Neuroprotective mechanisms of astaxanthin: a potential therapeutic role in preserving cognitive function in age and neurodegeneration

GeroScience

Volumn 39, Issue 1, 2017, Pages 19-32

  Grimmig, Bethany ^a   Kim, Seol Hee ^a   Nash, Kevin ^b   Bickford, Paula C ^a,c   Douglas Shytle, R ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aging; Astaxanthin; Microglial function; Neural plasticity; Neuroprotection

Indexed keywords

ASTAXANTHIN; NEUROPROTECTIVE AGENT; XANTHOPHYLL;

AGE; AGING; AGROBACTERIUM; AGROBACTERIUM AURANTIACUM; ANALYTICAL ERROR; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; BRAIN INJURY; CAENORHABDITIS ELEGANS; CHLORELLA; CHLORELLA ZOFINGIENSIS; CHLOROCOCCUM; CLINICAL TRIAL (TOPIC); COGNITIVE DEFECT; HAEMATOCOCCUS PLUVIALIS; HIPPOCAMPUS; HUMAN; LEARNING TEST; MAZE TEST; MENTAL DISEASE ASSESSMENT; MICROALGA; MILD COGNITIVE IMPAIRMENT; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLASTOMA; NEUROPATHY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOPHYSIOLOGY; PHAFFIA RHODOZYMA; RANDOMIZED CONTROLLED TRIAL (TOPIC); RECOGNITION; REVIEW; SELECTIVE ATTENTION; TREATMENT DURATION; ANIMAL; DEGENERATIVE DISEASE; DIETARY SUPPLEMENT; DRUG EFFECTS; PHYSIOLOGY; PROGNOSIS; RISK ASSESSMENT; TREATMENT OUTCOME;

AGING; ANIMALS; DIETARY SUPPLEMENTS; HUMANS; NEURODEGENERATIVE DISEASES; NEUROPROTECTION; NEUROPROTECTIVE AGENTS; PROGNOSIS; RISK ASSESSMENT; TREATMENT OUTCOME; XANTHOPHYLLS;

EID: 85017201647     PISSN: 25092715     EISSN: 25092723     Source Type: Journal    
DOI: 10.1007/s11357-017-9958-x     Document Type: Review

References (93)

1. Abadie-Guedes R, Santos SD, Cahu TB, Guedes RC, de Souza Bezerra R (2008) Dose-dependent effects of astaxanthin on cortical spreading depression in chronically ethanol-treated adult rats. Alcohol Clin Exp Res 32:1417–1421
2. Acosta S, Jernberg J, Sanberg C, Sanberg P, Small BJ, Gemma C, Bickford PC (2010) NT-020, a natural therapeutic approach to optimize spatial memory performance and increase neural progenitor cell proliferation and decrease inflammation in the aged rat. Rejuvenation Res 13:581–588
3. Al-Amin MM, Akhter S, Hasan AT, Alam T, Hasan SN, Saifullah A, Shohel M (2015a) The antioxidant effect of astaxanthin is higher in young mice than aged: a region specific study on brain. Metab Brain Dis 30:1237–1246
4. Al-Amin MM, Rahman MM, Khan FR, Zaman F, Mahmud Reza H (2015b) Astaxanthin improves behavioral disorder and oxidative stress in prenatal valproic acid-induced mice model of autism. Behav Brain Res 286:112–121. doi:10.1016/j.bbr.2015.02.041
5. Al-Amin MM et al (2016a) Astaxanthin ameliorates aluminum chloride-induced spatial memory impairment and neuronal oxidative stress in mice. Eur J Pharmacol 777:60–69
6. Al-Amin MM, Sultana R, Sultana S, Rahman MM, Reza HM (2016b) Astaxanthin ameliorates prenatal LPS-exposed behavioral deficits and oxidative stress in adult offspring BMC neuroscience 17:1
7. Ambati RR, Phang S-M, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Marine Drugs 12:128–152
8. Arvanitakis Z, Fleischman DA, Arfanakis K, Leurgans SE, Barnes LL, Bennett DA (2016) Association of white matter hyperintensities and gray matter volume with cognition in older individuals without cognitive impairment. Brain Struct Funct 221:2135–2146. doi:10.1007/s00429-015-1034-7
9. Bachstetter AD et al (2010) Spirulina promotes stem cell genesis and protects against LPS induced declines in neural stem cell proliferation. PLoS One 5:e10496
10. Balietti M et al (2016) The effect of astaxanthin on the aging rat brain: gender-related differences in modulating inflammation. J Sci Food Agric 96:615–618
11. Barros MP, Poppe SC, Bondan EF (2014) Neuroprotective properties of the marine carotenoid astaxanthin and omega-3 fatty acids, and perspectives for the natural combination of both in krill oil. Nutrients 6:1293–1317
12. Bickford PC et al (2015) Nutraceutical intervention reverses the negative effects of blood from aged rats on stem cells. Age 37:1–7
13. Bosman G, Bartholomeus I, De Man A, Van Kalmthout P, De Grip W (1991) Erythrocyte membrane characteristics indicate abnormal cellular aging in patients with Alzheimer’s disease. Neurobiol Aging 12:13–18
14. Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117
15. Boussiba S, Bing W, Yuan J-P, Zarka A, Chen F (1999) Changes in pigments profile in the green alga Haematococcus pluvialis exposed to environmental stresses. Biotechnol Lett 21:601–604
16. Capelli B, Bagchi D, Cysewski GR (2013) Synthetic astaxanthin is significantly inferior to algal-based astaxanthin as an antioxidant and may not be suitable as a human nutraceutical supplement. Nutrafoods 12:145–152. doi:10.1007/s13749-013-0051-5
17. Chang C-H, Chen C-Y, Chiou J-Y, Peng RY, Peng C-H (2010) Astaxanthine secured apoptotic death of PC12 cells induced by β-amyloid peptide 25–35: its molecular action targets. J Med Food 13:548–556
18. Chew BP, Mathison BD, Hayek MG, Massimino S, Reinhart GA, Park JS (2011) Dietary astaxanthin enhances immune response in dogs. Vet Immunol Immunopathol 140:199–206
19. Choi HD, Kang HE, Yang SH, Lee MG, Shin WG (2011) Pharmacokinetics and first-pass metabolism of astaxanthin in rats. Br J Nutr 105:220–227
20. Choi S-K, Park Y-S, Choi D-K, Chang H-I (2008) 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 18:1990–1996
21. Ekdahl CT, Claasen J-H, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci 100:13632–13637
22. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247
23. Furr HC, Clark RM (1997) Intestinal absorption and tissue distribution of carotenoids. J Nutr Biochem 8:364–377
24. Giavarotti L et al. (2013) Mild systemic oxidative stress in the subclinical stage of Alzheimer’s disease Oxidative medicine and cellular longevity
25. Glisky EL (2007) Changes in cognitive function in human aging brain aging: models, methods, and mechanisms:3–20
26. Goodall H, Reid A, Findlay D, Hind C, Kay J, Coghill G (1994) Irregular distortion of the erythrocytes (acanthocytes, spur cells) in senile dementia. Dis Markers 12:23–41
27. Grimmig B, Morganti J, Nash K, Bickford PC (2016) Immunomodulators as therapeutic agents in mitigating the progression of Parkinson’s disease brain. Sciences 6:41
28. Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21:210–216
29. Haider S et al (2014) Age-related learning and memory deficits in rats: role of altered brain neurotransmitters, acetylcholinesterase activity and changes in antioxidant defense system. Age 36:1291–1302
30. Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea F (2006) Astaxanthin: a review of its chemistry and applications. Crit Rev Food Sci Nutr 46:185–196
31. Hussein G, Nakamura M, Zhao Q, Iguchi T, Goto H, Sankawa U, Watanabe H (2005) Antihypertensive and neuroprotective effects of astaxanthin in experimental animals. Biol Pharm Bull 28:47–52
32. Jackson H, Braun CL, Ernst H (2008) The chemistry of novel xanthophyll carotenoids. Am J Cardiol 101:S50–S57. doi:10.1016/j.amjcard.2008.02.008
33. Jenner P, Olanow CW (1996) Oxidative stress and the pathogenesis of Parkinson’s disease. Neurology 47:161S–170S
34. Katagiri M, Satoh A, Tsuji S, Shirasawa T (2012) Effects of astaxanthin-rich Haematococcus pluvialis extract on cognitive function: a randomised, double-blind, placebo-controlled study. J Clin Biochem Nutr 51:102–107
35. Kaulmann A, Bohn T (2014) Carotenoids, inflammation, and oxidative stress—implications of cellular signaling pathways and relation to chronic disease prevention. Nutr Res 34:907–929
36. Kawamoto EM et al (2005) Oxidative state in platelets and erythrocytes in aging and Alzheimer’s disease. Neurobiol Aging 26:857–864
37. Kawamoto EM, Vasconcelos AR, Degaspari S, Böhmer AE, Scavone C, Marcourakis T (2013) Age-related changes in nitric oxide activity, cyclic GMP, and TBARS levels in platelets and erythrocytes reflect the oxidative status in central nervous system. Age 35:331–342
38. Kettenmann H, Hanisch U-K, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91:461–553
39. Kidd P (2011) Astaxanthin, cell membrane nutrient with diverse clinical benefits and anti-aging potential. Altern Med Rev 16:355–364
40. Kim J-H et al (2009) Astaxanthin inhibits H, O,-mediated apoptotic cell death in mouse neural progenitor cells via modulation of P38 and MEK signaling pathways. J Microbiol Biotechnol 19:1355–1363
41. Kim J-H, Kim Y-S, Song G-G, Park J-J, Chang H-I (2005) Protective effect of astaxanthin on naproxen-induced gastric antral ulceration in rats. Eur J Pharmacol 514:53–59
42. Kim J-H, Nam S-W, Kim B-W, Choi W, Lee J-H, Kim W-J, Choi Y-H (2010a) Astaxanthin improves stem cell potency via an increase in the proliferation of neural progenitor cells. Int J Mol Sci 11:5109–5119
43. Kim YH, Koh HK, Kim DS (2010b) Down-regulation of IL-6 production by astaxanthin via ERK-, MSK-, and NF-kappaB-mediated signals in activated microglia. Int Immunopharmacol 10:1560–1572
44. Komaki A, Karimi SA, Salehi I, Sarihi A, Shahidi S, Zarei M (2015) The treatment combination of vitamins E and C and astaxanthin prevents high-fat diet induced memory deficits in rats. Pharmacol Biochem Behav 131:98–103
45. Kosenko E, Tikhonova L, Poghosyan A, Kaminsky Y (2013) Antioxidants in erythrocytes in aging and dementia. Biomeditsinskaya khimiya 59:443–451
46. Koutsilieri E, Scheller C, Tribl F, Riederer P (2002) Degeneration of neuronal cells due to oxidative stress—microglial contribution. Parkinsonism Relat Disord 8:401–406
47. Lee D-H, Lee YJ, Kwon KH (2010) Neuroprotective effects of astaxanthin in oxygen-glucose deprivation in SH-SY5Y cells and global cerebral ischemia in rat. J Clin Biochem Nutr 47:121–129
48. Lee D-H, Kim C-S, Lee YJ (2011) Astaxanthin protects against MPTP/MPP + −induced mitochondrial dysfunction and ROS production in vivo and in vitro. Food Chem Toxicol 49:271
49. Li Z et al. (2013) Astaxanthin protects ARPE-19 cells from oxidative stress via upregulation of Nrf2-regulated phase II enzymes through activation of PI3K/Akt
50. Liu X, Luo Q, Cao Y, Goulette T, Liu X, Xiao H (2016) Mechanism of different stereoisomeric astaxanthin in resistance to oxidative stress in Caenorhabditis elegans. J Food Sci
51. Liu X, Shibata T, Hisaka S, Osawa T (2009a) Astaxanthin inhibits reactive oxygen species-mediated cellular toxicity in dopaminergic SH-SY5Y cells via mitochondria-targeted protective mechanism. Brain Res 1254:18–27. doi:10.1016/j.brainres.2008.11.076
52. Liu X, Shibata T, Hisaka S, Osawa T (2009b) Astaxanthin inhibits reactive oxygen species-mediated cellular toxicity in dopaminergic SH-SY5Y cells via mitochondria-targeted protective mechanism. Brain Res 13:18–27
53. Lobos P et al (2016) Astaxanthin protects primary hippocampal neurons against noxious effects of Abeta-oligomers. Neural Plast 3456783:1
54. Lu Y et al (2015) Astaxanthin rescues neuron loss and attenuates oxidative stress induced by amygdala kindling in adult rat hippocampus. Neurosci Lett 597:49–53
55. Lynch MA (2009) Age-related neuroinflammatory changes negatively impact on neuronal function
56. Naguib YM (2000) Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 48:1150–1154
57. Nakagawa K, Kiko T, Miyazawa T, Burdeos GC, Kimura F, Satoh A, Miyazawa T (2011) Antioxidant effect of astaxanthin on phospholipid peroxidation in human erythrocytes. Br J Nutr 105:1563–1571
58. Nguyen KD (2013) Astaxanthin: a comparative case of synthetic vs. natural production
59. Mattei R, Polotow TG, Vardaris CV, Guerra BA, Leite JR, Otton R, Barros MP (2011) Astaxanthin limits fish oil-related oxidative insult in the anterior forebrain of Wistar rats: putative anxiolytic effects? Pharmacol Biochem Behav 99:349–355
60. Odeberg JM, Lignell Å, Pettersson A, Höglund P (2003) Oral bioavailability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations. Eur J Pharm Sci 19:299–304
61. Østerlie M, Bjerkeng B, Liaaen-Jensen S (2000) Plasma appearance and distribution of astaxanthin E/Z and R/S isomers in plasma lipoproteins of men after single dose administration of astaxanthin1. J Nutr Biochem 11:482–490. doi:10.1016/S0955-2863(00)00104-2
62. Otton R, Marin DP, Bolin AP, dos Santos RD, Polotow TG, Sampaio SC, de Barros MP (2010) Astaxanthin ameliorates the redox imbalance in lymphocytes of experimental diabetic rats. Chem Biol Interact 186:306–315
63. Panis G, Carreon JR (2016) Commercial astaxanthin production derived by green alga Haematococcus pluvialis: a microalgae process model and a techno-economic assessment all through production line. Algal Res 18:175–190 doi:10.1016/j.algal.2016.06.007
64. Park SK, Kim K, Page GP, Allison DB, Weindruch R, Prolla TA (2009) Gene expression profiling of aging in multiple mouse strains: identification of aging biomarkers and impact of dietary antioxidants. Aging cell 8:484–495
65. Park J, Mathison B, Hayek M, Zhang J, Reinhart G, Chew B (2013) Astaxanthin modulates age-associated mitochondrial dysfunction in healthy dogs. J Anim Sci 91:268–275
66. Peng S, Zhang Y, Zhang J, Wang H, Ren B (2010) ERK in learning and memory: a review of recent research. Int J Mol Sci 11:222–232
67. Polich J, Ehlers CL, Otis S, Mandell AJ, Bloom FE (1986) P300 latency reflects the degree of cognitive decline in dementing illness. Electroencephalogr Clin Neurophysiol 63:138–144
68. Puertas M, Martinez-Martos J, Cobo M, Carrera M, Mayas M, Ramirez-Exposito M (2012) Plasma oxidative stress parameters in men and women with early stage Alzheimer type dementia. Exp Gerontol 47:625–630
69. Régnier P et al (2015) Astaxanthin from Haematococcus pluvialis prevents oxidative stress on human endothelial cells without toxicity. Marine drugs 13:2857–2874
70. Sahay A et al (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470
71. Satoh A et al (2009a) Preliminary clinical evaluation of toxicity and efficacy of a new astaxanthin-rich Haematococcus pluvialis extract. J Clin Biochem Nutr 44:280–284
72. Satoh A et al (2009b) Preliminary clinical evaluation of toxicity and efficacy of a new astaxanthin-rich Haematococcus pluvialis extract. J Clin Biochem Nutr 44:280–284
73. Seabra LMAJ, LFC P (2010) Astaxanthin: structural and functional aspects. Rev Nutr 23:1041–1050
74. Shen H et al (2009) Astaxanthin reduces ischemic brain injury in adult rats. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 23:1958–1968
75. Shetty GA, Hattiangady B, Shetty AK (2013) Neural stem cell-and neurogenesis-related gene expression profiles in the young and aged dentate gyrus. Age 35:2165–2176
76. Stranahan AM, Mattson MP (2012) Recruiting adaptive cellular stress responses for successful brain ageing. Nat Rev Neurosci 13:209–216
77. Thangthaeng N, Poulose SM, Gomes SM, Miller MG, Bielinski DF, Shukitt-Hale B (2016) Tart cherry supplementation improves working memory, hippocampal inflammation, and autophagy in aged rats. Age 38:393–404
78. Wahl D et al (2016) Nutritional strategies to optimise cognitive function in the aging brain. Ageing Res Rev 31:80–92
79. Wang H-Q, Sun X-B, Xu Y-X, Zhao H, Zhu Q-Y, Zhu C-Q (2010) 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 1360:159–167
80. Wang X, Michaelis EK (2010) Selective neuronal vulnerability to oxidative stress in the brain Frontiers in aging neuroscience 2:12
81. Wibrand K, Berge K, Messaoudi M, Duffaud A, Panja D, Bramham CR, Burri L (2013) Enhanced cognitive function and antidepressant-like effects after krill oil supplementation in rats. Lipids Health Dis 12:12–16
82. Woodside JV, McGrath AJ, Lyner N, MC MK (2015) Carotenoids and health in older people. Maturitas 80:63–68
83. Wu W et al (2014) Astaxanthin alleviates brain aging in rats by attenuating oxidative stress and increasing BDNF levels. Food Funct 5:158–166
84. Xu L, Zhu J, Yin W, Ding X (2015) 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 8:6083–6094
85. Ye Q, Huang B, Zhang X, Zhu Y, Chen X (2012) Astaxanthin protects against MPP(+)-induced oxidative stress in PC12 cells via the HO-1/NOX2 axis BMC. Neurosci 13:1471–2202
86. Yook JS et al (2016) Astaxanthin supplementation enhances adult hippocampal neurogenesis and spatial memory in mice. Mol Nutr Food Res 60:589–599
87. Yuan J-P, Chen F, Liu X, Li X-Z (2002) Carotenoid composition in the green microalga. Chlorococcum Food Chemistry 76:319–325
88. Yuan JP, Peng J, Yin K, Wang JH (2011) Potential health-promoting effects of astaxanthin: a high-value carotenoid mostly from microalgae. Mol Nutr Food Res 55:150–165
89. Zhang X, Pan L, Wei X, Gao H, Liu J (2007) Impact of astaxanthin-enriched algal powder of Haematococcus pluvialis on memory improvement in BALB/c mice. Environ Geochem Health 29:483–489. doi:10.1007/s10653-007-9117-x
90. Zhang XS et al (2014a) Astaxanthin offers neuroprotection and reduces neuroinflammation in experimental subarachnoid hemorrhage. J Surg Res 192:206–213
91. Zhang XS et al (2014b) Astaxanthin alleviates early brain injury following subarachnoid hemorrhage in rats: possible involvement of Akt/bad signaling. Mar Drugs 12:4291–4310
92. Zhang XS et al (2014c) Amelioration of oxidative stress and protection against early brain injury by astaxanthin after experimental subarachnoid hemorrhage. Journal of Neurosurgery 121:42–54
93. Zhou X et al (2015) Inhibition of inflammation by astaxanthin alleviates cognition deficits in diabetic mice. Physiol Behav 151:412–420