiprotozoal and antiviral activities affecting the cardiovascular, endocrine, immune and nervous systems, and other miscellaneous mechanisms of action. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2002, 132, 315–339. [Google Scholar] [CrossRef]
- Cheng, M.-M.; Tang, X.-L.; Sun, Y.-T.; Song, D.-Y.; Cheng, Y.-J.; Liu, H.; Li, P.-L.; Li, G.-Q. Biological and Chemical Diversity of Marine Sponge-Derived Microorganisms over the Last Two Decades from 1998 to 2017. Molecules 2020, 25, 853. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Höller, U.; Wright, A.D.; Matthee, G.F.; Konig, G.M.; Draeger, S.; Aust, H.-J.; Schulz, B. Fungi from marine sponges: Diversity, biological activity and secondary metabolites. Mycol. Res. 2000, 104, 1354–1365. [Google Scholar] [CrossRef]
- Hanif, N.; Murni, A.; Tanaka, C.; Tanaka, J. Marine Natural Products from Indonesian Waters. Mar. Drugs 2019, 17, 364. [Google Scholar] [CrossRef] [Green Version]
- Liang, X.; Luo, D.; Luesch, H. Advances in exploring the therapeutic potential of marine natural products. Pharmacol. Res. 2019, 147, 104373. [Google Scholar] [CrossRef]
- Pietra, F. Secondary metabolites from marine microorganisms: Bacteria, protozoa, algae and fungi. Achievements and prospects. Nat. Prod. Rep. 1997, 14, 453–464. [Google Scholar] [CrossRef] [PubMed]
- Blunt, J.W.; Carroll, A.R.; Copp, B.R.; Davis, R.A.; Keyzers, R.A.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 2018, 35, 8–53. [Google Scholar] [CrossRef] [Green Version]
- Leandro, A.; Pereira, L.; Gonçalves, A.M.M. Diverse Applications of Marine Macroalgae. Mar. Drugs 2019, 18, 17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Salehi, B.; Sharifi-Rad, J.; Seca, A.M.L.; Pinto, D.C.G.A.; Michalak, I.; Trincone, A.; Mishra, A.P.; Nigam, M.; Zam, W.; Martins, N. Current Trends on Seaweeds: Looking at Chemical Composition, Phytopharmacology, and Cosmetic Applications. Molecules 2019, 24, 4182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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]
- Vasili, E.; Dominguez-Meijide, A.; Outeiro, T.F. Spreading of α-Synuclein and Tau: A Systematic Comparison of the Mechanisms Involved. Front. Mol. Neurosci. 2019, 12, 107. [Google Scholar] [CrossRef] [Green Version]
- Ganguly, G.; Chakrabarti, S.; Chatterjee, U.; Saso, L. Proteinopathy, oxidative stress and mitochondrial dysfunction: Cross talk in Alzheimer’s disease and Parkinson’s disease. Drug Des. Devel. Ther. 2017, 11, 797–810. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Islam, M.T. Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol. Res. 2017, 39, 73–82. [Google Scholar] [CrossRef] [PubMed]
- León, R.; Garcia, A.G.; Marco-Contelles, J. Recent advances in the multitarget-directed ligands approach for the treatment of Alzheimer’s disease. Med. Res. Rev. 2013, 33, 139–189. [Google Scholar] [CrossRef]
- Galasso, C.; Corinaldesi, C.; Sansone, C. Carotenoids from Marine Organisms: Biological Functions and Industrial Applications. Antioxidants 2017, 6, 96. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grimmig, B.; Kim, S.-H.; Nash, K.; Bickford, P.C.; Shytle, R.D. Neuroprotective mechanisms of astaxanthin: A potential therapeutic role in preserving cognitive function in age and neurodegeneration. GeroScience 2017, 39, 19–32. [Google Scholar] [CrossRef]
- Masters, K.-S.; Bräse, S. Xanthones from Fungi, Lichens, and Bacteria: The Natural Products and Their Synthesis. Chem. Rev. 2012, 112, 3717–3776. [Google Scholar] [CrossRef]
- Anantachoke, N.; Tuchinda, P.; Kuhakarn, C.; Pohmakotr, M.; Reutrakul, V. Prenylated caged xanthones: Chemistry and biology. Pharm. Biol. 2011, 50, 78–91. [Google Scholar] [CrossRef] [Green Version]
- Chhouk, K.; Quitain, A.T.; Gaspillo, P.-A.D.; Maridable, J.B.; Sasaki, M.; Shimoyama, Y.; Goto, M. Supercritical carbon dioxide-mediated hydrothermal extraction of bioactive compounds from Garcinia Mangostana pericarp. J. Supercrit. Fluids 2016, 110, 167–175. [Google Scholar] [CrossRef]
- Yoo, J.-H.; Kang, K.; Jho, E.H.; Chin, Y.-W.; Kim, J.; Nho, C.W. α-and γ-Mangostin inhibit the proliferation of colon cancer cells via β-catenin gene regulation in Wnt/cGMP signalling. Food Chem. 2011, 129, 1559–1566. [Google Scholar] [CrossRef]
- Iinuma, M.; Tosa, H.; Tanaka, T.; Asai, F.; Kobayashl, Y.; Shimano, R.; Miyauchi, K.-I. Antibacterial Activity of Xanthones from Guttiferaeous Plants against Methicillin-resistant Staphylococcus aureus. J. Pharm. Pharmacol. 1996, 48, 861–865. [Google Scholar] [CrossRef]
- Shan, T.; Ma, Q.; Guo, K.; Liu, J.; Li, W.; Wang, F.; Wu, E. Xanthones from Mangosteen Extracts as Natural Chemopreventive Agents: Potential Anticancer Drugs. Curr. Mol. Med. 2011, 11, 666–677. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Lateff, A.; Klemke, C.; König, G.M.; Wright, A.D. Two New Xanthone Derivatives from the Algicolous Marine Fungus Wardomyces anomalus. J. Nat. Prod. 2003, 66, 706–708. [Google Scholar] [CrossRef] [PubMed]
- Shiratori, K.; Ohgami, K.; Ilieva, I.; Jin, X.-H.; Koyama, Y.; Miyashita, K.; Yoshida, K.; Kase, S.; Ohno, S. Effects of fucoxanthin on lipopolysaccharide-induced inflammation In Vitro and In Vivo. Exp. Eye Res. 2005, 81, 422–428. [Google Scholar] [CrossRef]
- Liu, M.; Li, W.; Chen, Y.; Wan, X.; Wang, J. Fucoxanthin: A promising compound for human inflammation-related diseases. Life Sci. 2020, 255, 117850. [Google Scholar] [CrossRef]
- Rengarajan, T.; Rajendran, P.; Nandakumar, N.; Balasubramanian, M.P.; Nishigaki, I. Cancer Preventive Efficacy of Marine Carotenoid Fucoxanthin: Cell Cycle Arrest and Apoptosis. Nutrients 2013, 5, 4978–4989. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miyashita, K.; Nishikawa, S.; Hosokawa, M. Therapeutic effect of fucoxanthin on metabolic syndrome and type 2 diabetes. In Nutritional and Therapeutic Interventions for Diabetes and Metabolic Syndrome; Bagchi, D., Sreejayan, N., Eds.; Academic Press: London, UK, 2012; Volume 1, pp. 367–379. [Google Scholar]
- Zhang, H.; Tang, Y.; Zhang, Y.; Zhang, S.; Qu, J.; Wang, X.; Kong, R.; Han, C.; Liu, Z. Fucoxanthin: A Promising Medicinal and Nutritional Ingredient. Evid. Based Complement. Altern. Med. 2015, 2015, 1–10. [Google Scholar] [CrossRef]
- Zou, Y.; Qian, Z.-J.; Li, Y.; Kim, M.-M.; Lee, S.-H.; Kim, S.-K. Antioxidant Effects of Phlorotannins Isolated from Ishige okamurae in Free Radical Mediated Oxidative Systems. J. Agric. Food Chem. 2008, 56, 7001–7009. [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]
- Kim, S.-K.; Pangestuti, R. Biological Activities and Potential Health Benefits of Fucoxanthin Derived from Marine Brown Algae. Adv. Food Nutr. Res. 2011, 64, 111–128. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Pangestuti, R.; Vo, T.-S.; Ngo, D.-H.; Kim, S.-K. Fucoxanthin Ameliorates Inflammation and Oxidative Reponses in Microglia. J. Agric. Food Chem. 2013, 61, 3876–3883. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Gammone, M.A.; Riccioni, G.; D’Orazio, N. Marine Carotenoids against Oxidative Stress: Effects on Human Health. Mar. Drugs 2015, 13, 6226–6246. [Google Scholar] [CrossRef] [PubMed]
- Gammone, M.A.; D’Orazio, N. Anti-Obesity Activity of the Marine Carotenoid Fucoxanthin. Mar. Drugs 2015, 13, 2196–2214. [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] [PubMed] [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]
- 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]
- 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]
- Sun, X.; Zhao, H.; Liu, Z.; Sun, X.; Zhang, D.; Wang, S.; Xu, Y.; Zhang, G.; Wang, D. Modulation of Gut Microbiota by Fucoxanthin During Alleviation of Obesity in High-Fat Diet-Fed Mice. J. Agric. Food Chem. 2020, 68, 5118–5128. [Google Scholar] [CrossRef] [PubMed]
- Guo, B.; Yang, B.; Pang, X.; Chen, T.; Chen, F.; Cheng, K.-W. Fucoxanthin modulates cecal and fecal microbiota differently based on diet. Food Funct. 2019, 10, 5644–5655. [Google Scholar] [CrossRef]
- Liu, Z.; Sun, X.; Sun, X.; Wang, S.; Xu, Y. Fucoxanthin Isolated from Undaria pinnatifida Can Interact with Escherichia coli and lactobacilli in the Intestine and Inhibit the Growth of Pathogenic Bacteria. J. Ocean Univ. China 2019, 18, 926–932. [Google Scholar] [CrossRef]
- Corinaldesi, C.; Barone, G.; Marcellini, F.; Dell’Anno, A.; Danovaro, R. Marine Microbial-Derived Molecules and Their Potential Use in Cosmeceutical and Cosmetic Products. Mar. Drugs 2017, 15, 118. [Google Scholar] [CrossRef]
- Viera, I.; Pérez-Gálvez, A.; Roca, M. Bioaccessibility of Marine Carotenoids. Mar. Drugs 2018, 16, 397. [Google Scholar] [CrossRef] [Green Version]
- Yuan, J.-P.; Peng, J.; Yin, K.; Wang, J.-H. Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae. Mol. Nutr. Food Res. 2010, 55, 150–165. [Google Scholar] [CrossRef] [PubMed]
- Fakhri, S.; Abbaszadeh, F.; Dargahi, L.; Jorjani, M. Astaxanthin: A mechanistic review on its biological activities and health benefits. Pharmacol. Res. 2018, 136, 1–20. [Google Scholar] [CrossRef] [PubMed]
- Khoei, H.H.; Fakhri, S.; Parvardeh, S.; Mofarahe, Z.S.; Baninameh, Z.; Vardiani, M. Astaxanthin prevents the methotrexate-induced reproductive toxicity by targeting oxidative stress in male mice. Toxin Rev. 2019, 38, 248–254. [Google Scholar] [CrossRef]
- Faraone, I.; Sinisgalli, C.; Ostuni, A.; Armentano, M.F.; Carmosino, M.; Milella, L.; Russo, D.; Labanca, F.; Khan, H. Astaxanthin anticancer effects are mediated through multiple molecular mechanisms: A systematic review. Pharmacol. Res. 2020, 155, 104689. [Google Scholar] [CrossRef]
- Bhuvaneswari, S.; Arunkumar, E.; Viswanathan, P.; Anuradha, C.V. Astaxanthin restricts weight gain, promotes insulin sensitivity and curtails fatty liver disease in mice fed a obesity-promoting diet. Process. Biochem. 2010, 45, 1406–1414. [Google Scholar] [CrossRef]
- Inoue, M.; Tanabe, H.; Matsumoto, A.; Takagi, M.; Umegaki, K.; Amagaya, S.; Takahashi, J. Astaxanthin functions differently as a selective peroxisome proliferator-activated receptor γ modulator in adipocytes and macrophages. Biochem. Pharmacol. 2012, 84, 692–700. [Google Scholar] [CrossRef] [PubMed]
- Rao, A.R.; Sarada, R.; Shylaja, M.D.; Ravishankar, G.A. Evaluation of hepatoprotective and antioxidant activity of astaxanthin and astaxanthin esters from microalga-Haematococcus pluvialis. J. Food Sci. Technol. 2015, 52, 6703–6710. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uchiyama, K.; Naito, Y.; Hasegawa, G.; Nakamura, N.; Takahashi, J.; Yoshikawa, T. Astaxanthin protects β-cells against glucose toxicity in diabetic db/db mice. Redox Rep. 2002, 7, 290–293. [Google Scholar] [CrossRef]
- Fakhri, S.; Dargahi, L.; Abbaszadeh, F.; Jorjani, M. Astaxanthin attenuates neuroinflammation contributed to the neuropathic pain and motor dysfunction following compression spinal cord injury. Brain Res. Bull. 2018, 143, 217–224. [Google Scholar] [CrossRef] [PubMed]
- Fakhri, S.; Dargahi, L.; Abbaszadeh, F.; Jorjani, M. Effects of astaxanthin on sensory-motor function in a compression model of spinal cord injury: Involvement of ERK and AKT signalling pathway. Eur. J. Pain 2019, 23, 750–764. [Google Scholar] [CrossRef]
- Fakhri, S.; Aneva, I.Y.; Farzaei, M.H.; Sobarzo-Sánchez, E. The Neuroprotective Effects of Astaxanthin: Therapeutic Targets and Clinical Perspective. Molecules 2019, 24, 2640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ambati, R.R.; Phang, S.-M.; Ravi, S.; Aswathanarayana, R.G. Astaxanthin: Sources, Extraction, Stability, Biological Activities and Its Commercial Applications—A Review. Mar. Drugs 2014, 12, 128–152. [Google Scholar] [CrossRef]
- Jackson, H.; Braun, C.L.; Ernst, H. The Chemistry of Novel Xanthophyll Carotenoids. Am. J. Cardiol. 2008, 101, S50–S57. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Shibata, T.; Hisaka, S.; Osawa, T. Astaxanthin inhibits reactive oxygen species-mediated cellular toxicity in dopaminergic SH-SY5Y cells via mitochondria-targeted protective mechanism. Brain Res. 2009, 1254, 18–27. [Google Scholar] [CrossRef]
- Barros, M.P.; Poppe, S.C.; Bondan, E.F. Neuroprotective Properties of the Marine Carotenoid Astaxanthin and Omega-3 Fatty Acids, and Perspectives for the Natural Combination of Both in Krill Oil. Nutrients 2014, 6, 1293–1317. [Google Scholar] [CrossRef] [Green Version]
- Choi, H.D.; Kang, H.E.; Yang, S.H.; Lee, M.G.; Shin, W.G. Pharmacokinetics and first-pass metabolism of astaxanthin in rats. Br. J. Nutr. 2010, 105, 220–227. [Google Scholar] [CrossRef] [Green Version]
- Park, J.S.; Chyun, J.H.; Kim, Y.K.; Line, L.L.; Chew, B.P. Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutr. Metab. 2010, 7, 18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, L.; Lyu, Y.; Srinivasagan, R.; Wu, J.; Ojo, B.; Tang, M.; El-Rassi, G.D.; Metzinger, K.; Smith, B.J.; Lucas, A.E.; et al. Astaxanthin-Shifted Gut Microbiota Is Associated with Inflammation and Metabolic Homeostasis in Mice. J. Nutr. 2020, 150, 2687–2698. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Zhao, S.; Jiao, D.; Yao, B.; Yang, S.; Li, P.; Long, M. Astaxanthin Alleviates Ochratoxin A-Induced Cecum Injury and Inflammation in Mice by Regulating the Diversity of Cecal Microbiota and TLR4/MyD88/NF-κB Signaling Pathway. Oxidative Med. Cell. Longev. 2021, 2021, 8894491. [Google Scholar] [CrossRef]
- Schweiggert, R.M.; Kopec, R.E.; Villalobos-Gutierrez, M.G.; Högel, J.; Quesada, S.; Esquivel, P.; Schwartz, S.J.; Carle, R. Carotenoids are more bioavailable from papaya than from tomato and carrot in humans: A randomised cross-over study. Br. J. Nutr. 2014, 111, 490–498. [Google Scholar] [CrossRef] [Green Version]
- Luna, R.A.; Foster, A.J. Gut brain axis: Diet microbiota interactions and implications for modulation of anxiety and depression. Curr. Opin. Biotechnol. 2015, 32, 35–41. [Google Scholar] [CrossRef] [PubMed]
- Akira, S.; Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4, 499–511. [Google Scholar] [CrossRef]
- Yan, S.; Shi, R.; Li, L.; Ma, S.; Zhang, H.; Ye, J.; Wang, J.; Pan, J.; Wang, Q.; Jin, X.; et al. Mannan Oligosaccharide Suppresses Lipid Accumulation and Appetite in Western-Diet-Induced Obese Mice Via Reshaping Gut Microbiome and Enhancing Short-Chain Fatty Acids Production. Mol. Nutr. Food Res. 2019, 63, e1900521. [Google Scholar] [CrossRef] [PubMed]
- Burcelin, R.; Garidou, L.; Pomié, C. Immuno-microbiota cross and talk: The new paradigm of metabolic diseases. Semin. Immunol. 2012, 24, 67–74. [Google Scholar] [CrossRef]
- Zhao, B.; Wu, J.; Li, J.; Bai, Y.; Luo, Y.; Ji, B.; Xia, B.; Liu, Z.; Tan, X.; Lv, J.; et al. Lycopene Alleviates DSS-Induced Colitis and Behavioral Disorders via Mediating Microbes-Gut–Brain Axis Balance. J. Agric. Food Chem. 2020, 68, 3963–3975. [Google Scholar] [CrossRef] [PubMed]
- Huang, C.; Wen, C.; Yang, M.; Gan, D.; Fan, C.; Li, A.; Li, Q.; Zhao, J.; Zhu, L.; Lu, D. Lycopene protects against t-BHP-induced neuronal oxidative damage and apoptosis via activation of the PI3K/Akt pathway. Mol. Biol. Rep. 2019, 46, 3387–3397. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.B.; Wang, R.; Yi, Y.F.; Gao, Z.; Chen, Y.Z. Lycopene mitigates β-amyloid induced inflammatory response and inhibits NF-κB signaling at the choroid plexus in early stages of Alzheimer’s disease rats. J. Nutr. Biochem. 2018, 53, 66–71. [Google Scholar] [CrossRef] [PubMed]
- Hua, Y.; Xu, N.; Ma, T.; Liu, Y.; Xu, H.; Lu, Y. Anti-Inflammatory Effect of Lycopene on Experimental Spinal Cord Ischemia Injury via Cyclooxygenase-2 Suppression. Neuroimmunomodulation 2019, 26, 84–92. [Google Scholar] [CrossRef] [PubMed]
- Wiese, M.; Bashmakov, Y.; Chalyk, N.; Nielsen, D.S.; Krych, Ł.; Kot, W.; Klochkov, V.; Pristensky, D.; Bandaletova, T.; Chernyshova, M. Prebiotic effect of lycopene and dark chocolate on gut microbiome with systemic changes in liver metabolism, skeletal muscles and skin in moderately obese persons. BioMed Res. Int. 2019, 2019, 4625279. [Google Scholar] [CrossRef]
- Florez, N.; Gonzalez-Munoz, M.J.; Ribeiro, D.; Fernandes, E.; Dominguez, H.; Freitas, M. Algae Polysaccharides’ Chemical Characterization and their Role in the Inflammatory Process. Curr. Med. Chem. 2017, 24, 149–175. [Google Scholar] [CrossRef]
- 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]
- Shang, Q.; Shan, X.; Cai, C.; Hao, J.; Li, G.; Yu, G. Correction: Dietary fucoidan modulates the gut microbiota in mice by increasing the abundance of Lactobacillus and Ruminococcaceae. Food Funct. 2016, 7, 3224–3232. [Google Scholar] [CrossRef]
- Wang, L.; Ai, C.; Wen, C.; Qin, Y.; Liu, Z.; Wang, L.; Gong, Y.; Su, C.; Wang, Z.; Song, S. Fucoidan isolated from Ascophyllum nodosum alleviates gut microbiota dysbiosis and colonic inflammation in antibiotic-treated mice. Food Funct. 2020, 11, 5595–5606. [Google Scholar] [CrossRef]
- Ikeda-Ohtsubo, W.; Nadal, A.L.; Zaccaria, E.; Iha, M.; Kitazawa, H.; Kleerebezem, M.; Brugman, S. Intestinal Microbiota and Immune Modulation in Zebrafish by Fucoidan from Okinawa Mozuku (Cladosiphon okamuranus). Front. Nutr. 2020, 7, 67. [Google Scholar] [CrossRef] [PubMed]
- Shi, H.; Chang, Y.; Gao, Y.; Wang, X.; Chen, X.; Wang, Y.; Xue, C.; Tang, Q. Dietary fucoidan of Acaudina molpadioides alters gut microbiota and mitigates intestinal mucosal injury induced by cyclophosphamide. Food Funct. 2017, 8, 3383–3393. [Google Scholar] [CrossRef]
- Kan, J.; Cheng, J.; Xu, L.; Hood, M.; Zhong, D.; Cheng, M.; Liu, Y.; Chen, L.; Du, J. The combination of wheat peptides and fucoidan protects against chronic superficial gastritis and alters gut microbiota: A double-blinded, placebo-controlled study. Eur. J. Nutr. 2019, 59, 1655–1666. [Google Scholar] [CrossRef]
- Zhang, Y.; Zuo, J.; Yan, L.; Cheng, Y.; Li, Q.; Wu, S.; Chen, L.; Thring, R.; Yang, Y.; Gao, Y.; et al. Sargassum fusiforme fucoidan alleviates high-fat diet-induced obesity and insulin resistance associated with the improvement of hepatic oxidative stress and gut microbiota profile. J. Agric. Food Chem. 2020, 68, 10626–10638. [Google Scholar] [CrossRef]
- Liu, X.-Y.; Liu, D.; Lin, G.-P.; Wu, Y.-J.; Gao, L.-Y.; Ai, C.; Huang, Y.-F.; Wang, M.-F.; El-Seedi, H.R.; Chen, X.-H.; et al. Anti-ageing and antioxidant effects of sulfate oligosaccharides from green algae Ulva lactuca and Enteromorpha prolifera in SAMP8 mice. Int. J. Biol. Macromol. 2019, 139, 342–351. [Google Scholar] [CrossRef]
- 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]
- Tang, Y.; Cui, Y.; De Agostini, A.; Zhang, L. Biological mechanisms of glycan- and glycosaminoglycan-based nutraceuticals. Prog. Mol. Biol. Transl. Sci. 2019, 163, 445–469. [Google Scholar] [CrossRef]
- Goy, R.C.; De Britto, D.; Assis, O.B.G. A review of the antimicrobial activity of chitosan. Polímeros 2009, 19, 241–247. [Google Scholar] [CrossRef]
- Younes, I.; Sellimi, S.; Rinaudo, M.; Jellouli, K.; Nasri, M. Influence of acetylation degree and molecular weight of homogeneous chitosans on antibacterial and antifungal activities. Int. J. Food Microbiol. 2014, 185, 57–63. [Google Scholar] [CrossRef] [PubMed]
- Park, P.-J.; Je, A.J.-Y.; Kim, S.-K. Free Radical Scavenging Activity of Chitooligosaccharides by Electron Spin Resonance Spectrometry. J. Agric. Food Chem. 2003, 51, 4624–4627. [Google Scholar] [CrossRef]
- Tokoro, A.; Takewaki, N.; Suzuki, K.; Mikami, T.; Suzuki, S.; Suzuki, M. Growth-inhibitory effect of hexa-N-acetylchitohexanse and chitohexaose against Meth-A solid tumor. Chem. Pharm. Bull. 1988, 36, 784–790. [Google Scholar] [CrossRef] [Green Version]
- Wiepjes, C.M.; Nota, N.M.; de Blok, C.J.; Klaver, M.; de Vries, A.L.; Wensing-Kruger, S.A.; de Jongh, R.T.; Bouman, M.-B.; Steensma, T.D.; Cohen-Kettenis, P.; et al. The Amsterdam Cohort of Gender Dysphoria Study (1972–2015): Trends in Prevalence, Treatment, and Regrets. J. Sex. Med. 2018, 15, 582–590. [Google Scholar] [CrossRef]
- He, B.; Wu, F.; Fan, L.; Li, X.-H.; Liu, Y.; Liu, Y.-J.; Ding, W.-J.; Deng, M.; Zhou, Y. Carboxymethylated chitosan protects Schwann cells against hydrogen peroxide-induced apoptosis by inhibiting oxidative stress and mitochondria dependent pathway. Eur. J. Pharmacol. 2018, 825, 48–56. [Google Scholar] [CrossRef]
- Zhang, X.; Yang, H.; Zheng, J.; Jiang, N.; Sun, G.; Bao, X.; Lin, A.; Liu, H. Chitosan oligosaccharides attenuate loperamide-induced constipation through regulation of gut microbiota in mice. Carbohydr. Polym. 2021, 253, 117218. [Google Scholar] [CrossRef] [PubMed]
- Zheng, J.; Yuan, X.; Cheng, G.; Jiao, S.; Feng, C.; Zhao, X.; Yin, H.; Du, Y.; Liu, H. Chitosan oligosaccharides improve the disturbance in glucose metabolism and reverse the dysbiosis of gut microbiota in diabetic mice. Carbohydr. Polym. 2018, 190, 77–86. [Google Scholar] [CrossRef]
- Xu, Y.; Mao, H.; Yang, C.; Du, H.; Wang, H.; Tu, J. Effects of chitosan nanoparticle supplementation on growth performance, humoral immunity, gut microbiota and immune responses after lipopolysaccharide challenge in weaned pigs. J. Anim. Physiol. Anim. Nutr. 2019, 104, 597–605. [Google Scholar] [CrossRef]
- Yu, T.; Wang, Y.; Chen, S.; Hu, M.; Wang, Z.; Wu, G.; Ma, X.; Chen, Z.; Zheng, C. Low-Molecular-Weight Chitosan Supplementation Increases the Population of Prevotella in the Cecal Contents of Weanling Pigs. Front. Microbiol. 2017, 8, 2182. [Google Scholar] [CrossRef] [PubMed]
- Holdt, S.L.; Kraan, S. Bioactive compounds in seaweed: Functional food applications and legislation. J. Appl. Phycol. 2011, 23, 543–597. [Google Scholar] [CrossRef]
- Michel, C.; Macfarlane, G. Digestive fates of soluble polysaccharides from marine macroalgae: Involvement of the colonic microflora and physiological consequences for the host. J. Appl. Bacteriol. 1996, 80, 349–369. [Google Scholar] [CrossRef]
- Wang, Y.; Li, L.; Ye, C.; Yuan, J.; Qin, S. Alginate oligosaccharide improves lipid metabolism and inflammation by modulating gut microbiota in high-fat diet fed mice. Appl. Microbiol. Biotechnol. 2020, 104, 3541–3554. [Google Scholar] [CrossRef]
- Zhang, P.; Liu, J.; Xiong, B.; Zhang, C.; Kang, B.; Gao, Y.; Li, Z.; Ge, W.; Cheng, S.; Hao, Y.; et al. Microbiota from alginate oligosaccharide-dosed mice successfully mitigated small intestinal mucositis. Microbiome 2020, 8, 112. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Xing, M.; Cao, Q.; Wang, Y.; Xiao, H.; Zhao, J.; Zhang, Q.; Ji, A.; Song, S. Advances in Research on the Bioactivity of Alginate Oligosaccharides. Mar. Drugs 2020, 18, 144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shang, Q.; Jiang, H.; Cai, C.; Hao, J.; Li, G.; Yu, G. Gut microbiota fermentation of marine polysaccharides and its effects on intestinal ecology: An overview. Carbohydr. Polym. 2018, 179, 173–185. [Google Scholar] [CrossRef]
- Zargarzadeh, M.; Amaral, A.J.; Custódio, C.A.; Mano, J.F. Biomedical applications of laminarin. Carbohydr. Polym. 2020, 232, 115774. [Google Scholar] [CrossRef]
- Nguyen, S.G.; Kim, J.; Guevarra, R.B.; Lee, J.-H.; Kim, E.; Kim, S.-I.; Unno, T. Laminarin favorably modulates gut microbiota in mice fed a high-fat diet. Food Funct. 2016, 7, 4193–4201. [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] [PubMed] [Green Version]
- 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] [PubMed]
- Jiang, Z.; Hama, Y.; Yamaguchi, K.; Oda, T. Inhibitory effect of sulphated polysaccharide porphyran on nitric oxide production in lipopolysaccharide-stimulated RAW264.7 macrophages. J. Biochem. 2011, 151, 65–74. [Google Scholar] [CrossRef] [Green Version]
- Mondol, M.A.M.; Shin, H.J.; Islam, M.T. Diversity of Secondary Metabolites from Marine Bacillus Species: Chemistry and Biological Activity. Mar. Drugs 2013, 11, 2846–2872. [Google Scholar] [CrossRef] [Green Version]
- Gustafson, K.; Roman, M.; Fenical, W. The macrolactins, a novel class of antiviral and cytotoxic macrolides from a deep-sea marine bacterium. J. Am. Chem. Soc. 1989, 111, 7519–7524. [Google Scholar] [CrossRef]
- Kim, E.-N.; Gao, M.; Choi, H.; Jeong, G.-S. Marine Microorganism-Derived Macrolactins Inhibit Inflammatory Mediator Effects in LPS-Induced Macrophage and Microglial Cells by Regulating BACH1 and HO-1/Nrf2 Signals through Inhibition of TLR4 Activation. Molecules 2020, 25, 656. [Google Scholar] [CrossRef] [Green Version]
- Yan, X.; Zhou, Y.-X.; Tang, X.-X.; Liu, X.-X.; Yi, Z.-W.; Fang, M.-J.; Wu, Z.; Jiang, F.-Q.; Qiu, Y.-K. Macrolactins from Marine-Derived Bacillus subtilis B5 Bacteria as Inhibitors of Inducible Nitric Oxide and Cytokines Expression. Mar. Drugs 2016, 14, 195. [Google Scholar] [CrossRef] [Green Version]
- Heo, S.-J.; Kim, J.-P.; Jung, W.-K.; Lee, N.-H.; Kang, H.-S.; Jun, E.-M.; Park, S.-H.; Kang, S.-M.; Lee, Y.-J.; Park, P.-J.; et al. Identification of chemical structure and free radical scavenging activity of diphlorethohydroxycarmalol isolated from a brown alga, Ishige okamurae. J. Microbiol. Biotechnol. 2008, 18, 676–681. [Google Scholar]
- Gessler, N.N.; Egorova, A.S.; Belozerskaia, T.A. Fungal anthraquinones (review). Prikl. Biokhim. Mikrobiol. 2013, 49, 109–123. [Google Scholar]
- Kosalec, I.; Kremer, D.; Locatelli, M.; Epifano, F.; Genovese, S.; Carlucci, G.; Randić, M.; Končić, M.Z. Anthraquinone profile, antioxidant and antimicrobial activity of bark extracts of Rhamnus alaternus, R. fallax, R. intermedia and R. pumila. Food Chem. 2013, 136, 335–341. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.-Y.; Tao, L.-Y.; Liang, Y.-J.; Chen, L.-M.; Mi, Y.-J.; Zheng, L.-S.; Wang, F.; She, Z.-G.; Lin, Y.-C.; To, K.K.W.; et al. Anthracenedione Derivatives as Anticancer Agents Isolated from Secondary Metabolites of the Mangrove Endophytic Fungi. Mar. Drugs 2010, 8, 1469–1481. [Google Scholar] [CrossRef]
- Tabolacci, C.; Cordella, M.; Turcano, L.; Rossi, S.; Lentini, A.; Mariotti, S.; Nisini, R.; Sette, G.; Eramo, A.; Piredda, L.; et al. Aloe-emodin exerts a potent anticancer and immunomodulatory activity on BRAF-mutated human melanoma cells. Eur. J. Pharmacol. 2015, 762, 283–292. [Google Scholar] [CrossRef] [PubMed]
- Huei-Chen, H.; Shu-Hsun, C.; Chao, P.-D.L. Vasorelaxants from Chinese herbs, emodin and scoparone, possess immunosuppressive properties. Eur. J. Pharmacol. 1991, 198, 211–213. [Google Scholar] [CrossRef]
- Zhao, X.-Y.; Qiao, G.-F.; Li, B.-X.; Chai, L.-M.; Li, Z.; Lu, Y.-J.; Yang, B.-F. Hypoglycaemic and hypolipidaemic effects of emodin and its effect on l-type calcium channels in dyslipidaemic-diabetic rats. Clin. Exp. Pharmacol. Physiol. 2009, 36, 29–34. [Google Scholar] [CrossRef] [PubMed]
- Matsuda, H.; Shimoda, H.; Morikawa, T.; Yoshikawa, M. Phytoestrogens from the roots of Polygonum cuspidatum (polygonaceae): Structure-Requirement of hydroxyanthraquinones for estrogenic activity. Bioorganic Med. Chem. Lett. 2001, 11, 1839–1842. [Google Scholar] [CrossRef]
- Fouillaud, M.; Venkatachalam, M.; Girard-Valenciennes, E.; Caro, Y.; Dufossé, L. Anthraquinones and Derivatives from Marine-Derived Fungi: Structural Diversity and Selected Biological Activities. Mar. Drugs 2016, 14, 64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.; Chu, S.; Liu, Y.; Chen, N. Neuroprotective Effects of Anthraquinones from Rhubarb in Central Nervous System Diseases. Evid. Based Complement. Altern. Med. 2019, 2019, 3790728. [Google Scholar] [CrossRef] [Green Version]
- Wei, Z.; Wu, J.; Yang, Y.; Shen, P.; Cheng, P.; Tao, L.; Shan, Y.; Sun, Z.; Lu, Y. Anthraquinone laxative-altered gut microbiota induces colonic mucosal barrier dysfunction for colorectal cancer progression. Res. Sq. 2020, 1–35. [Google Scholar] [CrossRef]
- González, Y.; Doens, D.; Santamaría, R.; Ramos, M.; Restrepo, C.M.; De Arruda, L.B.; Lleonart, R.; Gutiérrez, M.; Fernández, P.L. A Pseudopterane Diterpene Isolated from the Octocoral Pseudopterogorgia acerosa Inhibits the Inflammatory Response Mediated by TLR-Ligands and TNF-Alpha in Macrophages. PLoS ONE 2013, 8, e84107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de las Heras, B.; Hortelano, S. Molecular basis of the anti-inflammatory effects of terpenoids. Inflamm. Allergy Drug Targets 2009, 8, 28–39. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.-Y.; Lin, S.-C.; Feng, C.-W.; Chen, P.-C.; Su, Y.-D.; Li, C.-M.; Yang, S.-N.; Jean, Y.-H.; Sung, P.-J.; Duh, C.-Y.; et al. Anti-Inflammatory and Analgesic Effects of the Marine-Derived Compound Excavatolide B Isolated from the Culture-Type Formosan Gorgonian Briareum excavatum. Mar. Drugs 2015, 13, 2559–2579. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tak, P.P.; Firestein, G.S. NF-kappaB: A key role in inflammatory diseases. J. Clin. Investig. 2001, 107, 7–11. [Google Scholar] [CrossRef]
- Thao, N.P.; Luyen, B.T.T.; Ngan, N.T.T.; Song, S.B.; Cuong, N.X.; Nam, N.H.; Van Kiem, P.; Kim, Y.H.; Van Minh, C. New anti-inflammatory cembranoid diterpenoids from the Vietnamese soft coral Lobophytum crassum. Bioorg. Med. Chem. Lett. 2014, 24, 228–232. [Google Scholar] [CrossRef]
- Shimizu, H.; Koyama, T.; Yamada, S.; Lipton, S.A.; Satoh, T. Zonarol, a sesquiterpene from the brown algae Dictyopteris undulata, provides neuroprotection by activating the Nrf2/ARE pathway. Biochem. Biophys. Res. Commun. 2015, 457, 718–722. [Google Scholar] [CrossRef] [Green Version]
- Fiorucci, S.; Distrutti, E.; Bifulco, G.; D’Auria, M.V.; Zampella, A. Marine sponge steroids as nuclear receptor ligands. Trends Pharmacol. Sci. 2012, 33, 591–601. [Google Scholar] [CrossRef]
- Sepe, V.; Ummarino, R.; D’Auria, M.V.; Mencarelli, A.; D’Amore, C.; Renga, B.; Zampella, A.; Fiorucci, S. Total Synthesis and Pharmacological Characterization of Solomonsterol A, a Potent Marine Pregnane-X-Receptor Agonist Endowed with Anti-Inflammatory Activity. J. Med. Chem. 2011, 54, 4590–4599. [Google Scholar] [CrossRef]
- Hannan, A.; Dash, R.; Sohag, A.A.M.; 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] [PubMed] [Green Version]
- Yoo, M.S.; Shin, J.S.; Choi, H.E.; Cho, Y.W.; Bang, M.H.; Baek, N.I.; Lee, K.T. Fucosterol isolated from Undaria pinnatifida inhibits lipopolysaccharide-induced production of nitric oxide and pro-inflammatory cytokines via the inactivation of nuclear factor-κB and p38 mitogen-activated protein kinase in RAW264.7 macrophages. Food Chem. 2012, 135, 967–975. [Google Scholar] [CrossRef]
- Hannan, M.A.; Sohag, A.A.; Dash, R.; Haque, M.N.; Mohibbullah, M.; Oktaviani, D.F.; Hossain, M.T.; Choi, H.J.; Moon, I.S. Phytosterols of marine algae: Insights into the potential health benefits and molecular pharmacology. Phytomedicine 2020, 69, 153201. [Google Scholar] [CrossRef]
- Castro-Silva, E.S.; Bello, M.; Hernández-Rodríguez, M.; Correa-Basurto, J.; Murillo-Álvarez, J.I.; Rosales-Hernández, M.C.; Muñoz-Ochoa, M. In vitro and In Silico evaluation of fucosterol from Sargassum horridum as potential human acetylcholinesterase inhibitor. J. Biomol. Struct. Dyn. 2018, 37, 3259–3268. [Google Scholar] [CrossRef]
- Lee, S.; Lee, Y.S.; Jung, S.H.; Kang, S.S.; Shin, K.H. Anti-oxidant activities of fucosterol from the marine algae Pelvetia siliquosa. Arch. Pharmacal Res. 2003, 26, 719–722. [Google Scholar] [CrossRef]
- Jung, H.A.; Jin, S.E.; Ahn, B.R.; Lee, C.M.; Choi, J.S. Anti-inflammatory activity of edible brown alga Eisenia bicyclis and its constituents fucosterol and phlorotannins in LPS-stimulated RAW264.7 macrophages. Food Chem. Toxicol. 2013, 59, 199–206. [Google Scholar] [CrossRef]
- Choi, J.S.; Han, Y.R.; Byeon, J.S.; Choung, S.-Y.; Sohn, H.S.; Jung, H.A. Protective effect of fucosterol isolated from the edible brown algae, Ecklonia stolonifera and Eisenia bicyclis, on tert-butyl hydroperoxide- and tacrine-induced HepG2 cell injury. J. Pharm. Pharmacol. 2015, 67, 1170–1178. [Google Scholar] [CrossRef] [PubMed]
- Fernando, I.S.; Jayawardena, T.U.; Kim, H.-S.; Lee, W.W.; Vaas, A.; De Silva, H.; Abayaweera, G.; Nanayakkara, C.; Abeytunga, D.; Lee, D.-S.; et al. Beijing urban particulate matter-induced injury and inflammation in human lung epithelial cells and the protective effects of fucosterol from Sargassum binderi (Sonder ex J. Agardh). Environ. Res. 2019, 172, 150–158. [Google Scholar] [CrossRef]
- Brandhorst, S.; Choi, I.Y.; Wei, M.; Cheng, C.W.; Sedrakyan, S.; Navarrete, G.; Dubeau, L.; Yap, L.P.; Park, R.; Vinciguerra, M.; et al. A Periodic Diet that Mimics Fasting Promotes Multi-System Regeneration, Enhanced Cognitive Performance, and Healthspan. Cell Metab. 2015, 22, 86–99. [Google Scholar] [CrossRef] [Green Version]
- Kim, A.-R.; Lee, M.-S.; Choi, J.-W.; Utsuki, T.; Kim, J.-I.; Jang, B.-C.; Kim, H.-R. Phlorofucofuroeckol a Suppresses Expression of Inducible Nitric Oxide Synthase, Cyclooxygenase-2, and Pro-inflammatory Cytokines via Inhibition of Nuclear Factor-κB, c-Jun NH2-Terminal Kinases, and Akt in Microglial Cells. Inflammation 2012, 36, 259–271. [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]
- Kim, K.-S.; Cui, X.; Lee, D.-S.; Sohn, J.H.; Yim, J.H.; Kim, Y.-C.; Oh, H. Anti-Inflammatory Effect of Neoechinulin A from the Marine Fungus Eurotium sp. SF-5989 through the Suppression of NF-κB and p38 MAPK Pathways in Lipopolysaccharide-Stimulated RAW264.7 Macrophages. Molecules 2013, 18, 13245–13259. [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] [PubMed]
- Abdul, Q.A.; Choi, R.J.; Jung, H.A.; Choi, J.S. Health benefit of fucosterol from marine algae: A review. J. Sci. Food Agric. 2016, 96, 1856–1866. [Google Scholar] [CrossRef]
- Gan, S.Y.; Wong, L.Z.; Wong, J.W.; Tan, E.L. Fucosterol exerts protection against amyloid β-induced neurotoxicity, reduces intracellular levels of amyloid β and enhances the mRNA expression of neuroglobin in amyloid β-induced SH-SY5Y cells. Int. J. Biol. Macromol. 2019, 121, 207–213. [Google Scholar] [CrossRef]
- Mencarelli, A.; D’Amore, C.; Renga, B.; Cipriani, S.; Carino, A.; Sepe, V.; Perissutti, E.; D’Auria, M.V.; Zampella, A.; Distrutti, E.; et al. Solomonsterol A, a Marine Pregnane-X-Receptor Agonist, Attenuates Inflammation and Immune Dysfunction in a Mouse Model of Arthritis. Mar. Drugs 2013, 12, 36–53. [Google Scholar] [CrossRef]
- Shi, C.; Pan, T.; Cao, M.; Liu, Q.; Zhang, L.; Liu, G. Suppression of Th2 immune responses by the sulfated polysaccharide from Porphyra haitanensis in tropomyosin-sensitized mice. Int. Immunopharmacol. 2015, 24, 211–218. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Vo, T.-S.; Kim, S.-K. Fucoidans as a natural bioactive ingredient for functional foods. J. Funct. Foods 2013, 5, 16–27. [Google Scholar] [CrossRef]
Neurological Disorder | Changes of Microbiota | Effects/Outcomes | Reference |
---|---|---|---|
AD | Bacteroides vulgatus, Bacteroides fragilis, Eggerthella lenta, Odoribacter splanchnicus, Butyrivibrio hungatei, Butyrivibrio proteoclasticus, Eubacterium eligens, Eubacterium hallii, Eubacterium rectale, Clostridium sp., Roseburia hominis, Bifidobacterium bifidum, Faecalibacterium prausnitzii | ↑TLRs, ↑NF-κB, ↑IL-1β, ↑IL-18, ↑ Aβ, ↑caspase-1, CXCL2, ↑bacterial LPS, | [51,52,53,54] |
PD | Enterobacteriaceae, Prevotellaceae, Verrucomicrobiaceae, Lactobacillus, Porphyromonas, Parabacteroides, Mucispirillum, Bacteroides fragilis | ↑TLR4, ↑IL-1β, ↑IL-2, ↑IL-4, ↑IL-6, ↑IL-13, ↑IL-18, ↑IFN-γ, ↑TNF-α | [3] |
ASD | Bifidobacteraceae, Veillonellaceae, Lactobacillaceae, Bifidobacterium, Megasphaera, Mitsuokella, Rumnicoccus, Lachnoclostridium, Clostridium, Sutterella, Desulfovibrio, Lactobacillus, Eubacterium, Prevotella | ↑mTOR, ↑TNF-α, ↑IL-4, ↑IL-5, ↑IL-6, ↑IL-8, ↑valeric acid, ↑intestinal serotonin, ↓IL-10, ↓TGF-β, ↓fecal acetic acid and butyrate, ↓cerebral 5-HT | [11,81,84,85,86,87] |
Depression | Bifidobacterium, Alistipes, Prevotella, Parabacteroides, Lachnospiraceae, Anaerostipes, Oscillibacter, Faecalibacterium, Ruminococcus, Clostridium, Megamonas, Streptococcus, Klebsiella, Phascolarctobacterium | ↓GABA, ↓dopamine, ↓5-HT, ↓BDNF, ↓IL-10 | [63,64,65] |
ALS | Ruminococcaceae, Bacteroidetes, Enterobacteria, Escherichia coli, Butyrivibrio fibrisolvens, Bacterioidetes, Oscillobacte, Firmicutes, Anaerostipes, Lachnospiraceae | Dysregulated levels of NO, GABA, LPS, AMPA/NMDA, and oxidative pathways | [74,75,76] |
MS | Acinetobacteria, Bacteroidetes, Desulfovibrionaceae, Firmicutes, Proteobacteria, Verrucomicrobia, and associated genus | ↓5-HT, ↓dopamine, dysregulated GABA, ↑IFN-γ, ↑MCP-1, ↑MIP-1α, ↑MIP-1β, ↑IL-6 | [77,80,81,82] |
ASD | Bifidobacteraceae, Veillonellaceae, Lactobacillaceae, Bifidobacterium, Megasphaera, Mitsuokella, Rumnicoccus, Lachnoclostridium, Clostridium, Sutterella, Desulfovibrio, Lactobacillus, Eubacterium, Prevotella | ↑mTOR, ↑TNF-α, ↑IL-4, ↑IL-5, ↑IL-6, ↑IL-8, ↑valeric acid, ↑intestinal serotonin, ↓IL-10, ↓TGF-β, ↓fecal acetic acid and butyrate, ↓cerebral 5-HT | [11,81,84,85,86,87] |
Marine Class | Compound | Major Source | Effect/Outcome | Reference |
---|---|---|---|---|
Carotenoid | Fucoxanthin | Sargassum siliquastrum, Hijikia fusiformis, Undaria pinnatifida, Laminaria japonica, Alaria crassifolia, Cladosiphon okamuranus | ↑BDNF, ↑SOD, ↓ROS, ↓MDA, ↓cleaved caspase-3, ↑Bcl-2/Bax ratio | [117,127] |
↓ROS, ↑Beclin-1 (Atg6), ↑LC3 (Atg8) and ↓p62, ↓cleaved caspase-3, ↑HO-1, ↑NQO-1↑Nrf2 | [139,245] | |||
Astaxanthin | Hematococcus pluvialis, Chlorella zofingiensis, Chlorococcum sp., Phaffia rhodozyma, Agrobacterium aurantiacum | ↓Bax/Bcl-2 ratio, ↓caspase-3, ↓Ca2+ influx, ↓ROS, ↓MDA, ↓LPO, ↓IL-1β, ↓TNF-α, ↓OS, ↓ NF-κB, ↓IL-1β, ↓ICAMs1 | [149] | |
Lycopene | Haloarchaea belonging to the Haloferacaceae family | ↑GSH/GSSG, ↑BDNF, ↓TNF-α, ↓NF-κB, ↓ILs, ↓TLR4 | [167,174] | |
Phytosterol | Fucosterol | Anthophycus longifolius, Chondria dasyphylla, Ecklonia stolonifera, Undaria pinnatifida, Hizikia fusiformis | ↑TrkB-mediated ERK1/2, ↓GRP78 ↑BDNF, ↑Ngb mRNA ↓APP, ↓Aβ levels | [15,246,247] |
Solomonsterol A | Theonella swinhoei | ↓Arthritic score in anti-type II collagen, antibody-induced arthritis mice model | [248] | |
Polysaccharide | Sulfated polysaccharide | Porphyra haitanensis, Ecklonia cava, Laminaria japonica,Cladosiphon okamuranus | ↓IgE level in tropomyosin-induced mouse allergy model | [249] |
Fucoidan | ↑p-PKC, ↓OS ↓caspases-9/3, ↓ROS, ↓LC3-II, ↑SOD, ↑GPx, ↓MDA,↑Bcl-2/Bax ratio, ↓cytochrome C, ↑livin and XIAP; ↑GSH, ↓Bax | [250,251] | ||
Chitosan | Species of crustaceous and cephalopods | Modulating mitochondrial-dependent pathway | [189,190,193] | |
Laminarin | Brown seaweeds such as Laminariaceae, and Laminaria, Saccharina, or Eisenia | ↓Pro-inflammatory microglia | [204,205] | |
Alginate | Microalgae | ↓TLR4, ↓NF-κB, ↓ROS | [198,199,202] | |
Diterpene | Excavatolide B | Briareum excavatum | ↓iNOS, ↓COX-2 | [227] |
Crassumol E | Soft coral Lobophytum crassum | ↓NF-κB, ↓TNF-α | [227] | |
Lobocrasol | Soft coral Lobophytum crassum | ↓NF-κB | [228] | |
Hydroquinone sesquiterpene | Zonarol | Dictyopteris undulata | ↑NQO-1, ↑HO-1, ↑PRDX4 | [139,230] |
Macrolactin | Macrolactin A | Bacillus subtilis, Marine sediment, and soil isolates | ↑Nrf2, ↑HO-1, ↓NF-κB, ↓TLR4, ↓IL-6, ↓iNOS | [212,213] |
Alkaloid | Neoechinulin B | Eurotium sp. SF-5989 | ↓NF-κB, ↓p38 MAPK | [244] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fakhri, S.; Yarmohammadi, A.; Yarmohammadi, M.; Farzaei, M.H.; Echeverria, J. Marine Natural Products: Promising Candidates in the Modulation of Gut-Brain Axis towards Neuroprotection. Mar. Drugs 2021, 19, 165. https://doi.org/10.3390/md19030165
Fakhri S, Yarmohammadi A, Yarmohammadi M, Farzaei MH, Echeverria J. Marine Natural Products: Promising Candidates in the Modulation of Gut-Brain Axis towards Neuroprotection. Marine Drugs. 2021; 19(3):165. https://doi.org/10.3390/md19030165
Chicago/Turabian StyleFakhri, Sajad, Akram Yarmohammadi, Mostafa Yarmohammadi, Mohammad Hosein Farzaei, and Javier Echeverria. 2021. "Marine Natural Products: Promising Candidates in the Modulation of Gut-Brain Axis towards Neuroprotection" Marine Drugs 19, no. 3: 165. https://doi.org/10.3390/md19030165
APA StyleFakhri, S., Yarmohammadi, A., Yarmohammadi, M., Farzaei, M. H., & Echeverria, J. (2021). Marine Natural Products: Promising Candidates in the Modulation of Gut-Brain Axis towards Neuroprotection. Marine Drugs, 19(3), 165. https://doi.org/10.3390/md19030165