Docosahexaenoic acid: Brain accretion and roles in neuroprotection after brain hypoxia and ischemia

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 14, Issue 2, 2011, Pages 158-167

  Mayurasakorn, Korapat ^a   Williams, Jill J ^a   Ten, Vadim S ^a   Deckelbaum, Richard J ^a  

^a Columbia University ^*  (United States)

Author keywords

docosahexaenoic acid; hypoxic ischemic brain; neuroprotection; omega 3; polyunsaturated fatty acid

Indexed keywords

ARACHIDONIC ACID; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACID; FREE RADICAL; GLUTAMATE RECEPTOR; GLUTAMIC ACID; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INHIBITOR OF APOPTOSIS PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; LINOLEIC ACID; LYSOPHOSPHATIDYLCHOLINE; MALONALDEHYDE; OMEGA 3 FATTY ACID; PHOSPHOLIPID; PROSTAGLANDIN; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN LEVEL; BRAIN MITOCHONDRION; BRAIN NECROSIS; CELL PROTECTION; CEREBROVASCULAR DISEASE; CHRONIC DRUG ADMINISTRATION; DIETARY INTAKE; DOWN REGULATION; DRUG EFFECT; ENCEPHALITIS; GENE EXPRESSION REGULATION; HUMAN; MOLECULAR BIOLOGY; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PROTEIN EXPRESSION; STROKE; STROKE PATIENT; SYNAPTIC TRANSMISSION; UPREGULATION;

BRAIN; DOCOSAHEXAENOIC ACIDS; FATTY ACIDS, OMEGA-3; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; NEUROPROTECTIVE AGENTS; REPERFUSION INJURY;

ANIMALIA; MAMMALIA;

EID: 79952039402     PISSN: 13631950     EISSN: 14736519     Source Type: Journal    
DOI: 10.1097/MCO.0b013e328342cba5     Document Type: Article

References (93)

1. Adams HP Jr, del Zoppo G, Alberts MJ, et al. Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups. Circulation 2007;115:e478-e534.
2. Wei JW, Wang JG, Huang Y, et al. Secondary prevention of ischemic stroke in urban China. Stroke 2010;41:967-974.
3. Yusuf S, Hawken S, Ounpuu S, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004;364:937-952. (Pubitemid 39208455)
4. He K, Song Y, Daviglus ML, et al. Fish consumption and incidence of stroke: a meta-analysis of cohort studies. Stroke 2004;35:1538-1542. (Pubitemid 38823619)
5. Mozaffarian D, Longstreth WT Jr, Lemaitre RN, et al. Fish consumption and stroke risk in elderly individuals: the cardiovascular health study. Arch Intern Med 2005;165:200-206.
6. Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA 2006;296:1885-1899. (Pubitemid 44596197)
7. Yamagishi K, Iso H, Date C, et al. Fish, omega-3 polyunsaturated fatty acids, and mortality from cardiovascular diseases in a nationwide community-based cohort of Japanese men and women the JACC (Japan Collaborative Cohort Study for Evaluation of Cancer Risk) Study. J Am Coll Cardiol 2008;52:988-996.
8. He K, Rimm EB, Merchant A, et al. Fish consumption and risk of stroke in men. JAMA 2002;288:3130-3136. (Pubitemid 36014130)
9. Johnson EJ, Schaefer EJ. Potential role of dietary n-3 fatty acids in the prevention of dementia and macular degeneration. Am J Clin Nutr 2006;83:1494S-1498S. (Pubitemid 44713090)
10. Innis SM. The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev Neurosci 2000;22:474-480.
11. Youdim KA, Martin A, Joseph JA. Essential fatty acids and the brain: possible health implications. Int J Dev Neurosci 2000;18:383-399. (Pubitemid 30244351)
12. Salem N Jr, Litman B, Kim HY, et al. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 2001;36:945-959. (Pubitemid 33065196)
13. Robinson JG, Stone NJ. Antiatherosclerotic and antithrombotic effects of omega-3 fatty acids. Am J Cardiol 2006;98:39i-49i.
14. Jung UJ, Torrejon C, Tighe AP, et al. n-3 Fatty acids and cardiovascular disease: mechanisms underlying beneficial effects. Am J Clin Nutr 2008;87:2003S-2009S. (Pubitemid 351872682)
15. Zuliani G, Galvani M, Leitersdorf E, et al. The role of polyunsaturated fatty acids (PUFA) in the treatment of dyslipidemias. Curr Pharm Des 2009;15:4087-4093.
16. Manerba A, Vizzardi E, Metra M, et al. n-3 PUFAs and cardiovascular disease prevention. Future Cardiol 2010;6:343-350.
17. Bazan NG. Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol 2005;15:159-166. (Pubitemid 40546172)
18. Sauvaget C, Nagano J, Allen N, et al. Intake of animal products and stroke mortality in the Hiroshima/Nagasaki Life Span Study. Int J Epidemiol 2003;32:536-543. (Pubitemid 37039005)
19. Bouzan C, Cohen JT, Connor WE, et al. A quantitative analysis of fish consumption and stroke risk. Am J Prev Med 2005;29:347-352. (Pubitemid 41483544)
20. Tanaka K, Ishikawa Y, Yokoyama M, et al. Reduction in the recurrence of stroke by eicosapentaenoic acid for hypercholesterolemic patients: subanalysis of the JELIS trial. Stroke 2008;39:2052-2058.
21. Nakamura Y, Ueshima H, Okamura T, et al. Association between fish consumption and all-cause and cause-specific mortality in Japan: NIPPON DATA80, 1980-99. Am J Med 2005;118:239-245. (Pubitemid 40312634)
22. Wennberg M, Bergdahl IA, Stegmayr B, et al. Fish intake, mercury, long-chain n-3 polyunsaturated fatty acids and risk of stroke in northern Sweden. Br J Nutr 2007;98:1038-1045. (Pubitemid 47543464)
23. Haag M. Essential fatty acids and the brain. Can J Psychiatry 2003;48:195-203. (Pubitemid 36603376)
24. Giusto NM, Salvador GA, Castagnet PI, et al. Age-associated changes in central nervous system glycerolipid composition and metabolism. Neurochem Res 2002;27:1513-1523. (Pubitemid 36014163)
25. Innis SM. Dietary omega 3 fatty acids and the developing brain. Brain Res 2008;1237:35-43.
26. Wassall SR, Brzustowicz MR, Shaikh SR, et al. Order from disorder, corralling cholesterol with chaotic lipids. The role of polyunsaturated lipids in membrane raft formation. Chem Phys Lipids 2004;132:79-88. (Pubitemid 39458322)
27. Martinez M. Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr 1992;120:S129-S138.
28. Kitajka K, Sinclair AJ, Weisinger RS, et al. Effects of dietary omega-3 polyunsaturated fatty acids on brain gene expression. Proc Natl Acad Sci USA 2004;101:10931-10936. (Pubitemid 38989562)
29. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot Essent Fatty Acids 2006;75:259-269. (Pubitemid 44442912)
30. Coti Bertrand P, O'Kusky JR, Innis SM. Maternal dietary (n-3) fatty acid deficiency alters neurogenesis in the embryonic rat brain. J Nutr 2006;136:1570-1575. (Pubitemid 43765364)
31. Heinrichs SC. Dietary omega-3 fatty acid supplementation for optimizing neuronal structure and function. Mol Nutr Food Res 2010;54:447-456.
32. Bazan NG. Neuroprotectin D1-mediated anti-inflammatory and survival signaling in stroke, retinal degenerations, and Alzheimer's disease. J Lipid Res 2009;50 (Suppl):S400-S405.
33. Rapoport SI, Rao JS, Igarashi M. Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver. Prostaglandins Leukot Essent Fatty Acids 2007;77:251-261. (Pubitemid 350214520)
34. Rapoport SI, Igarashi M. Can the rat liver maintain normal brain DHA metabolism in the absence of dietary DHA? Prostaglandins Leukot Essent Fatty Acids 2009;81:119-123.
35. De Groot RH, Hornstra G, van Houwelingen AC, et al. Effect of alpha-linolenic acid supplementation during pregnancy on maternal and neonatal polyunsaturated fatty acid status and pregnancy outcome. Am J Clin Nutr 2004;79:251-260. (Pubitemid 41095978)
36. Innis SM. Essential fatty acid transfer and fetal development. Placenta 2005;.26. (Suppl A):S70-S75.
37. Liou YA, King DJ, Zibrik D, et al. Decreasing linoleic acid with constant alphalinolenic acid in dietary fats increases (n-3) eicosapentaenoic acid in plasma phospholipids in healthy men. J Nutr 2007;137:945-952. (Pubitemid 46596892)
38. Rao JS, Ertley RN, DeMar JC Jr, et al. Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex. Mol Psychiatry 2007;12:151-157. (Pubitemid 46160980)
39. Cao D, Yang B, Hou L, et al. Chronic daily administration of ethyl docosahexaenoate protects against gerbil brain ischemic damage through reduction of arachidonic acid liberation and accumulation. J Nutr Biochem 2007;18:297-304. (Pubitemid 46590711)
40. Goyens PL, Spilker ME, Zock PL, et al. Compartmental modeling to quantify alpha-linolenic acid conversion after longer term intake of multiple tracer boluses. J Lipid Res 2005;46:1474-1483. (Pubitemid 43109812)
41. Williams CM, Burdge G. Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc 2006;65:42-50. (Pubitemid 43259983)
42. Carnielli VP, Simonato M, Verlato G, et al. Synthesis of long-chain polyunsaturated fatty acids in preterm newborns fed formula with long-chain polyunsaturated fatty acids. Am J Clin Nutr 2007;86:1323-1330. (Pubitemid 350126234)
43. Rosell MS, Lloyd-Wright Z, Appleby PN, et al. Long-chain n-3 polyunsaturated fatty acids in plasma in British meat-eating, vegetarian, and vegan men. Am J Clin Nutr 2005;82:327-334.
44. Nakamura MT, Nara TY. Essential fatty acid synthesis and its regulation in mammals. Prostaglandins Leukot Essent Fatty Acids 2003;68:145-150. (Pubitemid 36216478)
45. Jump DB, Botolin D, Wang Y, et al. Fatty acid regulation of hepatic gene transcription. J Nutr 2005;135:2503-2506. (Pubitemid 43156586)
46. Igarashi M, Ma K, Chang L, et al. Dietary n-3 PUFA deprivation for 15 weeks upregulates elongase and desaturase expression in rat liver but not brain. J Lipid Res 2007;48:2463-2470. (Pubitemid 350058757)
47. Strokin M, Sergeeva M, Reiser G. Docosahexaenoic acid and arachidonic acid release in rat brain astrocytes is mediated by two separate isoforms of phospholipase A2 and is differently regulated by cyclic AMP and Ca2\+. Br J Pharmacol 2003;139:1014-1022. (Pubitemid 36877400)
48. DeMar JC Jr, Ma K, Bell JM, et al. Half-lives of docosahexaenoic acid in rat brain phospholipids are prolonged by 15 weeks of nutritional deprivation of n-3 polyunsaturated fatty acids. J Neurochem 2004;91:1125-1137. (Pubitemid 39587451)
49. Bosetti F, Weerasinghe GR. The expression of brain cyclooxygenase-2 is down-regulated in the cytosolic phospholipase A2 knockout mouse. J Neurochem 2003;87:1471-1477. (Pubitemid 38020580)
50. Matsuzaka T, Shimano H, Yahagi N, et al. Dual regulation of mouse Delta(5)- and Delta(6)-desaturase gene expression by SREBP-1 and PPARalpha. J Lipid Res 2002;43:107-114. (Pubitemid 34117224)
51. Perlman J. Pathogenesis of hypoxic-ischemic brain injury. J Perinatol 2007;27:S39-S46. (Pubitemid 46647890)
52. Sims NR, Muyderman H. Mitochondria, oxidative metabolism and cell death in stroke. Biochim Biophys Acta 2010;1802:80-91.
53. Northington FJ, Ferriero DM, Graham EM, et al. Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis 2001;8:207-219. (Pubitemid 32382476)
54. Picq M, Chen P, Perz M, et al. DHA metabolism: targeting the brain and lipoxygenation. Mol Neurobiol 2010;42:48-51.
55. Bazan NG. Synaptic lipid signaling: significance of polyunsaturated fatty acids and platelet-activating factor. J Lipid Res 2003;44:2221-2233. (Pubitemid 38082480)
56. Bazan NG. Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci 2006;29:263-271.
57. Cao DH, Xu JF, Xue RH, et al. Protective effect of chronic ethyl docosahexaenoate administration on brain injury in ischemic gerbils. Pharmacol Biochem Behav 2004;79:651-659.
58. Cao D, Zhou C, Sun L, et al. Chronic administration of ethyl docosahexaenoate reduces gerbil brain eicosanoid productions following ischemia and reperfusion. J Nutr Biochem 2006;17:234-241.
59. Cao D, Kevala K, Kim J, et al. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem 2009;111:510-521.
60. Rapoport SI. In vivo approaches and rationale for quantifying kinetics and imaging brain lipid metabolic pathways. Prostaglandins Other Lipid Mediat 2005;77:185-196. (Pubitemid 41133427)
61. Belayev L, Marcheselli VL, Khoutorova L, et al. Docosahexaenoic acid complexed to albumin elicits high-grade ischemic neuroprotection. Stroke 2005;36:118-123. (Pubitemid 40054186)
62. Belayev L, Khoutorova L, Atkins KD, et al. Robust docosahexaenoic acidmediated neuroprotection in a rat model of transient, focal cerebral ischemia. Stroke 2009;40:3121-3126.
63. Pan HC, Kao TK, Ou YC, et al. Protective effect of docosahexaenoic acid against brain injury in ischemic rats. J Nutr Biochem 2009;20:715-725.
64. Innis SM. Perinatal biochemistry and physiology of long-chain polyunsaturated fatty acids. J Pediatr 2003;143:S1-S8. (Pubitemid 37346688)
65. Sun GY, Xu J, Jensen MD, et al. Phospholipase A2 in the central nervous system: implications for neurodegenerative diseases. J Lipid Res 2004;45:205-213. (Pubitemid 38228817)
66. Marcheselli VL, Hong S, Lukiw WJ, et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem 2003;278:43807-43817. (Pubitemid 37346009)
67. Lukiw WJ, Cui JG, Marcheselli VL, et al. A role for docosahexaenoic acidderived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest 2005;115:2774-2783. (Pubitemid 41434404)
68. Gonzalez-Periz A, Planaguma A, Gronert K, et al. Docosahexaenoic acid (DHA) blunts liver injury by conversion to protective lipid mediators: protectin D1 and 17S-hydroxy-DHA. FASEB J 2006;20:2537-2539.
69. Mukherjee PK, Marcheselli VL, Serhan CN, et al. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc Natl Acad Sci USA 2004;101:8491-8496. (Pubitemid 38736602)
70. Moreira JD, Knorr L, Thomazi AP, et al. Dietary omega-3 fatty acids attenuate cellular damage after a hippocampal ischemic insult in adult rats. J Nutr Biochem 2010;21:351-356.
71. Lukiw WJ, Bazan NG. Docosahexaenoic acid and the aging brain. J Nutr 2008;138:2510-2514.
72. Lukiw WJ, Bazan NG. Inflammatory, apoptotic, and survival gene signaling in Alzheimer's disease: a review on the bioactivity of Neuroprotectin D1 and apoptosis. Mol Neurobiol 2010;42:10-16.
73. Choi-Kwon S, Park KA, Lee HJ, et al. Temporal changes in cerebral antioxidant enzyme activities after ischemia and reperfusion in a rat focal brain ischemia model: effect of dietary fish oil. Brain Res Dev Brain Res 2004;152:11-18. (Pubitemid 38993283)
74. Bas O, Songur A, Sahin O, et al. The protective effect of fish n-3 fatty acids on cerebral ischemia in rat hippocampus. Neurochem Int 2007;50:548-554. (Pubitemid 46186606)
75. Mrsic-Pelcic J, Zupan G, Maysinger D, et al. The influence of MK-801 on the hippocampal free arachidonic acid level and Na\+-K\+-ATPase activity in global cerebral ischemia-exposed rats. Prog Neuropsychopharmacol Biol Psychiatry 2002;26:1319-1326. (Pubitemid 35345159)
76. King VR, Huang WL, Dyall SC, et al. 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. (Pubitemid 44315368)
77. Pilitsis JG, Diaz FG, O'Regan MH, et al. Differential effects of phospholipase inhibitors on free fatty acid efflux in rat cerebral cortex during ischemia- reperfusion injury. Brain Res 2002;951:96-106. (Pubitemid 35253902)
78. Callaway JK. Investigation of AM-36: a novel neuroprotective agent. Clin Exp Pharmacol Physiol 2001;28:913-918. (Pubitemid 33071066)
79. Maragakis NJ, Rothstein JD. Glutamate transporters: animal models to neurologic disease. Neurobiol Dis 2004;15:461-473. (Pubitemid 38429961)
80. Sheldon AL, Robinson MB. The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 2007;51:333-355. (Pubitemid 47503456)
81. Johnston MV, Trescher WH, Ishida A, et al. Neurobiology of hypoxic- ischemic injury in the developing brain. Pediatr Res 2001;49:735-741. (Pubitemid 32522044)
82. Umemura A, Mabe H, Nagai H, et al. Action of phospholipases A2 and C on free fatty acid release during complete ischemia in rat neocortex. Effect of phospholipase C inhibitor and N-methyl-D-aspartate antagonist. J Neurosurg 1992;76:648-651.
83. Mehta SL, Manhas N, Raghubir R. Molecular targets in cerebral ischemia for developing novel therapeutics. Brain Res Rev 2007;54:34-66. (Pubitemid 46498164)
84. Besancon E, Guo S, Lok J, et al. Beyond NMDA and AMPA glutamate receptors: emerging mechanisms for ionic imbalance and cell death in stroke. Trends Pharmacol Sci 2008;29:268-275.
85. Starkov AA, Chinopoulos C, Fiskum G. Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 2004;36:257-264. (Pubitemid 38992351)
86. Blomgren K, Hagberg H. Free radicals, mitochondria, and hypoxia-ischemia in the developing brain. Free Radic Biol Med 2006;40:388-397. (Pubitemid 43139674)
87. Robertson CL, Scafidi S, McKenna MC, et al. Mitochondrial mechanisms of cell death and neuroprotection in pediatric ischemic and traumatic brain injury. Exp Neurol 2009;218:371-380.
88. Castino R, Bellio N, Nicotra G, et al. Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells. Free Radic Biol Med 2007;42:1305-1316. (Pubitemid 46467267)
89. Galluzzi L, Morselli E, Kepp O, et al. Targeting postmitochondrial effectors of apoptosis for neuroprotection. Biochim Biophys Acta 2009;1787:402-413.
90. Zhu C, Qiu L, Wang X, et al. Involvement of apoptosis-inducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain. J Neurochem 2003;86:306-317. (Pubitemid 36842430)
91. Ying W, Wei G, Wang D, et al. Intranasal administration with NAD\+ profoundly decreases brain injury in a rat model of transient focal ischemia. Front Biosci 2007;12:2728-2734.
92. Wall R, Ross RP, Fitzgerald GF, et al. Fatty acids from fish: the antiinflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 2010;68:280-289.
93. Zhang W, Hu X, Yang W, et al. Omega-3 polyunsaturated fatty acid supplementation confers long-term neuroprotection against neonatal hypoxic-ischemic brain injury through anti-inflammatory actions. Stroke 2010;41:2341-2347.