Dietary Astaxanthin: A Promising Antioxidant and Anti-Inflammatory Agent for Brain Aging and Adult Neurogenesis
Abstract
:1. Introduction
2. Astaxanthin
2.1. Sources and Structures of Astaxanthin
2.2. Safety of Commercial Astaxanthin
2.3. Biological Properties of Astaxanthin
3. Adult Neurogenesis and Aging
3.1. Mechanisms of Adult Neurogenesis
3.2. Aging and Adult Neurogenesis
4. Astaxanthin and Adult Neurogenesis
4.1. Beneficial Effects of Astaxanthin on Molecular Pathways of Adult Neurogenesis
4.2. Positive Effects of Astaxanthin on Molecular Pathways of Neuroinflammation and Oxidative Stress
4.2.1. Oxidative Stress and Nrf2 Pathway
4.2.2. Neuroinflammation and NF-κB Pathways
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Mattson, M.P.; Arumugam, T.V. Hallmarks of Brain Aging: Adaptive and Pathological Modification by Metabolic States. Cell Metab. 2018, 27, 1176–1199. [Google Scholar] [CrossRef] [PubMed]
- Culig, L.; Chu, X.; Bohr, V.A. Neurogenesis in aging and age-related neurodegenerative diseases. Ageing Res. Rev. 2022, 78, 101636. [Google Scholar] [CrossRef] [PubMed]
- Leal-galicia, P.; Chávez-hernández, M.E.; Mata, F.; Mata-luévanos, J.; Rodríguez-serrano, L.M.; Tapia-de-jesús, A.; Buenrostro-jáuregui, M.H. Adult Neurogenesis: A Story Ranging from Controversial New Neurogenic Areas and Human Adult Neurogenesis to Molecular Regulation. Int. J. Mol. Sci. 2021, 22, 11489. [Google Scholar] [CrossRef] [PubMed]
- Niklison-Chirou, M.V.; Agostini, M.; Amelio, I.; Melino, G. Regulation of Adult Neurogenesis in Mammalian Brain. Int. J. Mol. Sci. 2020, 21, 4869. [Google Scholar] [CrossRef] [PubMed]
- Davinelli, S.; Medoro, A.; Ali, S.; Passarella, D.; Intrieri, M.; Scapagnini, G. Dietary Flavonoids and Adult Neurogenesis: Potential Implications for Brain Aging. Curr. Neuropharmacol. 2022, 21, 651–668. [Google Scholar] [CrossRef]
- Davinelli, S.; Sapere, N.; Zella, D.; Bracale, R.; Intrieri, M.; Scapagnini, G. Pleiotropic protective effects of phytochemicals in Alzheimer’s disease. Oxidative Med. Cell. Longev. 2012, 2012, 386527. [Google Scholar] [CrossRef]
- Zhang, S.; Lam, K.K.H.; Wan, J.H.; Yip, C.W.; Liu, H.K.H.; Lau, Q.M.N.; Man, A.H.Y.; Cheung, C.H.; Wong, L.H.; Chen, H.B.; et al. Dietary phytochemical approaches to stem cell regulation. J. Funct. Foods 2020, 66, 103822. [Google Scholar] [CrossRef]
- Manochkumar, J.; Doss, C.G.P.; El-Seedi, H.R.; Efferth, T.; Ramamoorthy, S. The neuroprotective potential of carotenoids in vitro and in vivo. Phytomedicine 2021, 91, 153676. [Google Scholar] [CrossRef]
- Grimmig, B.; Kim, S.H.; Nash, K.; Bickford, P.C.; Douglas Shytle, R. Neuroprotective mechanisms of astaxanthin: A potential therapeutic role in preserving cognitive function in age and neurodegeneration. GeroScience 2017, 39, 19–32. [Google Scholar] [CrossRef]
- Willcox, D.C.; Scapagnini, G.; Willcox, B.J. Healthy aging diets other than the Mediterranean: A focus on the Okinawan diet. Mech. Ageing Dev. 2014, 136–137, 148–162. [Google Scholar] [CrossRef]
- Landon, R.; Gueguen, V.; Petite, H.; Letourneur, D.; Pavon-Djavid, G.; Anagnostou, F. Impact of Astaxanthin on Diabetes Pathogenesis and Chronic Complications. Mar. Drugs 2020, 18, 357. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.-T.; Kotani, K. Astaxanthin as a Potential Protector of Liver Function: A Review. J. Clin. Med. Res. 2016, 8, 701–704. [Google Scholar] [CrossRef] [PubMed]
- Brotosudarmo, T.H.P.; Limantara, L.; Setiyono, E.; Heriyanto. Structures of Astaxanthin and Their Consequences for Therapeutic Application. Int. J. Food Sci. 2020, 2020, 2156582. [Google Scholar] [CrossRef]
- Li, B.; Lee, J.Y.; Luo, Y. Health benefits of astaxanthin and its encapsulation for improving bioavailability: A review. J. Agric. Food Res. 2023, 14, 100685. [Google Scholar] [CrossRef]
- Higuera-Ciapara, I.; Félix-Valenzuela, L.; Goycoolea, F.M. Astaxanthin: A review of its chemistry and applications. Crit. Rev. Food Sci. Nutr. 2006, 46, 185–196. [Google Scholar] [CrossRef] [PubMed]
- Ambati, R.R.; Moi, P.S.; Ravi, S.; Aswathanarayana, R.G. Astaxanthin: Sources, Extraction, Stability, Biological Activities and Its Commercial Applications—A Review. Mar. Drugs 2014, 12, 128. [Google Scholar] [CrossRef] [PubMed]
- Agostoni, C.; Berni Canani, R.; Fairweather-Tait, S.; Heinonen, M.; Korhonen, H.; La Vieille, S.; Marchelli, R.; Martin, A.; Naska, A.; Neuhäuser-Berthold, M.; et al. Scientific Opinion on the safety of astaxanthin-rich ingredients (AstaREAL A1010 and AstaREAL L10) as novel food ingredients. EFSA J. 2014, 12, 3757. [Google Scholar] [CrossRef]
- Aquilina, G.; Bampidis, V.; De, M.; Bastos, L.; Guido Costa, L.; Flachowsky, G.; Gralak, A.; Hogstrand, C.; Leng, L.; López-Puente, S.; et al. Scientific Opinion on the safety and efficacy of synthetic astaxanthin as feed additive for salmon and trout, other fish, ornamental fish, crustaceans and ornamental birds. EFSA J. 2014, 12, 3724. [Google Scholar] [CrossRef]
- Spiller, G.A.; Dewell, A. Safety of an astaxanthin-rich Haematococcus pluvialis algal extract: A randomized clinical trial. J. Med. Food 2003, 6, 51–56. [Google Scholar] [CrossRef]
- Res, P.T.; Cermak, N.M.; Stinkens, R.; Tollakson, T.J.; Haenen, G.R.; Bast, A.; Van Loon, L.J.C. Astaxanthin supplementation does not augment fat use or improve endurance performance. Med. Sci. Sports Exerc. 2013, 45, 1158–1165. [Google Scholar] [CrossRef]
- Odeberg, J.M.; Lignell, Å.; Pettersson, A.; Höglund, P. Oral bioavailability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations. Eur. J. Pharm. Sci. 2003, 19, 299–304. [Google Scholar] [CrossRef] [PubMed]
- Kupcinskas, L.; Lafolie, P.; Lignell, Å.; Kiudelis, G.; Jonaitis, L.; Adamonis, K.; Andersen, L.P.; Wadström, T. Efficacy of the natural antioxidant astaxanthin in the treatment of functional dyspepsia in patients with or without Helicobacter pylori infection: A prospective, randomized, double blind, and placebo-controlled study. Phytomedicine 2008, 15, 391–399. [Google Scholar] [CrossRef] [PubMed]
- Brendler, T.; Williamson, E.M. Astaxanthin: How much is too much? A safety review. Phytother. Res. 2019, 33, 3090–3111. [Google Scholar] [CrossRef] [PubMed]
- Rizzardi, N.; Pezzolesi, L.; Samorì, C.; Senese, F.; Zalambani, C.; Pitacco, W.; Calonghi, N.; Bergamini, C.; Prata, C.; Fato, R. Natural Astaxanthin Is a Green Antioxidant Able to Counteract Lipid Peroxidation and Ferroptotic Cell Death. Int. J. Mol. Sci. 2022, 23, 15137. [Google Scholar] [CrossRef] [PubMed]
- Petyaev, I.M.; Klochkov, V.A.; Chalyk, N.E.; Pristensky, D.V.; Chernyshova, M.P.; Kyle, N.H.; Bashmakov, Y.K. Markers of Hypoxia and Oxidative Stress in Aging Volunteers Ingesting Lycosomal Formulation of Dark Chocolate Containing Astaxanthin. J. Nutr. Health Aging 2018, 22, 1092–1098. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.Q.; Sun, X.B.; Xu, Y.X.; Zhao, H.; Zhu, Q.Y.; Zhu, C.Q. Astaxanthin upregulates heme oxygenase-1 expression through ERK1/2 pathway and its protective effect against beta-amyloid-induced cytotoxicity in SH-SY5Y cells. Brain Res. 2010, 1360, 159–167. [Google Scholar] [CrossRef]
- Li, Z.; Dong, X.; Liu, H.; Chen, X.; Shi, H.; Fan, Y.; Hou, D.; Zhang, X. Astaxanthin protects ARPE-19 cells from oxidative stress via upregulation of Nrf2-regulated phase II enzymes through activation of PI3K/Akt. Mol. Vis. 2013, 19, 1656. [Google Scholar]
- Ma, H.; Chen, S.; Xiong, H.; Wang, M.; Hang, W.; Zhu, X.; Zheng, Y.; Ge, B.; Li, R.; Cui, H. Astaxanthin from Haematococcus pluvialis ameliorates the chemotherapeutic drug (doxorubicin) induced liver injury through the Keap1/Nrf2/HO-1 pathway in mice. Food Funct. 2020, 11, 4659–4671. [Google Scholar] [CrossRef]
- Li, L.; Chen, Y.; Jiao, D.; Yang, S.; Li, L.; Li, P. Protective Effect of Astaxanthin on Ochratoxin A-Induced Kidney Injury to Mice by Regulating Oxidative Stress-Related NRF2/KEAP1 Pathway. Molecules 2020, 25, 1386. [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]
- Xie, X.; Chen, Q.; Tao, J. Astaxanthin Promotes Nrf2/ARE Signaling to Inhibit HG-Induced Renal Fibrosis in GMCs. Mar. Drugs 2018, 16, 117. [Google Scholar] [CrossRef] [PubMed]
- Davinelli, S.; Medoro, A.; Intrieri, M.; Saso, L.; Scapagnini, G.; Kang, J.X. Targeting NRF2–KEAP1 axis by Omega-3 fatty acids and their derivatives: Emerging opportunities against aging and diseases. Free Radic. Biol. Med. 2022, 193, 736–750. [Google Scholar] [CrossRef] [PubMed]
- Medoro, A.; Scapagnini, G.; Davinelli, S. Regulation of NRF2 signaling pathway and the hallmarks of aging: An overview. Modul. Oxidative Stress 2023, 3, 29–41. [Google Scholar] [CrossRef]
- Medoro, A.; Saso, L.; Scapagnini, G.; Davinelli, S. NRF2 signaling pathway and telomere length in aging and age-related diseases. Mol. Cell. Biochem. 2023, 1, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Wardyn, J.D.; Ponsford, A.H.; Sanderson, C.M. Dissecting molecular cross-talk between Nrf2 and NF-κB response pathways. Biochem. Soc. Trans. 2015, 43, 621–626. [Google Scholar] [CrossRef] [PubMed]
- Deng, X.; Wang, M.; Hu, S.; Feng, Y.; Shao, Y.; Xie, Y.; Wu, M.; Chen, Y.; Shi, X. The Neuroprotective Effect of Astaxanthin on Pilocarpine-Induced Status Epilepticus in Rats. Front. Cell. Neurosci. 2019, 13, 123. [Google Scholar] [CrossRef]
- Kim, Y.H.; Koh, H.K.; Kim, D.S. Down-regulation of IL-6 production by astaxanthin via ERK-, MSK-, and NF-κB-mediated signals in activated microglia. Int. Immunopharmacol. 2010, 10, 1560–1572. [Google Scholar] [CrossRef]
- 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]
- Sorrenti, V.; Davinelli, S.; Scapagnini, G.; Willcox, B.J.; Allsopp, R.C.; Willcox, D.C. Astaxanthin as a Putative Geroprotector: Molecular Basis and Focus on Brain Aging. Mar. Drugs 2020, 18, 351. [Google Scholar] [CrossRef]
- Lim, D.A.; Alvarez-Buylla, A. The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis. Cold Spring Harb. Perspect. Biol. 2016, 8, a018820. [Google Scholar] [CrossRef]
- Lazarini, F.; Gabellec, M.M.; Moigneu, C.; De Chaumont, F.; Olivo-Marin, J.C.; Lledo, P.M. Adult neurogenesis restores dopaminergic neuronal loss in the olfactory bulb. J. Neurosci. 2014, 34, 14430–14442. [Google Scholar] [CrossRef] [PubMed]
- Gao, A.; Xia, F.; Guskjolen, A.J.; Ramsaran, A.I.; Santoro, A.; Josselyn, S.A.; Frankland, P.W. Elevation of Hippocampal Neurogenesis Induces a Temporally Graded Pattern of Forgetting of Contextual Fear Memories. J. Neurosci. 2018, 38, 3190–3198. [Google Scholar] [CrossRef] [PubMed]
- Bonaguidi, M.A.; Song, J.; Ming, G.L.; Song, H. A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Curr. Opin. Neurobiol. 2012, 22, 754–761. [Google Scholar] [CrossRef] [PubMed]
- Kozareva, D.A.; Cryan, J.F.; Nolan, Y.M. Born this way: Hippocampal neurogenesis across the lifespan. Aging Cell 2019, 18, e13007. [Google Scholar] [CrossRef]
- Favaro, R.; Valotta, M.; Ferri, A.L.M.; Latorre, E.; Mariani, J.; Giachino, C.; Lancini, C.; Tosetti, V.; Ottolenghi, S.; Taylor, V.; et al. Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat. Neurosci. 2009, 12, 1248–1256. [Google Scholar] [CrossRef]
- Kuwabara, T.; Hsieh, J.; Muotri, A.; Yeo, G.; Warashina, M.; Lie, D.C.; Moore, L.; Nakashima, K.; Asashima, M.; Gage, F.H. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat. Neurosci. 2009, 12, 1097–1105. [Google Scholar] [CrossRef]
- Ortiz-López, L.; Vega-Rivera, N.M.; Babu, H.; Ramírez-Rodríguez, G.B. Brain-Derived Neurotrophic Factor Induces Cell Survival and the Migration of Murine Adult Hippocampal Precursor Cells During Differentiation In Vitro. Neurotox. Res. 2017, 31, 122–135. [Google Scholar] [CrossRef]
- Seri, B.; García-Verdugo, J.M.; McEwen, B.S.; Alvarez-Buylla, A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 2001, 21, 7153–7160. [Google Scholar] [CrossRef]
- Filippov, V.; Kronenberg, G.; Pivneva, T.; Reuter, K.; Steiner, B.; Wang, L.P.; Yamaguchi, M.; Kettenmann, H.; Kempermann, G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 2003, 23, 373–382. [Google Scholar] [CrossRef]
- Brown, J.P.; Couillard-Després, S.; Cooper-Kuhn, C.M.; Winkler, J.; Aigner, L.; Kuhn, H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467, 1–10. [Google Scholar] [CrossRef]
- Kronenberg, G.; Reuter, K.; Steiner, B.; Brandt, M.D.; Jessberger, S.; Yamaguchi, M.; Kempermann, G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 2003, 467, 455–463. [Google Scholar] [CrossRef] [PubMed]
- Brandt, M.D.; Jessberger, S.; Steiner, B.; Kronenberg, G.; Reuter, K.; Bick-Sander, A.; Von Der Behrens, W.; Kempermann, G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol. Cell. Neurosci. 2003, 24, 603–613. [Google Scholar] [CrossRef] [PubMed]
- Kempermann, G.; Gast, D.; Kronenberg, G.; Yamaguchi, M.; Gage, F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003, 130, 391–399. [Google Scholar] [CrossRef] [PubMed]
- Biebl, M.; Cooper, C.M.; Winkler, J.; Kuhn, H.G. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett. 2000, 291, 17–20. [Google Scholar] [CrossRef] [PubMed]
- Tashiro, A.; Sandler, V.M.; Toni, N.; Zhao, C.; Gage, F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 2006, 442, 929–933. [Google Scholar] [CrossRef] [PubMed]
- Imielski, Y.; Schwamborn, J.C.; Lüningschrör, P.; Heimann, P.; Holzberg, M.; Werner, H.; Leske, O.; Püschel, A.W.; Memet, S.; Heumann, R.; et al. Regrowing the adult brain: NF-κB controls functional circuit formation and tissue homeostasis in the dentate gyrus. PLoS ONE 2012, 7, e30838. [Google Scholar] [CrossRef]
- Cancino, G.I.; Yiu, A.P.; Fatt, M.P.; Dugani, C.B.; Flores, E.R.; Frankland, P.W.; Josselyn, S.A.; Miller, F.D.; Kaplan, D.R. p63 Regulates adult neural precursor and newly born neuron survival to control hippocampal-dependent Behavior. J. Neurosci. 2013, 33, 12569–12585. [Google Scholar] [CrossRef]
- Jurkowski, M.P.; Bettio, L.; Woo, E.K.; Patten, A.; Yau, S.Y.; Gil-Mohapel, J. Beyond the Hippocampus and the SVZ: Adult Neurogenesis Throughout the Brain. Front. Cell. Neurosci. 2020, 14, 576444. [Google Scholar] [CrossRef]
- Pellegrino, G.; Trubert, C.; Terrien, J.; Pifferi, F.; Leroy, D.; Loyens, A.; Migaud, M.; Baroncini, M.; Maurage, C.A.; Fontaine, C.; et al. A comparative study of the neural stem cell niche in the adult hypothalamus of human, mouse, rat and gray mouse lemur (Microcebus murinus). J. Comp. Neurol. 2018, 526, 1419–1443. [Google Scholar] [CrossRef]
- Kokoeva, M.V.; Yin, H.; Flier, J.S. Neurogenesis in the hypothalamus of adult mice: Potential role in energy balance. Science 2005, 310, 679–683. [Google Scholar] [CrossRef]
- Zhao, M.; Momma, S.; Delfani, K.; Carlén, M.; Cassidy, R.M.; Johansson, C.B.; Brismar, H.; Shupliakov, O.; Frisén, J.; Janson, A.M. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. USA 2003, 100, 7925–7930. [Google Scholar] [CrossRef] [PubMed]
- Shapiro, L.A.; Ng, K.; Zhou, Q.Y.; Ribak, C.E. Subventricular zone-derived, newly generated neurons populate several olfactory and limbic forebrain regions. Epilepsy Behav. 2009, 14 (Suppl. S1), 74–80. [Google Scholar] [CrossRef]
- Bernier, P.J.; Bédard, A.; Vinet, J.; Lévesque, M.; Parent, A. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. USA 2002, 99, 11464–11469. [Google Scholar] [CrossRef] [PubMed]
- Magavi, S.S.; Leavitt, B.R.; Macklis, J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 2000, 405, 951–955. [Google Scholar] [CrossRef] [PubMed]
- Sachs, B.D.; Caron, M.G. Chronic fluoxetine increases extra-hippocampal neurogenesis in adult mice. Int. J. Neuropsychopharmacol. 2014, 18, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Andreotti, J.P.; Prazeres, P.H.D.M.; Magno, L.A.V.; Romano-Silva, M.A.; Mintz, A.; Birbrair, A. Neurogenesis in the postnatal cerebellum after injury. Int. J. Dev. Neurosci. 2018, 67, 33–36. [Google Scholar] [CrossRef] [PubMed]
- Enwere, E.; Shingo, T.; Gregg, C.; Fujikawa, H.; Ohta, S.; Weiss, S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci. 2004, 24, 8354–8365. [Google Scholar] [CrossRef]
- Hollands, C.; Tobin, M.K.; Hsu, M.; Musaraca, K.; Yu, T.S.; Mishra, R.; Kernie, S.G.; Lazarov, O. Depletion of adult neurogenesis exacerbates cognitive deficits in Alzheimer’s disease by compromising hippocampal inhibition. Mol. Neurodegener. 2017, 12, 64. [Google Scholar] [CrossRef]
- Moreno-Jiménez, E.P.; Flor-García, M.; Terreros-Roncal, J.; Rábano, A.; Cafini, F.; Pallas-Bazarra, N.; Ávila, J.; Llorens-Martín, M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat. Med. 2019, 25, 554–560. [Google Scholar] [CrossRef]
- Terreros-Roncal, J.; Moreno-Jiménez, E.P.; Flor-García, M.; Rodríguez-Moreno, C.B.; Trinchero, M.F.; Cafini, F.; Rábano, A.; Llorens-Martín, M. Impact of neurodegenerative diseases on human adult hippocampal neurogenesis. Science 2021, 374, 1106–1113. [Google Scholar] [CrossRef]
- Li, Y.; Guo, W. Neural Stem Cell Niche and Adult Neurogenesis. Neuroscientist 2021, 27, 235–245. [Google Scholar] [CrossRef] [PubMed]
- Arredondo, S.B.; Valenzuela-Bezanilla, D.; Santibanez, S.H.; Varela-Nallar, L. Wnt Signaling in the Adult Hippocampal Neurogenic Niche. Stem Cells 2022, 40, 630–640. [Google Scholar] [CrossRef] [PubMed]
- Solano Fonseca, R.; Mahesula, S.; Apple, D.M.; Raghunathan, R.; Dugan, A.; Cardona, A.; O’Connor, J.; Kokovay, E. Neurogenic Niche Microglia Undergo Positional Remodeling and Progressive Activation Contributing to Age-Associated Reductions in Neurogenesis. Stem Cells Dev. 2016, 25, 542. [Google Scholar] [CrossRef] [PubMed]
- Shetty, A.K.; Hattiangady, B.; Shetty, G.A. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: Role of astrocytes. Glia 2005, 51, 173–186. [Google Scholar] [CrossRef]
- Buckwalter, M.S.; Yamane, M.; Coleman, B.S.; Ormerod, B.K.; Chin, J.T.; Palmer, T.; Wyss-Coray, T. Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am. J. Pathol. 2006, 169, 154–164. [Google Scholar] [CrossRef] [PubMed]
- Decarolis, N.A.; Kirby, E.D.; Wyss-Coray, T.; Palmer, T.D. The Role of the Microenvironmental Niche in Declining Stem-Cell Functions Associated with Biological Aging. Cold Spring Harb. Perspect. Med. 2015, 5, a025874. [Google Scholar] [CrossRef] [PubMed]
- Kase, Y.; Kase, Y.; Shimazaki, T.; Okano, H. Current understanding of adult neurogenesis in the mammalian brain: How does adult neurogenesis decrease with age? Inflamm. Regen. 2020, 40, 10. [Google Scholar] [CrossRef]
- Paik, J.; Ding, Z.; Narurkar, R.; Ramkissoon, S.; Muller, F.; Kamoun, W.S.; Chae, S.S.; Zheng, H.; Ying, H.; Mahoney, J.; et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 2009, 5, 540. [Google Scholar] [CrossRef]
- Navarro Negredo, P.; Yeo, R.W.; Brunet, A. Aging and Rejuvenation of Neural Stem Cells and Their Niches. Cell Stem Cell 2020, 27, 202–223. [Google Scholar] [CrossRef]
- Shohayeb, B.; Diab, M.; Ahmed, M.; Ng, D.C.H. Factors that influence adult neurogenesis as potential therapy. Transl. Neurodegener. 2018, 7, 1–19. [Google Scholar] [CrossRef]
- Yuan, T.F.; Gu, S.; Shan, C.; Marchado, S.; Arias-Carrión, O. Oxidative Stress and Adult Neurogenesis. Stem Cell Rev. Rep. 2015, 11, 706–709. [Google Scholar] [CrossRef] [PubMed]
- Simon, M.; Czéh, B.; Fuchs, E. Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res. 2005, 1049, 244–248. [Google Scholar] [CrossRef] [PubMed]
- Singh, S.; Mishra, A.; Tiwari, V.; Shukla, S. Enhanced neuroinflammation and oxidative stress are associated with altered hippocampal neurogenesis in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine treated mice. Behav. Pharmacol. 2019, 30, 688–698. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Nam, S.W.; Kim, B.W.; Choi, W.; Lee, J.H.; Kim, W.J.; Choi, Y.H. Astaxanthin Improves Stem Cell Potency via an Increase in the Proliferation of Neural Progenitor Cells. Int. J. Mol. Sci. 2010, 11, 5109–5119. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.; Wang, X.; Xiang, Q.; Meng, X.; Peng, Y.; Du, N.; Liu, Z.; Sun, Q.; Wang, C.; Liu, X. Astaxanthin alleviates brain aging in rats by attenuating oxidative stress and increasing BDNF levels. Food Funct. 2013, 5, 158–166. [Google Scholar] [CrossRef] [PubMed]
- Jin, W. Regulation of BDNF-TrkB Signaling and Potential Therapeutic Strategies for Parkinson’s Disease. J. Clin. Med. 2020, 9, 257. [Google Scholar] [CrossRef] [PubMed]
- Yook, J.S.; Okamoto, M.; Rakwal, R.; Shibato, J.; Lee, M.C.; Matsui, T.; Chang, H.; Cho, J.Y.; Soya, H. Astaxanthin supplementation enhances adult hippocampal neurogenesis and spatial memory in mice. Mol. Nutr. Food Res. 2016, 60, 589–599. [Google Scholar] [CrossRef]
- Hussein, G.; Nakamura, M.; Zhao, Q.; Iguchi, T.; Goto, H.; Sankawa, U.; Watanabe, H. Antihypertensive and Neuroprotective Effects of Astaxanthin in Experimental Animals. Biol. Pharm. Bull. 2005, 28, 47–52. [Google Scholar] [CrossRef]
- Xu, L.; Zhu, J.; Yin, W.; Ding, X. Astaxanthin improves cognitive deficits from oxidative stress, nitric oxide synthase and inflammation through upregulation of PI3K/Akt in diabetes rat. Int. J. Clin. Exp. Pathol. 2015, 8, 6083. [Google Scholar]
- Zhang, X.; Pan, L.; Wei, X.; Gao, H.; Liu, J. Impact of astaxanthin-enriched algal powder of Haematococcus pluvialis on memory improvement in BALB/c mice. Environ. Geochem. Health 2007, 29, 483–489. [Google Scholar] [CrossRef]
- Grimmig, B.; Hudson, C.; Moss, L.; Peters, M.; Subbarayan, M.; Weeber, E.J.; Bickford, P.C. Astaxanthin supplementation modulates cognitive function and synaptic plasticity in young and aged mice. GeroScience 2019, 41, 77. [Google Scholar] [CrossRef] [PubMed]
- Chen, M.H.; Wang, T.J.; Chen, L.J.; Jiang, M.Y.; Wang, Y.J.; Tseng, G.F.; Chen, J.R. The effects of astaxanthin treatment on a rat model of Alzheimer’s disease. Brain Res. Bull. 2021, 172, 151–163. [Google Scholar] [CrossRef] [PubMed]
- Taksima, T.; Chonpathompikunlert, P.; Sroyraya, M.; Hutamekalin, P.; Limpawattana, M.; Klaypradit, W. Effects of Astaxanthin from Shrimp Shell on Oxidative Stress and Behavior in Animal Model of Alzheimer’s Disease. Mar. Drugs 2019, 17, 628. [Google Scholar] [CrossRef] [PubMed]
- Liu, N.; Lyu, X.; Zhang, X.; Zhang, F.; Chen, Y.; Li, G. Astaxanthin attenuates cognitive deficits in Alzheimer’s disease models by reducing oxidative stress via the SIRT1/PGC-1α signaling pathway. Cell Biosci. 2023, 13, 173. [Google Scholar] [CrossRef] [PubMed]
- Stranahan, A.M.; Mattson, M.P. Recruiting Adaptive Cellular Stress Responses for Successful Brain Aging. Nat. Rev. Neurosci. 2012, 13, 209. [Google Scholar] [CrossRef] [PubMed]
- Audesse AJ, Dhakal S, Hassell L-A, Gardell Z, Nemtsova Y, Webb AE (2019) FOXO3 directly regulates an autophagy network to functionally regulate proteostasis in adult neural stem cells. PLoS Genet. 2019, 15, e1008097. [CrossRef] [PubMed]
- Shimidzu, N.; Goto, M.; Miki, W. Carotenoids as Singlet Oxygen Quenchers in Marine Organisms. Fish. Sci. 1996, 62, 134–137. [Google Scholar] [CrossRef]
- Miller, N.J.; Sampson, J.; Candeias, L.P.; Bramley, P.M.; Rice-Evans, C.A. Antioxidant activities of carotenes and xanthophylls. FEBS Lett. 1996, 384, 240–242. [Google Scholar] [CrossRef]
- 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]
- Al-Amin, M.M.; Akhter, S.; Hasan, A.T.; Alam, T.; Nageeb Hasan, S.M.; Saifullah, A.R.M.; Shohel, M. The antioxidant effect of astaxanthin is higher in young mice than aged: A region specific study on brain. Metab. Brain Dis. 2015, 30, 1237–1246. [Google Scholar] [CrossRef]
- Lu, Y.; Xie, T.; He, X.X.; Mao, Z.F.; Jia, L.J.; Wang, W.P.; Zhen, J.L.; Liu, L.M. Astaxanthin rescues neuron loss and attenuates oxidative stress induced by amygdala kindling in adult rat hippocampus. Neurosci. Lett. 2015, 597, 49–53. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.S.; Zhang, X.; Zhou, M.L.; Zhou, X.M.; Li, N.; Li, W.; Cong, Z.X.; Sun, Q.; Zhuang, Z.; Wang, C.X.; et al. Amelioration of oxidative stress and protection against early brain injury by astaxanthin after experimental subarachnoid hemorrhage. J. Neurosurg. 2014, 121, 42–54. [Google Scholar] [CrossRef]
- Park, J.S.; Mathison, B.D.; Hayek, M.G.; Zhang, J.; Reinhart, G.A.; Chew, B.P. Astaxanthin modulates age-associated mitochondrial dysfunction in healthy dogs. J. Anim. Sci. 2013, 91, 268–275. [Google Scholar] [CrossRef] [PubMed]
- Balendra, V.; Singh, S.K. Therapeutic potential of astaxanthin and superoxide dismutase in Alzheimer’s disease. Open Biol. 2021, 11, 2021. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, S.M.U.; Luo, L.; Namani, A.; Wang, X.J.; Tang, X. Nrf2 signaling pathway: Pivotal roles in inflammation. Biochim. Biophys. Acta. Mol. Basis Dis. 2017, 1863, 585–597. [Google Scholar] [CrossRef] [PubMed]
- Zhang, R.; Xu, M.; Wang, Y.; Xie, F.; Zhang, G.; Qin, X. Nrf2-a Promising Therapeutic Target for Defensing Against Oxidative Stress in Stroke. Mol. Neurobiol. 2017, 54, 6006–6017. [Google Scholar] [CrossRef]
- Lu, M.C.; Ji, J.A.; Jiang, Z.Y.; You, Q.D. The Keap1-Nrf2-ARE Pathway As a Potential Preventive and Therapeutic Target: An Update. Med. Res. Rev. 2016, 36, 924–963. [Google Scholar] [CrossRef]
- Kim, J.H.; Choi, W.; Lee, J.H.; Jeon, S.J.; Choi, Y.H.; Kim, B.W.; Chang, H.I.; Nam, S.W. Astaxanthin inhibits H2O2-mediated apoptotic cell death in mouse neural progenitor cells via modulation of P38 and MEK signaling pathways. J. Microbiol. Biotechnol. 2009, 19, 1355–1363. [Google Scholar] [CrossRef]
- Yuan, L.; Qu, Y.; Li, Q.; An, T.; Chen, Z.; Chen, Y.; Deng, X.; Bai, D. Protective effect of astaxanthin against La2O3 nanoparticles induced neurotoxicity by activating PI3K/AKT/Nrf-2 signaling in mice. Food Chem. Toxicol. 2020, 144, 111582. [Google Scholar] [CrossRef]
- Han, J.H.; Lee, Y.S.; Im, J.H.; Ham, Y.W.; Lee, H.P.; Han, S.B.; Hong, J.T. Astaxanthin Ameliorates Lipopolysaccharide-Induced Neuroinflammation, Oxidative Stress and Memory Dysfunction through Inactivation of the Signal Transducer and Activator of Transcription 3 Pathway. Mar. Drugs 2019, 17, 123. [Google Scholar] [CrossRef]
- El-Agamy, S.E.; Abdel-Aziz, A.K.; Wahdan, S.; Esmat, A.; Azab, S.S. Astaxanthin Ameliorates Doxorubicin-Induced Cognitive Impairment (Chemobrain) in Experimental Rat Model: Impact on Oxidative, Inflammatory, and Apoptotic Machineries. Mol. Neurobiol. 2018, 55, 5727–5740. [Google Scholar] [CrossRef] [PubMed]
- Wendimu, M.Y.; Hooks, S.B. Microglia Phenotypes in Aging and Neurodegenerative Diseases. Cells 2022, 11, 2091. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Qi, X. The Putative Role of Astaxanthin in Neuroinflammation Modulation: Mechanisms and Therapeutic Potential. Front. Pharmacol. 2022, 13, 916653. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.C. NF-κB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2, 17023. [Google Scholar] [CrossRef] [PubMed]
- Choi, S.K.; Park, Y.S.; Choi, D.K.; Chang, H.I. Effects of Astaxanthin on the Production of NO and the Expression of COX-2 and iNOS in LPS-Stimulated BV2 Microglial Cells. J. Microbiol. Biotechnol. 2008, 18, 1990–1996. [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] [PubMed]
- Bhuvaneswari, S.; Anuradha, C.V. Astaxanthin prevents loss of insulin signaling and improves glucose metabolism in liver of insulin resistant mice. Can. J. Physiol. Pharmacol. 2012, 90, 1544–1552. [Google Scholar] [CrossRef]
- Terazawa, S.; Nakajima, H.; Shingo, M.; Niwano, T.; Imokawa, G. Astaxanthin attenuates the UVB-induced secretion of prostaglandin E2 and interleukin-8 in human keratinocytes by interrupting MSK1 phosphorylation in a ROS depletion-independent manner. Exp. Dermatol. 2012, 21 (Suppl. 1), 11–17. [Google Scholar] [CrossRef]
- Park, S.K.; Kim, K.; Page, G.P.; Allison, D.B.; Weindruch, R.; Prolla, T.A. Gene Expression Profiling of Aging in Multiple Mouse Strains: Identification of Aging Biomarkers and Impact of Dietary Antioxidants. Aging Cell 2009, 8, 484. [Google Scholar] [CrossRef]
- Balietti, M.; Giannubilo, S.R.; Giorgetti, B.; Solazzi, M.; Turi, A.; Casoli, T.; Ciavattini, A.; Fattorettia, P. The effect of astaxanthin on the aging rat brain: Gender-related differences in modulating inflammation. J. Sci. Food Agric. 2016, 96, 615–618. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Medoro, A.; Davinelli, S.; Milella, L.; Willcox, B.J.; Allsopp, R.C.; Scapagnini, G.; Willcox, D.C. Dietary Astaxanthin: A Promising Antioxidant and Anti-Inflammatory Agent for Brain Aging and Adult Neurogenesis. Mar. Drugs 2023, 21, 643. https://doi.org/10.3390/md21120643
Medoro A, Davinelli S, Milella L, Willcox BJ, Allsopp RC, Scapagnini G, Willcox DC. Dietary Astaxanthin: A Promising Antioxidant and Anti-Inflammatory Agent for Brain Aging and Adult Neurogenesis. Marine Drugs. 2023; 21(12):643. https://doi.org/10.3390/md21120643
Chicago/Turabian StyleMedoro, Alessandro, Sergio Davinelli, Luigi Milella, Bradley J. Willcox, Richard C. Allsopp, Giovanni Scapagnini, and Donald Craig Willcox. 2023. "Dietary Astaxanthin: A Promising Antioxidant and Anti-Inflammatory Agent for Brain Aging and Adult Neurogenesis" Marine Drugs 21, no. 12: 643. https://doi.org/10.3390/md21120643