Neuroprotective properties of the marine carotenoid astaxanthin and omega-3 fatty acids, and perspectives for the natural combination of both in krill oil

Nutrients

Volumn 6, Issue 3, 2014, Pages 1293-1317

  Barros, Marcelo P ^a   Poppe, Sandra C ^a,b   Bondan, Eduardo F ^a,b  

^a UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

^b PAULISTA UNIVERSITY   (Brazil)

Author keywords

Alzheimer's; Anti inflammatory; Antioxidant; Cognition; Hormesis; Natural products; Neurodegenerative disorders; Oxidative stress; Parkinson's; Seafood

Indexed keywords

AMYLOID BETA PROTEIN; ARACHIDONIC ACID; ASCORBIC ACID; ASTAXANTHIN; CAROTENOID; CASPASE 9; CATALASE; CREATINE KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTAMATE AMMONIA LIGASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KRILL OIL; NATURAL PRODUCT; OMEGA 3 FATTY ACID; OXIDOPAMINE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE; TOCOPHEROL; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; URATE;

AMYOTROPHIC LATERAL SCLEROSIS; ANTIGEN PRESENTING CELL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; CLINICAL TRIAL (TOPIC); CYTOTOXICITY; DEGENERATIVE DISEASE; DNA REPAIR; ENZYME ACTIVITY; HUMAN; IMMUNE RESPONSE; MENTAL HEALTH; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PARKINSON DISEASE; PHOTOOXIDATION; REVIEW; SEA FOOD; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; EUPHAUSIACEA; FATTY ACIDS, OMEGA-3; FISH OILS; HUMANS; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; OBSERVATIONAL STUDY AS TOPIC; OXIDATION-REDUCTION; OXIDATIVE STRESS; SHELLFISH; XANTHOPHYLLS;

EID: 84897068159     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu6031293     Document Type: Review

References (174)

1. Wang, J.-Y.; Wen, Y.-L.; Huan, Y.-N.; Chen, T.; Ku, M.-C. Dual effects of antioxidants in neurodegeneration: Direct neuroprotection against oxidative stress and indirect protection via suprresion of gliamediated inflammation. Curr. Pharm. Des. 2006, 12, 3521-3533.
2. Buonocore, G.; Perrone, S.; Tataranno, M. L. Oxygen toxicity: Chemistry and biology of reactive oxygen species. Semin. Fetal Neonatal Med. 2010, 15, 186-190.
3. Schiavone, S.; Jaquet, V.; Trabace, L.; Krause, K.-H. Severe life stress and oxidative stress in the brain: From animal models to human pathology. Antioxid. Redox. Signal. 2013, 18, 1475-1490.
4. Emerit, J.; Edeas, M.; Bricaire, F. Neurodegenerative diseases and stress. Biomed. Pharmacother. 2004, 58, 39-46.
5. Bedard, K.; Krause, K. The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol. Rev. 2007, 87, 245-313.
6. Drechsel, D. A.; Estévez, A. G.; Barbeito, L.; Beckman, J. S. Nitric oxide-mediated oxidative damage and the progressive demise of motor neurons in ALS. Neurotox. Res. 2012, 22, 251-264.
7. Kannan, K.; Jain, S. K. Oxidative stress. Pathophysiology 2000, 7, 153-157.
8. Schafer, F. Q.; Buettner, G. R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2001, 30, 1191-1212.
9. Gomez-Cabrera, M. C.; Viña, J.; Ji, L. L. Interplay of oxidants and antioxidants during exercise: Implications for muscle health. Phys. Sportsmed. 2009, 37, 16-23.
10. Choi, B. H. Oxygen, antioxidants and brain dysfunction. Yonsei Med. J. 1993, 34, 1-10.
11. Halliwell, B. Oxidative stress and neurodegeneration: Where are we now? J. Neurochem. 2006, 97, 1634-1658.
12. Stoll, G.; Jander, S.; Schroeter, M. Inflammation and glial responses in ischemic brain lesions. Prog. Neurobiol. 1998, 56, 149-171.
13. Repetto, M. G.; Reides, C. G.; Evelson, P.; Kohan, S.; de Lustig, E. S.; Llesuy, S. F. Peripheral markers of oxidative stress in probable Alzheimer patients. Eur. J. Clin. Investig. 1999, 29, 643-649.
14. Migliore, L.; Fontana, I.; Colognato, R.; Coppede, F.; Siciliano, G.; Murri, L. Searching for the role and the most suitable biomarkers of oxidative stress in Alzheimer's disease and in other neurodegenerative diseases. Neurobiol. Aging 2005, 26, 587-595.
15. Ikeda, K.; Negishi, H.; Yamori, Y. Antioxidant nutrients and hypoxia/ischemia brain injury in rodents. Toxicology 2003, 189, 55-61.
16. Gutteridge, J. M. C.; Halliwell, B. Antioxidants: Molecules, medicines, and myths. Biochem. Biophys. Res. Commun. 2010, 393, 561-564.
17. Koutsilieri, E.; Scheller, C.; Tribl, F.; Riederer, P. Degeneration of neuronal cells due to oxidative stress-Microglial contribution. Parkinsonism Relat. Disord. 2002, 8, 401-406.
18. Mattson, M. P.; Cheng, A. Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci. 2006, 29, 632-639.
19. Wang, Q.; Xu, J.; Rottinghaus, G. E.; Simonyi, A.; Lubahn, D.; Sun, G. Y.; Sun, A. Y. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 2002, 958, 439-447.
20. Kaplan, S.; Bisleri, G.; Morgan, J. A.; Cheema, F. H.; Oz, M. C. Resveratrol, a natural red wine polyphenol, reduces ischemia-reperfusion-induced spinal cord injury. Ann. Thorac. Surg. 2005, 80, 2242-2249.
21. Ohshima, Y.; Mizuno, T.; Yamada, K.; Matsumoto, S.; Nagakane, Y.; Kondo, M.; Kuriyama, N.; Miyazaki, T.; Takeda, K.; Nishimura, T.; et al. Low vitamin and carotenoid levels are related to cerebral white matter lesions. J. Nutr. Health Aging 2013, 17, 456-460.
22. Mattei, R.; Polotow, T. G.; Vardaris, C. V.; Guerra, B. A.; Leite, J. R.; Otton, R.; Barros, M. P. Astaxanthin limits fish oil-related oxidative insult in the anterior forebrain of Wistar rats: Putative anxiolytic effects? Pharmacol. Biochem. Behav. 2011, 99, 349-355.
23. Mattson, M. P.; Meffert, M. K. Roles for NF-κB in nerve cell survival, plasticity, and disease. Cell Death Differ. 2006, 13, 852-860.
24. West, A. E.; Chen, W. G.; Dalva, M. B.; Dolmetsch, R. E.; Kornhauser, J. M.; Shaywitz, A. J.; Takasu, M. A.; Tao, X.; Greenberg, M. E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA 2001, 98, 11024-11031.
25. Jeong, W. S.; Jun, M.; Kong, A. N. Nrf2: A potential molecular target for cancer chemoprevention by natural compounds. Antioxid. Redox. Signal. 2006, 8, 99-106.
26. Liu, J.; Narasimhan, P.; Yu, F.; Chan, P. H. Neuroprotection by hypoxic preconditioning involves oxidative stress-mediated expression of hypoxia-inducible factor and erythropoietin. Stroke 2005, 36, 1264-1269.
27. Kalyanaraman, B. Teaching the basics of redox biology to medical and graduate students: Oxidants, antioxidants and disease mechanisms. Redox. Biol. 2013, 1, 244-257.
28. Zhang, M.; An, C.; Gao, Y.; Leak, R. K.; Chen, J.; Zhang, F. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog. Neurobiol. 2013, 100, 30-47.
29. De Vries, H. E.; Witte, M.; Hondius, D.; Rozemuller, A. J. M.; Drukarch, B.; Hoozemans, J.; van Horssen, J. Nrf2-induced antioxidant protection: A promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic. Biol. Med. 2008, 45, 1375-1383.
30. Bains, M.; Hall, E. D. Antioxidant therapies in traumatic brain and spinal cord injury. Biochim. Biophys. Acta. 2012, 1822, 675-684.
31. Currais, A.; Maher, P. Functional consequences of age-dependent changes in glutathione status in the brain. Antioxid. Redox. Signal. 2013, 19, 813-822.
32. Klegeris, A.; Walker, D. G.; McGeer, P. L. Activation of macrophages by Alzheimer beta amyloid peptide. Biochem. Biophys. Res. Commun. 1994, 199, 984-991.
33. Meda, L.; Cassatella, M. A.; Szendrei, G. I.; Otvos, L., Jr.; Villalba, M.; Ferrari, D.; Rossi, F. Activation of microglial cells by β-amyloid protein and interferon-gamma. Nature 1995, 374, 647-650.
34. Liu, F.; McCullough, L. D. Inflammatory responses in hypoxic ischemic encephalopathy. Acta Pharmacol. Sin. 2013, 34, 1121-1130.
35. Juurlink, B. H. Response of glial cells to ischemia: Roles of reactive oxygen species and glutathione. Neurosci. Biobehav. Rev. 1997, 21, 151-166.
36. Thorborne, S. K.; Juurlink, B. H. Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 1996, 67, 1014-1022.
37. Hollensworth, S. B.; Shen, C.; Sim, J. E.; Spitz, D. R.; LeDoux, S. P. Glial cell type-specific responses to menadione-induced oxidative stress. Free Radic. Biol. Med. 2000, 28, 1161-1174.
38. Dringen, R. Metabolism and functions of glutathione in brain. Prog. Neurobiol. 2000, 62, 649-671.
39. Burgoyne, R. D.; Pearce, I. A.; Cambray-Deakin, M. N-Methyl-D-aspartate raises cytosolic calcium concentration in rat cerebellar granule cells in culture. Neurosci. Lett. 1988, 91, 47-52.
40. Kambe, Y.; Nakamichi, N.; Takarada, T.; Fukumori, R.; Nakazato, R.; Hinoi, E.; Yoneda, Y. A possible pivotal role of mitochondrial free calcium in neurotoxicity mediated by N-methyl-D-aspartate receptors in cultured rat hippocampal neurons. Neurochem. Int. 2011, 59, 10-20.
41. Le, T. M.; Jiang, H.; Cunningham, G. R.; Magarik, J. A.; Barge, W. S.; Cato, M. C.; Farina, M.; Rocha, J. B. T.; Milatovic, D.; Lee, E.; et al. γ-Glutamylcysteine ameliorates oxidative injury in neurons and astrocytes in vitro and increases brain glutathione in vivo. Neurotoxicology 2011, 32, 518-525.
42. Butterfield, D. A.; Drake, J.; Pocernich, C.; Castegna, A. Evidence of oxidative damage in Alzheimer's disease brain: Central role for amyloid β-peptide. Trends Mol. Med. 2001, 7, 548-554.
43. Bandy, B.; Davidson, A. J. Mitochondrial mutations may increase oxidative stress. Free Radic. Biol. Med. 1990, 8, 523-529.
44. Reddy, P. H.; Reddy, T. P. Mitochondria as a therapeutic target for aging and neurodegenerative diseases. Curr. Alzheimer Res. 2011, 8, 393-409.
45. Federico, A.; Cardaioli, E.; Da Pozzo, P.; Formichi, P.; Gallus, G. N.; Radi, E. Mitochondria, oxidative stress and neurodegeneration. J. Neurol. Sci. 2012, 322, 254-262.
46. Cassarino, D. S.; Bennett, J. P., Jr. An evaluation of the role of mitochondria in neurodegenerative diseases: Mitochondrial and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 1999, 29, 1-25.
47. Bredt, D. S.; Snyder, S. H. Nitric oxide: A physiologic messenger molecule. Ann. Rev. Biochem. 1994, 63, 175-195.
48. Smith, J. A.; Park, S.; Krause, J. S.; Banik, N. L. Oxidative stress, DNA damage, and the telomeric complex as therapeutic targets in acute neurodegeneration. Neurochem. Int. 2013, 62, 764-775.
49. Markesbery, W. Oxidative stress hypothesis in Alzheimer's disease. Free. Radic. Biol. Med. 1997, 23, 134-147.
50. Draczynska-Lusiak, B.; Doung, A.; Sun, A. Y. Oxidized lipoproteins may play a role in neuronal cell dath in Alzheimer disease. Mol. Chem. Neuropathol. 1998, 33, 139-148.
51. Smith, M. A.; Rottkamp, C. A.; Nunomura, A.; Raina, A. K.; Perry, G. Oxidative stress in Alzheimer's disease. Biochim. Biophys. Acta 2000, 1502, 139-144.
52. Varadarajan, S.; Yatin, S.; Aksenova, M.; Butterfield, D. A. Alzheimer's amyloid β-peptide-associated free radical oxidative stress. J. Struct. Biol. 2000, 130, 184-208.
53. Butterfield, D. A. Amyloid beta-peptide (1, 42)-induced oxidative stress and neurotoxicity: Implications form neurodegeneration in Alzheimer's disease brain. A review. Free Radic. Res. 2002, 12, 1307-1313.
54. Butterfield, D. A.; Castegna, A.; Lauderback, C. M.; Drake, J. Evidence that amyloid beta-peptide-induced peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol. Aging 2002, 23, 655-664.
55. Butterfield, D. A.; Lauderback, C. M. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: Potential causes and consequences involving amyloid β-peptide-associated free radical oxidative stress. Free. Radic. Biol. Med. 2002, 32, 1050-1060.
56. Montine, T. J.; Neely, M. D.; Quinn, J. F.; Beal, M. F.; Markesbery, W. R.; Roberts, L. J., II; Morrow, J. D. Lipid peroxidation in aging brain and Alzheimer's disease. Free. Radic. Biol. Med. 2002, 33, 620-626.
57. Perry, G.; Taddeo, M. A.; Nunomura, A.; Zhu, X.; Zenteno-Svin, T.; Drew, K. L.; Shimohamam, S.; Avila, J.; Castellani, R. J.; Smith, M. A. Comparative biology and pathology of oxidative stress in Alzheimer and other neurodegenerative diseases: Beyond damage and response. Comp. Biochem. Physiol. 2002, 133, 507-513.
58. Gilkun-Sherki, Y.; Melamed, E.; Offen, D. Antioxidant treatment in Alzheimer's disease: Current state. J. Mol. Neurosci. 2003, 21, 1-11.
59. Meraz-Ríos, M. A.; Franco-Bocanegra, D.; Toral-Rios, D.; Campos-Peña, V. Early onset Alzheimer's disease and oxidative stress. Oxid. Med. Cell. Longev. 2014, 2014, 375968.
60. Chauhan, V.; Chauhan, A. Oxidative stress in Alzheimer's disease. Pathophysiology 2006, 13, 195-208.
61. Nunomura, A.; Moreira, P. I.; Lee, H. G.; Zhu, X.; Castellani, R. J.; Smith, M. A.; Perry, G. Neuronal cell death and survival under oxidative stress in Alzheimer and Parkinson disease. CNS Neurol. Disord. Drug Targets 2007, 6, 411-423.
62. Marlatt, M. W.; Lucassen, P. J.; Perry, G.; Smith, M. A.; Zhu, X. Alzheimer's disease: Cerebrovascular dysfunction, oxidative stress, and advanced clinical therapies. J. Alzheimer Dis. 2008, 15, 199-210.
63. Koudinov, A.; Koudinova, K. E.; Berezov, T. Amyloid-β, tau protein, and oxidative changes as a physiological compensatory mechanism to maintain CNS plasticity under Alzheimer's disease and other degenerative conditions. J. Alzheimer Dis. 2009, 18, 381-400.
64. Butterfield, D. A.; Langue, M. L. B.; Sultana, R. Involvements of the lipid peroxidation production, HNE, in the pathogenesis and progression of Alzheimer's disease. Biochim. Biophys. Acta 2010, 180, 924-929.
65. Whitton, P. S. Inflammation as a causative factor in the aethiology of Parkinson's disease. Br. J. Pharmacol. 2007, 150, 963-976.
66. Qian, L.; Flood, P. M.; Hong, J.-S. Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J. Neural Transm. 2010, 117, 971-979.
67. Sierra, A.; Abiega, O.; Shahraz, A.; Neumann, H. Janus-faced microglia: Beneficial and detrimental consequences of microglial phagocytosis. Front. Cell. Neurosci. 2013, 7, 6.
68. Koppula, C.; Kumar, H.; More, S. V.; Kim, B. W.; Kim, I. S.; Choi, D. K. Recent advances on the neuroprotective potential of antioxidants in experimental models of Parkinson's disease. Int. J. Mol. Sci. 2012, 13, 10608-10629.
69. Barber, S. C.; Shaw, P. J. Oxidative stress in ALS: A key role in motor neuron injury and therapeutic target. Free Radic. Biol. Med. 2010, 48, 629-641.
70. Galea, E.; Launay, N.; Portero-Otin, M.; Ruiz, M.; Pamplona, R.; Aubourg, P.; Ferrer, I.; Pujol, A. Oxidative stress underlying axonal degeneration in adrenoleukodystrophy: A paradigm for multifactorial neurodegenerative disease? Biochim. Biophys. Acta 2012, 1822, 1475-1488.
71. Reddy, P. H.; Mao, P.; Manczak, M. Mitochondrial structural and functional dynamics in Huntington's disease. Brain Res. Rev. 2009, 61, 33-48.
72. Shin, E.-J.; Jeong, J. H.; Chung, Y. H.; Kim, W.-K.; KO, K.-H.; Bach, J.-H.; Hong, J.-S.; Yoneda, Y.; Kim, H.-C. Role of oxidative stress in epileptic seizures. Neurochem. Int. 2011, 59, 122-137.
73. Mariani, E.; Polidori, M. C.; Cherubini, A.; Mecocci, P. Oxidative stress in brain aging, neurodegenerative and vascular diseases: An overview. J. Chromatogr. 2005, 827, 65-75.
74. Valcour, V.; Shiramizu, B. HIV-associated dementia, mitochondrial dysfunction, and oxidative stress. Mitochondrion 2004, 4, 119-129.
75. Rawdin, B. J.; Mellon, S. H.; Dhabhar, F. S.; Epel, E. S.; Puterman, E.; Burke, H. M.; Reus, V. I.; Rosser, R.; Hamilton, S. P.; Nelson, J. C.; et al. Dysregulated relationship of inflammation and oxidative stress in major depression. Brain Behav. Immun. 2013, 31, 143-152.
76. Anderson, G.; Maes, M.; Berk, M. Schizophrenia is primed for an increased expression of depression through activation of immune-inflammatory, oxidative and nitrosative stress, and tryptophan catabolite pathways. Prog. Neuro-Psycopharmacol. Biol. Psichyatry 2013, 42, 101-114.
77. Frustaci, A.; Neri, M.; Cesario, A.; Adams, J. B.; Domeneci, E.; Dalla Bernardina, B.; Bonassi, S. Oxidative stress-related biomarkers in autism: Systematic review and meta-analysis. Free Radic. Biol. Med. 2012, 52, 2128-2141.
78. Corsinovi, L.; Biasi, F.; Poli, G.; Leonarduzzi, G.; Isaia, G. Dietary lipids and their oxidized products in Alzheimer's disease. Mol. Nutr. Food Res. 2011, 55, S161-S172.
79. Rodriguez-Amaya, D. B. Quantitative analysis, in vitro assessment of bioavailability and antioxidant activity of food carotenoids-A review. J. Food Comp. Anal. 2010, 23, 726-740.
80. Britton, G. Carotenoids: Spectroscopy, 1st ed.; Britton, G., Liaaen-Jensen, S., Pfander, H., Eds.; Birkhäuser: Basel, Switzerland, 1995; Volume 1B, pp. 13-62.
81. Clydesdale, F. M. Color as a factor in food choice. Crit. Rev. Food Sci. Nutr. 1993, 33, 83-101.
82. Meléndez-Martínez, A. J.; Britton, G.; Vicario, I. M.; Heredia, F. J. Relationship between the colour and the chemical structure of carotenoid pigments. Food Chem. 2007, 101, 1145-1150.
83. Young, A. J.; Lowe, G. M. Antioxidant and prooxidant properties of carotenoids. Arch. Biochem. Biophys. 2001, 385, 20-27.
84. Palozza, P. Prooxidant actions of carotenoids in biologic systems. Nutr. Rev. 1998, 56, 257-265.
85. Barros, M. P.; Colepicolo, P.; Guaratini, T. Catalysis and Photochemistry in Heterogeneous Media; Nantes, I. L., Brochsztain, S., Eds.; Research Signpost: Kerala, India, 2007; pp. 161-186.
86. Barros, M. P.; Pinto, E.; Colepicolo, P.; Pedersén, M. Astaxanthin and peridinin inhibit oxidative damage in Fe2+-loaded liposomes: Scavenging oxyradicals or changing membrane permeability? Biochem. Biophys. Res. Commun. 2001, 288, 225-232.
87. Otton, R.; Marin, D. P.; Bolin, A. P.; Santos, R. C.; Polotow, T. G.; Sampaio, S. C.; Barros, M. P. Astaxanthin ameliorates the redox imbalance in lymphocytes of experimental diabetic rats. Chem. Biol. Interact. 2010, 186, 306-315.
88. Bolin, A. P.; Macedo, R. C.; Marin, D. P.; Barros, M. P.; Otton, R. Astaxanthin prevents in vitro auto-oxidative injury in human lymphocytes. Cell Biol. Toxicol. 2010, 26, 457-467.
89. Guerin, M.; Huntley, M. E.; Olaizola, M. Haematococcus astaxanthin: Applications for human health and nutrition. Trends Biotechnol. 2003, 21, 210-216.
90. Barros, M. P.; Poppe, S. C.; Souza-Junior, T. P. Putative benefits of microalgal astaxanthin on exercise and human health. Braz. J. Pharmacognos. 2011, 21, 283-289.
91. Ghosh, S.; Hayden, M. S. New regulators of NF-κB in inflammation. Nat. Rev. Immunol. 2008, 8, 837-848.
92. Karin, M. Nuclear factor-κB in cancer development and progression. Nature 2006, 441, 431-436.
93. O'Neill, L. A. J.; Kaltschmidt, C. NF-κB: A crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 1997, 20, 252-258.
94. Folmer, F.; Jaspars, M.; Solano, G.; Cristofanon, S.; Henry, E.; Tabudravu, J.; Black, K.; Green, D. H.; Küpper, F. C.; Aalbersberg, W.; et al. The inhibition of TNF-α-induced NF-κB activation by marine natural products. Biochem. Pharmacol. 2009, 78, 592-606.
95. 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.
96. Lee, S. J.; Bai, S. K.; Lee, K. S.; Namkoong, S.; Na, H. J.; Ha, K. S.; Han, J. A.; Yim, S. V.; Chang, K.; Kwon, Y. G.; et al. Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing I(kappa)B kinase-dependent NF-kappaB activation. Mol. Cells 2003, 16, 97-105.
97. Nagendraprabhu, P.; Sudhandiran, G. Astaxanthin inhibits tumor invasion by decreasing extracellular matrix production and induces apoptosis in experimental rat colon carcinogenesis by modulating the expressions of ERK-2, NFκB and COX-2. Investig. New Drugs 2011, 29, 207-224.
98. Chew, B. P.; Park, J. S. Carotenoid action on the immune response. J. Nutr. 2004, 134, 257S-261S.
99. Ohgami, K.; Shiratori, K.; Kotake, S.; Nishida, T.; Mizuki, N.; Yazawa, K.; Ohno, S. Effects of astaxanthin on lipopolysaccharide-induced inflammation in vitro and in vivo. Investig. Ophthalmol. Vis. Sci. 2003, 44, 2694-2701.
100. Chew, B. P.; Wong, M. W.; Park, J. S.; Wong, T. S. Dietary β-carotene and astaxanthin but not canthaxanthin stimulate splenocyte function in mice. Anticancer Res. 1999, 19, 5223-5227.
101. Jyonouchi, H.; Zhang, L.; Gross, M.; Tomita, Y. Immunomodulating actions of carotenoids: Enhancement of in vivo and in vitro antibody production to T-dependent antigens. Nutr. Cancer 1994, 21, 47-58.
102. 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.
103. Kurihara, H.; Koda, H.; Asami, S.; Kiso, Y.; Tanaka, T. Contribution of the antioxidative property of astaxanthin to its protective effect on the promotion of cancer metastasis in mice treated with restraint stress. Life Sci. 2002, 70, 2509-2520.
104. Marin, D. P.; Bolin, A. P.; Macedo, R. C.; Sampaio, S. C.; Otton, R. ROS production in neutrophils from alloxan-induced diabetic rats treated in vivo with astaxanthin. Int. Immunopharmacol. 2011, 11, 103-109.
105. Ye, Q.; Huang, B.; Zhang, X.; Zhu, Y.; Chen, X. Astaxanthin protects against MPP+-induced oxidative stress in PC12 cells via the HO-1/NOX2 axis. BMC Neurosci. 2012, 13, 156.
106. Santos, S. D.; Cahú, T. B.; Firmino, G. O.; de Castro, C. C.; Carvalho, L. B., Jr.; Bezerra, R. S.; Filho, J. L. Shrimp waste extract and astaxanthin: Rat alveolar macrophage, oxidative stress and inflammation. J. Food Sci. 2012, 77, H141-H146.
107. Souza-Junior, T. P.; Yamada, A. K.; Simão, R.; Polotow, T. G.; Curi, R.; Pope, Z.; Willardson, J. M.; Barros, M. P. Supra-physiological doses of testosterone affect membrane oxidation of human neutrophils monitored by the fluorescent probe C11-BODIPY581/591. Eur. J. Appl. Physiol. 2013, 113, 1241-1248.
108. Li, Z. R.; Dong, X.; Liu, H. L.; Chen, X.; Shi, H. Q.; Fan, Y. S.; Hou, D. S.; Zhang, X. M. 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, 1656-1666.
109. Kuroki, T.; Ikeda, S.; Okada, T.; Maoka, T.; Kitamura, A.; Sugimoto, M.; Kume, S. Astaxanthin ameliorates heat stress-induced impairment of blastocyst development in vitro: Astaxanthin colocalization with and action on mitochondria. J. Assist. Reprod. Genet. 2013, 30, 623-631.
110. 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.
111. Lee, D. H.; Kim, C. S.; Lee, Y. J. Astaxanthin protects against MPTP/MPP+-induced mitochondrial dysfunction and ROS production in vivo and in vitro. Food Chem. Toxicol. 2011, 49, 271-280.
112. Wolf, A. M.; Asoh, S.; Hiranuma, H.; Ohsawa, I.; Iio, K.; Satou, A.; Ishikura, M.; Ohta, S. Astaxanthin protects mitochondrial redox state and functional integrity against oxidative stress. J. Nutr. Biochem. 2010, 21, 381-389.
113. Song, X. D.; Zhang, J. J.; Wang, M. R.; Liu, W. B.; Gu, X. B.; Ly, C. J. Astaxanthin induces mitochondria-mediated apoptosis in rat hepatocellular carcinoma CBRH-7919 cells. Biol. Pharm. Bull. 2011, 34, 839-844.
114. Kavitha, K.; Kowshik, J.; Kishore, T. K.; Baba, A. B.; Nagini, S. Astaxanthin inhibits NF-κB and Wnt/β-catenin signaling pathways via inactivation of Erk/MAPK and PI3K/Akt to induce intrinsic apoptosis in a hamster model of oral cancer. Biochim. Biophys. Acta 2013, 1830, 4433-4444.
115. Dong, L. Y.; Jin, J.; Lu, G.; Kang, X. L. Astaxanthin attenuates the apoptosis of retinal ganglion cells in db/db mice by inhibition of oxidative stress. Mar. Drugs 2013, 11, 960-974.
116. Otton, R.; Marin, D. P.; Bolin, A. P.; Macedo, R. C. S.; Campoio, T. R.; Fineto, C., Jr.; Guerra, B. A.; Leite, J. R.; Barros, M. P.; Mattei, R. Combined fish oil and astaxanthin supplementation modulates rat lymphocyte function. Eur. J. Nutr. 2012, 51, 707-718.
117. Dhillon, V. S.; Fenech, M. Mutations that affect mitochondrial functions and their association with neurodegenerative diseases. Mutat. Res. 2014, 759, 1-13.
118. Mao, P.; Manczak, M.; Shirendeb, U. P.; Reddy, P. H. MitoQ, a mitochondria-targeted antioxidant, delays disease progression and alleviates pathogenesis in an experimental autoimmune encephalomyelitis mouse model of multiple sclerosis. Biochim. Biophys. Acta 2013, 1832, 2322-2331.
119. Liu, X.; Osawa, T. Astaxanthin protects neuronal cells against oxidative damage and is a potent candidate for brain food. Forum Nutr. 2009, 61, 129-135.
120. 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.
121. Lu, Y.-P.; Liu, S.-Y.; Sun, H.; Wu, X.-M.; Li, J.-J.; Zhu, L. Neuroprotective effect of astaxanthin on H2O2-induced neurotoxicity in vitro and on focal cerebral ischemia in vivo. Brain Res. 2010, 1360, 40-48.
122. Chan, K.-C.; Mong, M.-C.; Yin, A.-C. Antioxidative and anti-inflammatory, neuroprotective effects of astaxanthin and canthaxanthin in nerve growth factor differentiated PC12 cells. J. Food Sci. 2009, 74, H225-H231.
123. Stillwell, W.; Wassall, S. R. Docosahexaenoic acid: Membrane properties of a unique fatty acid. Chem. Phys. Lipids 2003, 126, 1-27.
124. Weintraub, H. Update on marine omega-3 fatty acids: Management of dyslipidemia and current omega-3 treatment options. Atherosclerosis 2013, 230, 381-389.
125. Freemantle, E.; Vandal, M.; Tremblay-Mercier, J.; Tremblay, S.; Blachère, J. C.; Bégin, M. E.; Brenna, J. T.; Windust, A.; Cunnane, S. C. Omega-3 fatty acids, energy substrates, and brain function during aging. Prostagl. Leukot. Essent. Fatty Acids 2006, 75, 213-220.
126. Yehuda, S.; Rabinovitz, S.; Mostofsky, D. I. Essential fatty acids and the brain: From infancy to aging. Neurobiol. Aging 2005, 26, 98-102.
127. Whelan, J.; Rust, C. Innovative dietary sources of n-3 fatty acids. Annu. Rev. Nutr. 2006, 26, 75-103.
128. Lukiw, W. J.; Bazan, N. G. Docosahexaenoic acid and the aging brain. J. Nutr. 2008, 138, 2510-2514.
129. Connor, W. E.; Neuringer, M.; Lin, D. S. Dietary effects on brain fatty acid composition: The reversibility of n-3 fatty acid deficiency and turnover of docosahexaenoic acid in the brain, erythrocytes, and plasma of rhesus monkeys. J. Lipid Res. 2009, 31, 237-247.
130. Hichami, A.; Datiche, F.; Ullah, S.; Liénard, F.; Chardigny, J. M.; Cattarelli, M.; Khan, N. A. Olfactory discrimination ability and brain expression of c-fos, Gir and Glut1 mRNA are altered in n-3 fatty acid-depleted rats. Behav. Brain Res. 2007, 184, 1-10.
131. Shirai, N.; Suzuki, H. Effect of dietary docosahexaenoic acid and catechins on maze behavior in mice. Ann. Nutr. Metab. 2004, 48, 51-58.
132. Uauy, R.; Dangour, A. D. Nutrition in brain development and aging: Role of essential fatty acids. Nutr. Rev. 2006, 64, S24-S33.
133. Giusto, N. M.; Salvador, G. A.; Castagnet, P. I.; Pasquaré, S. J.; Ilincheta de Boschero, M. G. Age-associated changes in central nervous system glycerolipid composition and metabolism. Neurochem. Res. 2002, 27, 1513-1523.
134. Hardy, J. A.; Higgins, G. A. Alzheimer's disease: The amyloid cascade hypothesis. Science 1992, 256, 184-185.
135. Moore, S. A.; Yoder, E.; Murphy, S.; Dutton, G. R.; Spector, A. A. Astrocytes, not neurons, produce docosahexaenoic acid (22: 6 omega-3) and arachidonic acid (20: 4 omega-6). J. Neurochem. 1991, 56, 518-524.
136. Hashimoto, M.; Tanabe, Y.; Fujii, Y.; Kikuta, T.; Shibata, H.; Shido, O. Chronic administration of docosahexaenoic acid ameliorates the impairment of spatial cognition learning ability in amyloid beta-infused rats. J. Nutr. 2005, 13, 549-555.
137. Hashimoto, M.; Hossain, S.; Shimada, T.; Shido, O. Docosahexaenoic acid-induced protective effect against impaired learning in amyloid beta-infused rats is associated with increased synaptosomal membrane fluidity. Clin. Exp. Pharmacol. Physiol. 2006, 33, 934-939.
138. Calon, F.; Lim, G. P.; Morihara, T.; Yang, F.; Ubeda, O.; Salem, N., Jr.; Frautschy, S. A.; Cole, G. M. Dietary n-3 polyunsaturated fatty acid depletion activates caspases and decreases NMDA receptors in the brain of a transgenic mouse model of Alzheimer's disease. Eur. J. Neurosci. 2005, 22, 617-626.
139. Lim, G. P.; Calon, F.; Morihara, T.; Yang, F.; Teter, B.; Ubeda, O.; Salem, N., Jr.; Frautschy, S. A.; Cole, G. M. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J. Neurosci. 2005, 25, 3032-3040.
140. Ma, Q. L.; Teter, B.; Ubeda, O. J.; Morihara, T.; Dhoot, D.; Nyby, M. D.; Tuck, M. L.; Frautschy, S. A.; Cole, G. M. Omega-3 fatty acid docosahexaenoic acid increases SorLA/LR11, a sorting protein with reduced expression in sporadic Alzheimer's disease (AD): Relevance to AD prevention. J. Neurosci. 2007, 27, 14299-14307.
141. Arendash, G. W.; Jensen, M. T.; Salem, N., Jr.; Hussein, N.; Cracchiolo, J.; Dickson, A.; Leighty, R.; Potter, H. A diet high in omega-3 fatty acids does not improve or protect cognitive performance in Alzheimer's transgenic mice. Neuroscience 2007, 149, 286-302.
142. Gillette-Guyonnet, S.; Abellan Van Kan, G.; Andrieu, S.; Barberger-Gateau, P.; Berr, C.; Bonnefoy, M.; Dartigues, J. F.; de Groot, L.; Ferry, M.; Galan, P.; et al. IANA task force on nutrition and cognitive decline with aging. J. Nutr. Health Aging 2007, 11, 132-152.
143. Barberger-Gateau, P.; Raffaitin, C.; Letenneur, L.; Berr, C.; Tzourio, C.; Dartigues, J. F.; Alpérovitch, A. Dietary patterns and risk of dementia: The Three-City cohort study. Neurology 2007, 69, 1921-1930.
144. Calon, F. Omega-3 polyunsaturated fatty acids in Alzheimer's disease: Key questions and partial answers. Curr. Alzheimer Res. 2011, 8, 470-478.
145. Calon, F.; Cole, G. Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegenerative diseases: Evidence from animal studies. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77, 287-293.
146. Bousquet, M.; Saint-Pierre, M.; Julien, C.; Salem, N., Jr.; Cicchetti, F.; Calon, F. Beneficial effects of dietary omega-3 polyunsaturated fatty acid on toxin-induced neuronal degeneration in an animal model of Parkinson's disease. FASEB J. 2008, 22, 1213-1325.
147. De Lau, L. M.; Schipper, C. M.; Hofman, A.; Koudstaal, P. J.; Breteler, M. M. Prognosis of Parkinson disease: Risk of dementia and mortality: The Rotterdam Study. Arch. Neurol. 2005, 62, 1265-1269.
148. Da Silva, T. M.; Munhoz, R. P.; Alvarez, C.; Naliwaiko, K.; Kiss, A.; Andreatini, R.; Ferraz, A. C. Depression in Parkinson's disease: A double-blind, randomized, placebo-controlled pilot study of omega-3 fatty-acid supplementation. J. Affect. Disord. 2008, 111, 351-359.
149. Gorjão, R.; Azevedo-Martins, A. K.; Rodrigues, H. G.; Abdulkader, F.; Arcisio-Miranda, M.; Procopio, J.; Curi, R. Comparative effects of DHA and EPA on cell function. Pharmacol. Ther. 2009, 122, 56-64.
150. 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. 2011, 105, 220-227.
151. Cunnane, S. C.; Plourde, M.; Pifferi, F.; Bégin, M.; Féart, C.; Barberger-Gateau, P. Fish, docosahexaenoic acid and Alzheimer's disease. Prog. Lipid Res. 2009, 48, 239-256.
152. Appleton, K. M.; Gunnell, D.; Peters, T. J.; Ness, A. R.; Kessler, D.; Rogers, P. J. No clear evidence of an association between plasma concentrations of n-3 long-chain polyunsaturated fatty acids and depressed mood in a non-clinical population. Prostaglandins Leukot. Essent. Fatty Acids 2008, 78, 337-342.
153. Bas, O.; Songur, A.; Sahin, O.; Mollaoglu, H.; Ozen, O. A.; Yaman, M.; Eser, O.; Fidan, H.; Yagmurca, M. The protective effect of fish n-3 fatty acids on cerebral ischemia in rat hippocampus. Neurochem. Int. 2007, 50, 548-554.
154. King, V. R.; Huang, W. L.; Dyall, S. C.; Curran, O. E.; Priestley, J. V.; Michael-Titus, A. T. Omega-3 fatty acids improve recovery, whereas omega-6 fatty acids worsen outcome, after spinal cord injury in the adult rat. J. Neurosci. 2006, 26, 4672-4680.
155. Calabrese, V.; Cornelius, C.; Dinkova-Kostova, A. T.; Calabrese, E. J.; Mattson, M. P. Cellular stress responses, the hormesis paradigm, and vitagenes: Novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid. Redox Signal. 2010, 13, 1763-1811.
156. Jicha, G. A.; Markesbery, W. R. Omega-3 fatty acids: Potential role in the management of early Alzheimer's disease. Clin. Interv. Aging 2010, 5, 45-61.
157. Tarling, G. A. Population dynamics of Northern krill (Meganyctiphanes norvegica Sars). Adv. Mar. Biol. 2010, 57, 59-90.
158. Tou, J. C.; Jaczynski, J.; Chen, Y. Krill for human consumption: Nutritional value and potential health benefits. Nutr. Rev. 2007, 65, 63-77.
159. Ulven, S. M.; Kirkhus, B.; Lamglait, A.; Basu, S.; Elind, E.; Haider, T.; Berge, K.; Vik, H.; Pedersen, J. I. Metabolic effects of krill oil are essentially similar to those of fish oil but at lower dose of EPA and DHA, in healthy volunteers. Lipids 2011, 46, 37-46.
160. Grantham, G. J. The Southern Ocean: The Utilization of Krill; Southern Ocean Fisheries Survey Programme, GLO/SO/7/3; Food and Agriculture Organization: Rome, Italy, 1977; pp. 1-61.
161. Grynbaum, M. D.; Hentschel, P.; Putzbach, K.; Rehbein, J.; Krucker, M.; Nicholson, G.; Albert, K. Unambiguous detection of astaxanthin and astaxanthin fatty acid esters in krill (Euphausia superba Dana). J. Sep. Sci. 2005, 28, 1685-1693.
162. Miyashita, K. Function of marine carotenoids. Forum Nutr. 2009, 61, 136-146.
163. Gigliotti, J. C.; Davenport, M. P.; Beamer, S. K.; Tou, J. C.; Jaczynski, J. Extraction and characterisation of lipids from Antarctic krill (Euphausia superba). Food Chem. 2011, 125, 1028-1036.
164. Suzuki, T.; Shibata, N. The utilization of Antarctic krill for human food. Food Rev. Int. 1990, 6, 119-147.
165. Maki, K. C.; Reeves, M. S.; Farmer, M.; Griinari, M.; Berge, K.; Vik, H.; Hubacher, R.; Rains, T. M. Krill oil supplementation increases plasma concentrations of eicosapentaenoic and docosahexaenoic acids in overweight and obese men and women. Nutr. Res. 2009, 29, 609-615.
166. Mancuso, J. R.; McClements, D. J.; Decker, E. A. The effects of surfactant type, pH, and chelators on the oxidation of salmon oil-in-water emulsions. J. Agric. Food Chem. 1999, 47, 4112-4116.
167. Tou, J. C.; Altman, S. N.; Gigliotti, J. C.; Benedito, V. A.; Cordonier, E. L. Different sources of omega-3 polyunsaturated fatty acids affects apparent digestibility, tissue deposition, and tissue oxidative stability in growing female rats. Lipids Health Dis. 2011, 10, 179.
168. Venkatraman, J. T.; Chandrasekar, B.; Kim, J. D.; Fernandes, G. Effects of n-3 and n-6 fatty acids on the activities and expression of hepatic antioxidant enzymes in autoimmune-prone NZB × NZW F1 mice. Lipids 1994, 29, 561-568.
169. Di Marzo, V.; Griinari, M.; Carta, G.; Murru, E.; Ligresti, A.; Cordeddu, L.; Giordano, E.; Bisogno, T.; Collu, M.; Batetta, B.; et al. Dietary krill oil increases docosahexaenoic acid and reduces 2-arachidonoylglycerol but not N-acylethanolamine levels in the brain of obese Zucker rats. Int. Dairy J. 2010, 20, 231-235.
170. Tillander, V.; Burri, L.; Alexson, S. Fish oil and Krill oil differentially regulate gene expression. Chem. Phys. Lipids 2010, 163S, S22-S33.
171. Vigerust, N. F.; Bjørndal, B.; Bohov, P.; Brattelid, T.; Svardal, A.; Berge, R. K. Krill oil versus fish oil in modulation of inflammation and lipid metabolism in mice transgenic for TNF-α. Eur. J. Nutr. 2013, 52, 1315-1325.
172. Deutsch, L. Evaluation of the effect of neptune krill oil on chronic inflammation and arthritic symptoms. J. Am. Coll. Nutr. 2007, 26, 39-48.
173. Wibrand, K.; Berge, K.; Messaoudi, M.; Duffaud, A.; Panja, D.; Bramham, C. R.; Burri, L. Enhanced cognitive function and antidepressant-like effects after krill oil supplementation in rats. Lipids Health Dis. 2013, 12, 6.
174. Lee, B.; Sur, B.-J.; Han, J.-J.; Shim, I.; Her, S.; Lee, H.-J.; Hahm, D.-H. Krill phosphatidylserine improves learning and memory in Morris water maze in aged rats. Progr. Neuro-Psychopharmacol. Biol. Psych. 2010, 34, 1085-1093.