The Journal of Nutritional Biochemistry
Volume 21, Issue 5 , Pages 364-373 , May 2010

Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance

  • Hui-Min Su

      Affiliations

    • Corresponding Author InformationTel.: +886 2 2312 3456x88248; fax: +886 2 2396 4350.

Received 19 May 2009 ,Revised 29 October 2009 ,Accepted 9 November 2009.

References 

  1. Fedorova I, Salem N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot Essent Fatty Acids. 2006;754-5:271–289
  2. Sastry PS. Lipids of nervous tissue: composition and metabolism. Prog Lipid Res. 1985;242:69–176
  3. Rapoport SI. In vivo fatty acid incorporation into brain phosholipids in relation to plasma availability, signal transduction and membrane remodeling. J Mol Neurosci. 2001;162-3:243–261[discussion 79-84]
  4. Aid S, Vancassel S, Poumes-Ballihaut C, Chalon S, Guesnet P, Lavialle M. Effect of a diet-induced n-3 PUFA depletion on cholinergic parameters in the rat hippocampus. J Lipid Res. 2003;448:1545–1551
  5. Ahmad A, Murthy M, Greiner RS, Moriguchi T, Salem N. A decrease in cell size accompanies a loss of docosahexaenoate in the rat hippocampus. Nutr Neurosci. 2002;52:103–113
  6. Puskas LG, Kitajka K, Nyakas C, Barcelo-Coblijn G, Farkas T. Short-term administration of omega 3 fatty acids from fish oil results in increased transthyretin transcription in old rat hippocampus. Proc Natl Acad Sci U S A. 2003;1004:1580–1585
  7. Novak EM, Dyer RA, Innis SM. High dietary omega-6 fatty acids contribute to reduced docosahexaenoic acid in the developing brain and inhibit secondary neurite growth. Brain Res. 2008;1237:136–145
  8. Wurtman RJ, Ulus IH, Cansev M, Watkins CJ, Wang L, Marzloff G. Synaptic proteins and phospholipids are increased in gerbil brain by administering uridine plus docosahexaenoic acid orally. Brain Res. 2006;10881:83–92
  9. Dobbing J, Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev. 1979;31:79–83
  10. Green P, Glozman S, Kamensky B, Yavin E. Developmental changes in rat brain membrane lipids and fatty acids. The preferential prenatal accumulation of docosahexaenoic acid. J Lipid Res. 1999;405:960–966
  11. Martinez M. Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr. 1992;1204(Pt 2):S129–S138
  12. Favreliere S, Stadelmann-Ingrand S, Huguet F, De Javel D, Piriou A, Tallineau C, et al. Age-related changes in ethanolamine glycerophospholipid fatty acid levels in rat frontal cortex and hippocampus. Neurobiol Aging. 2000;215:653–660
  13. Delion S, Chalon S, Guilloteau D, Lejeune B, Besnard JC, Durand G. Age-related changes in phospholipid fatty acid composition and monoaminergic neurotransmission in the hippocampus of rats fed a balanced or an n-3 polyunsaturated fatty acid-deficient diet. J Lipid Res. 1997;384:680–689
  14. Soderberg M, Edlund C, Kristensson K, Dallner G. Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids. 1991;266:421–425
  15. Prasad MR, Lovell MA, Yatin M, Dhillon H, Markesbery WR. Regional membrane phospholipid alterations in Alzheimer's disease. Neurochem Res. 1998;231:81–88
  16. Lukiw WJ, Cui JG, Marcheselli VL, Bodker M, Botkjaer A, Gotlinger K, et al. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest. 2005;11510:2774–2783
  17. Moser MB, Moser EI. Functional differentiation in the hippocampus. Hippocampus. 1998;86:608–619
  18. de Hoz L, Knox J, Morris RG. Longitudinal axis of the hippocampus: both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol. Hippocampus. 2003;135:587–603
  19. Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;2975868:681–683
  20. Chung WL, Chen JJ, Su HM. Fish oil supplementation of control and (n-3) fatty acid-deficient male rats enhances reference and working memory performance and increases brain regional docosahexaenoic acid levels. J Nutr. 2008;1386:1165–1171
  21. Tully AM, Roche HM, Doyle R, Fallon C, Bruce I, Lawlor B, et al. Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer's disease: a case-control study. Br J Nutr. 2003;894:483–489
  22. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;111:47–60
  23. Whelan J, Rust C. Innovative dietary sources of n-3 fatty acids. Annu Rev Nutr. 2006;26:75–103
  24. Su HM, Moser AB, Moser HW, Watkins PA. Peroxisomal straight-chain Acyl-CoA oxidase and d-bifunctional protein are essential for the retroconversion step in docosahexaenoic acid synthesis. J Biol Chem. 2001;27641:38115–38120
  25. Scott BL, Bazan NG. Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proc Natl Acad Sci U S Am. 1989;868:2903–2907
  26. Su HM, Huang MC, Saad NM, Nathanielsz PW, Brenna JT. Fetal baboons convert 18:3n-3 to 22:6n-3 in vivo. A stable isotope tracer study. J Lipid Res. 2001;424:581–586
  27. Green P, Yavin E. Elongation, desaturation, and esterification of essential fatty acids by fetal rat brain in vivo. J Lipid Res. 1993;3412:2099–2107
  28. Cook HW. In vitro formation of polyunsaturated fatty acids by desaturation in rat brain: some properties of the enzymes in developing brain and comparisons with liver. J Neurochem. 1978;306:1327–1334
  29. Bourre JM, Piciotti M, Dumont O. Delta 6 desaturase in brain and liver during development and aging. Lipids. 1990;256:354–356
  30. Su HM, Bernardo L, Mirmiran M, Ma XH, Corso TN, Nathanielsz PW, et al. Bioequivalence of dietary alpha-linolenic and docosahexaenoic acids as sources of docosahexaenoate accretion in brain and associated organs of neonatal baboons. Pediatr Res. 1999;451:87–93
  31. Bowen RA, Wierzbicki AA, Clandinin MT. Does increasing dietary linolenic acid content increase the docosahexaenoic acid content of phospholipids in neuronal cells of neonatal rats?. Pediatr Res. 1999;456:815–819
  32. Bourre JM, Francois M, Youyou A, Dumont O, Piciotti M, Pascal G, et al. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J Nutr. 1989;11912:1880–1892
  33. Salem N, Wegher B, Mena P, Uauy R. Arachidonic and docosahexaenoic acids are biosynthesized from their 18-carbon precursors in human infants. Proc Natl Acad Sci U S Am. 1996;931:49–54
  34. Umhau JC, Zhou W, Carson RE, Rapoport SI, Polozova A, Demar J, et al. Imaging incorporation of circulating docosahexaenoic acid into the human brain using positron emission tomography. J Lipid Res. 2009;507:1259–1268
  35. Williams CM, Burdge G. Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc. 2006;651:42–50
  36. Francois CA, Connor SL, Bolewicz LC, Connor WE. Supplementing lactating women with flaxseed oil does not increase docosahexaenoic acid in their milk. Am J Clin Nutr. 2003;771:226–233
  37. Brenna JT, Salem N, Sinclair AJ, Cunnane SC. alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fatty Acids. 2009;802-3:85–91
  38. Shindou H, Shimizu T. Acyl-CoA:lysophospholipid acyltransferases. J Biol Chem. 2009;2841:1–5
  39. Vergnes L, Beigneux AP, Davis R, Watkins SM, Young SG, Reue K. Agpat6 deficiency causes subdermal lipodystrophy and resistance to obesity. J Lipid Res. 2006;474:745–754
  40. Cao J, Shan D, Revett T, Li D, Wu L, Liu W, et al. Molecular identification of a novel mammalian brain isoform of acyl-CoA:lysophospholipid acyltransferase with prominent ethanolamine lysophospholipid acylating activity, LPEAT2. J Biol Chem. 2008;28327:19049–19057
  41. Ginsberg L, Rafique S, Xuereb JH, Rapoport SI, Gershfeld NL. Disease and anatomic specificity of ethanolamine plasmalogen deficiency in Alzheimer's disease brain. Brain Res. 1995;6981-2:223–226
  42. Guan Z, Wang Y, Cairns NJ, Lantos PL, Dallner G, Sindelar PJ. Decrease and structural modifications of phosphatidylethanolamine plasmalogen in the brain with Alzheimer disease. J Neuropathol Exp Neurol. 1999;587:740–747
  43. Farooqui AA, Rapoport SI, Horrocks LA. Membrane phospholipid alterations in Alzheimer's disease: deficiency of ethanolamine plasmalogens. Neurochem Res. 1997;224:523–527
  44. Kaduce TL, Chen Y, Hell JW, Spector AA. Docosahexaenoic acid synthesis from n-3 fatty acid precursors in rat hippocampal neurons. J Neurochem. 2008;
  45. Marszalek JR, Kitidis C, Dararutana A, Lodish HF. Acyl-CoA synthetase 2 overexpression enhances fatty acid internalization and neurite outgrowth. J Biol Chem. 2004;27923:23882–23891
  46. Marszalek JR, Kitidis C, Dirusso CC, Lodish HF. Long-chain acyl-CoA synthetase 6 preferentially promotes DHA metabolism. J Biol Chem. 2005;28011:10817–10826
  47. Wu H, Ichikawa S, Tani C, Zhu B, Tada M, Shimoishi Y, et al. Docosahexaenoic acid induces ERK1/2 activation and neuritogenesis via intracellular reactive oxygen species production in human neuroblastoma SH-SY5Y cells. Biochim Biophys Acta. 2009;17911:8–16
  48. Calderon F, Kim HY. Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J Neurochem. 2004;904:979–988
  49. Cao D, Kevala K, Kim J, Moon HS, Jun SB, Lovinger D, et al. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem. 2009;1112:510–521
  50. Cao D, Xue R, Xu J, Liu Z. Effects of docosahexaenoic acid on the survival and neurite outgrowth of rat cortical neurons in primary cultures. J Nutr Biochem. 2005;169:538–546
  51. Kan I, Melamed E, Offen D, Green P. Docosahexaenoic acid and arachidonic acid are fundamental supplements for the induction of neuronal differentiation. J Lipid Res. 2007;483:513–517
  52. He C, Qu X, Cui L, Wang J, Kang JX. Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proc Natl Acad Sci U S Am. 2009;10627:11370–11375
  53. Salvati S, Natali F, Attorri L, Di Benedetto R, Leonardi F, Di Biase A, et al. Eicosapentaenoic acid stimulates the expression of myelin proteins in rat brain. J Neurosci Res. 2008;864:776–784
  54. Ahmad A, Moriguchi T, Salem N. Decrease in neuron size in docosahexaenoic acid-deficient brain. Pediatr Neurol. 2002;263:210–218
  55. Wang PY, Chen JJ, Su HM. Docosahexaenoic acid supplementation of primary rat hippocampal neurons attenuates the neurotoxicity induced by aggregated amyloid beta protein42 and upregulates cytoskeletal protein expression. J Nutr Biochem. 2009;accepted
  56. Contreras MA, Greiner RS, Chang MC, Myers CS, Salem N, Rapoport SI. Nutritional deprivation of alpha-linolenic acid decreases but does not abolish turnover and availability of unacylated docosahexaenoic acid and docosahexaenoyl-CoA in rat brain. J Neurochem. 2000;756:2392–2400
  57. Diau GY, Hsieh AT, Sarkadi-Nagy EA, Wijendran V, Nathanielsz PW, Brenna JT. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med. 2005;3:11
  58. Moriguchi T, Greiner RS, Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J Neurochem. 2000;756:2563–2573
  59. Lim SY, Hoshiba J, Moriguchi T, Salem N. N-3 fatty acid deficiency induced by a modified artificial rearing method leads to poorer performance in spatial learning tasks. Pediatr Res. 2005;584:741–748
  60. Moriguchi T, Salem N. Recovery of brain docosahexaenoate leads to recovery of spatial task performance. J Neurochem. 2003;872:297–309
  61. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature. 2004;4296993:761–766
  62. Mizuno K, Giese KP. Hippocampus-dependent memory formation: do memory type-specific mechanisms exist?. J Pharmacol Sci. 2005;983:191–197
  63. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993;3616407:31–39
  64. Kawashima A, Harada T, Kami H, Yano T, Imada K, Mizuguchi K. Effects of eicosapentaenoic acid on synaptic plasticity, fatty acid profile and phosphoinositide 3-kinase signaling in rat hippocampus and differentiated PC12 cells. J Nutr Biochem. 2009;
  65. Fujita S, Ikegaya Y, Nishikawa M, Nishiyama N, Matsuki N. Docosahexaenoic acid improves long-term potentiation attenuated by phospholipase A(2) inhibitor in rat hippocampal slices. Br J Pharmacol. 2001;1327:1417–1422
  66. Wu A, Ying Z, Gomez-Pinilla F. Docosahexaenoic acid dietary supplementation enhances the effects of exercise on synaptic plasticity and cognition. Neuroscience. 2008;1553:751–759
  67. Sakamoto T, Cansev M, Wurtman RJ. Oral supplementation with docosahexaenoic acid and uridine-5'-monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res. 2007;1182:50–59
  68. Tanabe Y, Hashimoto M, Sugioka K, Maruyama M, Fujii Y, Hagiwara R, et al. Improvement of spatial cognition with dietary docosahexaenoic acid is associated with an increase in Fos expression in rat CA1 hippocampus. Clin Exp Pharmacol Physiol. 2004;3110:700–703
  69. Cansev M, Wurtman RJ. Chronic administration of docosahexaenoic acid or eicosapentaenoic acid, but not arachidonic acid, alone or in combination with uridine, increases brain phosphatide and synaptic protein levels in gerbils. Neuroscience. 2007;1482:421–431
  70. Cansev M, Wurtman RJ, Sakamoto T, Ulus IH. Oral administration of circulating precursors for membrane phosphatides can promote the synthesis of new brain synapses. Alzheimers Dement. 2008;41(Suppl 1):S153–S168
  71. Calon F, Lim GP, Yang F, Morihara T, Teter B, Ubeda O, et al. Docosahexaenoic Acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron. 2004;435:633–645
  72. Kaplan MS, Bell DH. Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci. 1984;46:1429–1441
  73. Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci. 2002;223:629–634
  74. Eckenhoff MF, Rakic P. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci. 1988;88:2729–2747
  75. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;411:1313–1317
  76. Bruel-Jungerman E, Davis S, Rampon C, Laroche S. Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci. 2006;2622:5888–5893
  77. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S Am. 2003;10024:14385–14390
  78. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature. 2001;4106826:372–376
  79. 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;1366:1570–1575
  80. Kawakita E, Hashimoto M, Shido O. Docosahexaenoic acid promotes neurogenesis in vitro and in vivo. Neuroscience. 2006;1393:991–997
  81. Kim HY, Akbar M, Lau A, Edsall L. Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n-3). Role of phosphatidylserine in antiapoptotic effect. J Biol Chem. 2000;27545:35215–35223
  82. Akbar M, Calderon F, Wen Z, Kim HY. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc Natl Acad Sci U S Am. 2005;10231:10858–10863
  83. Akbar M, Kim HY. Protective effects of docosahexaenoic acid in staurosporine-induced apoptosis: involvement of phosphatidylinositol-3 kinase pathway. J Neurochem. 2002;823:655–665
  84. Rotstein NP, Politi LE, German OL, Girotti R. Protective effect of docosahexaenoic acid on oxidative stress-induced apoptosis of retina photoreceptors. Invest Ophthalmol Vis Sci. 2003;445:2252–2259
  85. Rotstein NP, Aveldano MI, Barrantes FJ, Roccamo AM, Politi LE. Apoptosis of retinal photoreceptors during development in vitro: protective effect of docosahexaenoic acid. J Neurochem. 1997;692:504–513
  86. Lauritzen I, Blondeau N, Heurteaux C, Widmann C, Romey G, Lazdunski M. Polyunsaturated fatty acids are potent neuroprotectors. EMBO J. 2000;198:1784–1793
  87. Lonergan PE, Martin DS, Horrobin DF, Lynch MA. Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J Biol Chem. 2002;27723:20804–20811
  88. Bas O, Songur A, Sahin O, Mollaoglu H, Ozen OA, Yaman M, et al. The protective effect of fish n-3 fatty acids on cerebral ischemia in rat hippocampus. Neurochem Int. 2007;503:548–554
  89. Wu A, Ying Z, Gomez-Pinilla F. Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats. J Neurotrauma. 2004;2110:1457–1467
  90. Dyall SC, Michael GJ, Whelpton R, Scott AG, Michael-Titus AT. Dietary enrichment with omega-3 polyunsaturated fatty acids reverses age-related decreases in the GluR2 and NR2B glutamate receptor subunits in rat forebrain. Neurobiol Aging. 2007;283:424–439
  91. McGahon BM, Martin DS, Horrobin DF, Lynch MA. Age-related changes in synaptic function: analysis of the effect of dietary supplementation with omega-3 fatty acids. Neuroscience. 1999;941:305–314
  92. Martin DS, Spencer P, Horrobin DF, Lynch MA. Long-term potentiation in aged rats is restored when the age-related decrease in polyunsaturated fatty acid concentration is reversed. Prostaglandins Leukot Essent Fatty Acids. 2002;672-3:121–130
  93. Nacher J, Alonso-Llosa G, Rosell DR, McEwen BS. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging. 2003;242:273–284
  94. Markham JA, Juraska JM. Aging and sex influence the anatomy of the rat anterior cingulate cortex. Neurobiol Aging. 2002;234:579–588
  95. Jacobs B, Driscoll L, Schall M. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. The Journal of comparative neurology. 1997;3864:661–680
  96. O'Donnell E, Vereker E, Lynch MA. Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. The European journal of neuroscience. 2000;121:345–352
  97. Lynch AM, Loane DJ, Minogue AM, Clarke RM, Kilroy D, Nally RE, et al. Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus. Neurobiol Aging. 2007;286:845–855
  98. Bourre JM, Dumont OS, Piciotti MJ, Pascal GA, Durand GA. Dietary alpha-linolenic acid deficiency in adult rats for 7 months does not alter brain docosahexaenoic acid content, in contrast to liver, heart and testes. Biochim Biophys Acta. 1992;11242:119–122
  99. Favreliere S, Perault MC, Huguet F, De Javel D, Bertrand N, Piriou A, et al. DHA-enriched phospholipid diets modulate age-related alterations in rat hippocampus. Neurobiol Aging. 2003;242:233–243
  100. Teather LA, Wurtman RJ. Dietary cytidine (5′)-diphosphocholine supplementation protects against development of memory deficits in aging rats. Progress in neuro-psychopharmacology & biological psychiatry. 2003;274:711–717
  101. Barcelo-Coblijn G, Hogyes E, Kitajka K, Puskas LG, Zvara A, Hackler L, et al. Modification by docosahexaenoic acid of age-induced alterations in gene expression and molecular composition of rat brain phospholipids. Proc Natl Acad Sci U S Am. 2003;10020:11321–11326
  102. Gamoh S, Hashimoto M, Hossain S, Masumura S. Chronic administration of docosahexaenoic acid improves the performance of radial arm maze task in aged rats. Clin Exp Pharmacol Physiol. 2001;284:266–270
  103. Mulder C, Scheltens P, Visser JJ, van Kamp GJ, Schutgens RB. Genetic and biochemical markers for Alzheimer's disease: recent developments. Ann Clin Biochem. 2000;37(Pt 5):593–607
  104. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A. Tau is essential to beta -amyloid-induced neurotoxicity. Proc Natl Acad Sci U S Am. 2002;999:6364–6369
  105. Spires TL, Hyman BT. Transgenic models of Alzheimer's disease: learning from animals. NeuroRx. 2005;23:423–437
  106. Braak H, Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol Aging. 1997;184:351–357
  107. Florent S, Malaplate-Armand C, Youssef I, Kriem B, Koziel V, Escanye MC, et al. Docosahexaenoic acid prevents neuronal apoptosis induced by soluble amyloid-beta oligomers. J Neurochem. 2006;962:385–395
  108. Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O, et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci. 2005;2512:3032–3040
  109. Green KN, Martinez-Coria H, Khashwji H, Hall EB, Yurko-Mauro KA, Ellis L, et al. Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-beta and tau pathology via a mechanism involving presenilin 1 levels. J Neurosci. 2007;2716:4385–4395
  110. Hashimoto M, Hossain S, Tanabe Y, Kawashima A, Harada T, Yano T, et al. The protective effect of dietary eicosapentaenoic acid against impairment of spatial cognition learning ability in rats infused with amyloid beta((1-40)). J Nutr Biochem. 2009;[in press]
  111. 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;1353:549–555
  112. Hashimoto M, Hossain S, Shimada T, Sugioka K, Yamasaki H, Fujii Y, et al. Docosahexaenoic acid provides protection from impairment of learning ability in Alzheimer's disease model rats. J Neurochem. 2002;815:1084–1091
  113. Freund-Levi Y, Eriksdotter-Jonhagen M, Cederholm T, Basun H, Faxen-Irving G, Garlind A, et al. Omega-3 fatty acid treatment in 174 patients with mild to moderate Alzheimer disease: OmegAD study: a randomized double-blind trial. Arch Neurol. 2006;6310:1402–1408
  114. Beydoun MA, Kaufman JS, Satia JA, Rosamond W, Folsom AR. Plasma n-3 fatty acids and the risk of cognitive decline in older adults: the Atherosclerosis Risk in Communities Study. Am J Clin Nutr. 2007;854:1103–1111
  115. Whalley LJ, Deary IJ, Starr JM, Wahle KW, Rance KA, Bourne VJ, et al. n-3 Fatty acid erythrocyte membrane content, APOE varepsilon4, and cognitive variation: an observational follow-up study in late adulthood. Am J Clin Nutr. 2008;872:449–454
  116. Boudrault C, Bazinet RP, Ma DW. Experimental models and mechanisms underlying the protective effects of n-3 polyunsaturated fatty acids in Alzheimer's disease. J Nutr Biochem. 2009;201:1–10
  117. Bakewell L, Burdge GC, Calder PC. Polyunsaturated fatty acid concentrations in young men and women consuming their habitual diets. Br J Nutr. 2006;961:93–99
  118. Crowe FL, Skeaff CM, Green TJ, Gray AR. Serum n-3 long-chain PUFA differ by sex and age in a population-based survey of New Zealand adolescents and adults. Br J Nutr. 2008;991:168–174
  119. Giltay EJ, Gooren LJ, Toorians AW, Katan MB, Zock PL. Docosahexaenoic acid concentrations are higher in women than in men because of estrogenic effects. Am J Clin Nutr. 2004;805:1167–1174
  120. Burdge GC, Jones AE, Wootton SA. Eicosapentaenoic and docosapentaenoic acids are the principal products of alpha-linolenic acid metabolism in young men⁎. Br J Nutr. 2002;884:355–363
  121. Burdge GC, Wootton SA. Conversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br J Nutr. 2002;884:411–420
  122. Giltay EJ, Duschek EJ, Katan MB, Zock PL, Neele SJ, Netelenbos JC. Raloxifene and hormone replacement therapy increase arachidonic acid and docosahexaenoic acid levels in postmenopausal women. J Endocrinol. 2004;1823:399–408
  123. Sumino H, Ichikawa S, Murakami M, Nakamura T, Kanda T, Sakamaki T, et al. Effects of hormone replacement therapy on circulating docosahexaenoic acid and eicosapentaenoic acid levels in postmenopausal women. Endocr J. 2003;501:51–59
  124. Extier A, Langelier B, Perruchot MH, Guesnet P, Van Veldhoven PP, Lavialle M, et al. Gender affects liver desaturase expression in a rat model of n-3 fatty acid repletion. J Nutr Biochem. 2009;[in press]
  125. McNamara RK, Able J, Jandacek R, Rider T, Tso P. Gender differences in rat erythrocyte and brain docosahexaenoic acid composition: Role of ovarian hormones and dietary omega-3 fatty acid composition. Psychoneuroendocrinology. 2008;
  126. McNamara RK, Able J, Jandacek R, Rider T, Tso P. Gender differences in rat erythrocyte and brain docosahexaenoic acid composition: role of ovarian hormones and dietary omega-3 fatty acid composition. Psychoneuroendocrinology. 2009;344:532–539
  127. Hojo Y, Murakami G, Mukai H, Higo S, Hatanaka Y, Ogiue-Ikeda M, et al. Estrogen synthesis in the brain–role in synaptic plasticity and memory. Mol Cell Endocrinol. 2008;2901-2:31–43
  128. Frick KM. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here?. Horm Behav. 2009;551:2–23
  129. Behl C. Oestrogen as a neuroprotective hormone. Nat Rev Neurosci. 2002;36:433–442
  130. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R, et al. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci. 2008;113:334–343
  131. de Urquiza AM, Liu S, Sjoberg M, Zetterstrom RH, Griffiths W, Sjovall J, et al. Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science (New York, NY. 2000;2905499:2140–2144
  132. Misner DL, Jacobs S, Shimizu Y, de Urquiza AM, Solomin L, Perlmann T, et al. Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc Natl Acad Sci U S Am. 2001;9820:11714–11719
  133. Jacobs S, Lie DC, DeCicco KL, Shi Y, DeLuca LM, Gage FH, et al. Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc Natl Acad Sci U S Am. 2006;10310:3902–3907
  134. Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell. 2008;1346:921–931
  135. McCaffery P, Zhang J, Crandall JE. Retinoic acid signaling and function in the adult hippocampus. J Neurobiol. 2006;667:780–791
  136. Lane MA, Bailey SJ. Role of retinoid signalling in the adult brain. Prog Neurobiol. 2005;754:275–293
  137. Mey J. New therapeutic target for CNS injury? The role of retinoic acid signaling after nerve lesions. J Neurobiol. 2006;667:757–779
  138. Goodman AB. Retinoid receptors, transporters, and metabolizers as therapeutic targets in late onset Alzheimer disease. J Cell Physiol. 2006;2093:598–603

PII: S0955-2863(09)00245-9

doi: 10.1016/j.jnutbio.2009.11.003

The Journal of Nutritional Biochemistry
Volume 21, Issue 5 , Pages 364-373 , May 2010

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