Long term adequate n-3 polyunsaturated fatty acid diet protects from depressive-like behavior but not from working memory disruption and brain cytokine expression in aged mice

Brain, Behavior, and Immunity

Volumn 26, Issue 5, 2012, Pages 721-731

  Moranis, Aurélie ^a,b   Delpech, Jean Christophe ^a,b   De Smedt Peyrusse, Véronique ^a,b   Aubert, Agnès ^a,b   Guesnet, Philippe ^c   Lavialle, Monique ^c   Joffre, Corinne ^a,b   Layé, Sophie ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INRA   (France)

Author keywords

Aging; Brain; Cognition; Cytokine; Depression; DHA

Indexed keywords

CYTOKINE; DOCOSAHEXAENOIC ACID; INTERLEUKIN 10; INTERLEUKIN 6; LINOLENIC ACID; OMEGA 3 FATTY ACID;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; DIETARY INTAKE; EMOTION; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL MEMORY; SPLEEN; WORKING MEMORY;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; CEREBRAL CORTEX; CYTOKINES; DEPRESSION; DIET; EMOTIONS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; FEMALE; INTERLEUKIN-10; INTERLEUKIN-6; LIVER; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; PHOSPHOLIPIDS; SPLEEN;

EID: 84861960992     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.11.001     Document Type: Article

References (97)

1. Arita M., Yoshida M., Hong S., Tjonahen E., Glickman J.N., Petasis N.A., Blumberg R.S., Serhan C.N. Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc. Natl. Acad. Sci. USA 2005, 102:7671-7676.
2. Astorg P., Couthouis A., Bertrais S., Arnault N., Meneton P., Guesnet P., Alessandri J.M., Galan P., Hercberg S. Association of fish and long-chain n-3 polyunsaturated fatty acid intakes with the occurrence of depressive episodes in middle-aged French men and women. Prostaglandins Leukot. Essent. Fatty Acids 2008, 78:171-182.
3. Barberger-Gateau P., Letenneur L., Deschamps V., Peres K., Dartigues J.F., Renaud S. Fish, meat, and risk of dementia: cohort study. BMJ 2002, 325:932-933.
4. Barcelo-Coblijn G., Hogyes E., Kitajka K., Puskas L.G., Zvara A., Hackler L., Nyakas C., Penke Z., Farkas T. Modification by docosahexaenoic acid of age-induced alterations in gene expression and molecular composition of rat brain phospholipids. Proc. Natl. Acad. Sci. USA 2003, 100:11321-11326.
5. Bazan N.G., Molina M.F., Gordon W.C. Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. Annu. Rev. Nutr. 2011, 31:321-351.
6. Bazan N.G., Musto A.E., Knott E.J. Endogenous signaling by Omega-3 docosahexaenoic acid-derived mediators sustains homeostatic synaptic and circuitry integrity. Mol. Neurobiol. 2011, 44:216-222.
7. Blok W.L., Deslypere J.P., Demacker P.N., van der Ven-Jongekrijg J., Hectors M.P., van der Meer J.W., Katan M.B. Pro- and anti-inflammatory cytokines in healthy volunteers fed various doses of fish oil for 1year. Eur. J. Clin. Invest. 1997, 27:1003-1008.
8. Bodles A.M., Barger S.W. Cytokines and the aging brain - what we don't know might help us. Trends Neurosci. 2004, 27:621-626.
9. Bourre J.M. Dietary omega-3 fatty acids and psychiatry: mood, behaviour, stress, depression, dementia and aging. J. Nutr. Health Aging 2005, 9:31-38.
10. Bourre J.M., Bonneil M., Clement M., Dumont O., Durand G., Lafont H., Nalbone G., Piciotti M. Function of dietary polyunsaturated fatty acids in the nervous system. Prostaglandins Leukot. Essent. Fatty Acids 1993, 48:5-15.
11. Calder P.C. Omega 3 polyunsaturated fatty acids, inflammation and immunity. World Rev. Nutr. Diet 2001, 88:109-116.
12. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., Rostaing P., Triller A., Salem N., Ashe K.H., Frautschy S.A., Cole G.M. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43:633-645.
13. Capuron L., Moranis A., Combe N., Cousson-Gelie F., Fuchs D., De Smedt-Peyrusse V., Barberger-Gateau P., Laye S. Vitamin E status and quality of life in the elderly: influence of inflammatory processes. Br. J. Nutr. 2009, 102:1390-1394.
14. Capuron L., Schroecksnadel S., Feart C., Aubert A., Higueret D., Barberger-Gateau P., Laye S., Fuchs D. Chronic low-grade inflammation in elderly persons is associated with altered tryptophan and tyrosine metabolism: role in neuropsychiatric symptoms. Biol. Psychiatry 2011, 70:175-182.
15. Carrie I., Clement M., De Javel D., Frances H., Bourre J.M. Learning deficits in first generation OF1 mice deficient in (n-3) polyunsaturated fatty acids do not result from visual alteration. Neurosci. Lett. 1999, 266:69-72.
16. Carrie I., Clement M., de Javel D., Frances H., Bourre J.M. Phospholipid supplementation reverses behavioral and biochemical alterations induced by n-3 polyunsaturated fatty acid deficiency in mice. J. Lipid Res. 2000, 41:473-480.
17. Carrie I., Clement M., de Javel D., Frances H., Bourre J.M. Specific phospholipid fatty acid composition of brain regions in mice. Effects of n-3 polyunsaturated fatty acid deficiency and phospholipid supplementation. J. Lipid Res. 2000, 41:465-472.
18. Carrie I., Guesnet P., Bourre J.M., Frances H. Diets containing long-chain n-3 polyunsaturated fatty acids affect behaviour differently during development than ageing in mice. Br. J. Nutr. 2000, 83:439-447.
19. Catalan J., Moriguchi T., Slotnick B., Murthy M., Greiner R.S., Salem N. Cognitive deficits in docosahexaenoic acid-deficient rats. Behav. Neurosci. 2002, 116:1022-1031.
20. Caughey G.E., Mantzioris E., Gibson R.A., Cleland L.G., James M.J. The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am. J. Clin. Nutr. 1996, 63:116-122.
21. Chavali S.R., Weeks C.E., Zhong W.W., Forse R.A. Increased production of TNF-alpha and decreased levels of dienoic eicosanoids, IL-6 and IL-10 in mice fed menhaden oil and juniper oil diets in response to an intraperitoneal lethal dose of LPS. Prostaglandins Leukot. Essent. Fatty Acids 1998, 59:89-93.
22. Choi Y., Kim H.S., Shin K.Y., Kim E.M., Kim M., Park C.H., Jeong Y.H., Yoo J., Lee J.P., Chang K.A., Kim S., Suh Y.H. Minocycline attenuates neuronal cell death and improves cognitive impairment in Alzheimer's disease models. Neuropsychopharmacology 2007, 32:2393-2404.
23. 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. 1990, 31:237-247.
24. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
25. Datta S.C., Opp M.R. Lipopolysaccharide-induced increases in cytokines in discrete mouse brain regions are detectable using Luminex xMAP technology. J. Neurosci. Methods 2008, 175:119-124.
26. De Smedt-Peyrusse V., Sargueil F., Moranis A., Harizi H., Mongrand S., Laye S. Docosahexaenoic acid prevents lipopolysaccharide-induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization. J. Neurochem. 2008, 105:296-307.
27. Delion S., Chalon S., Guilloteau D., Besnard J.C., Durand G. Alpha-Linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex. J. Neurochem. 1996, 66:1582-1591.
28. DeMar J.C., Ma K., Bell J.M., Igarashi M., Greenstein D., Rapoport S.I. One generation of n-3 polyunsaturated fatty acid deprivation increases depression and aggression test scores in rats. J. Lipid Res. 2006, 47:172-180.
29. Dinel A.L., Andre C., Aubert A., Ferreira G., Laye S., Castanon N. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One 2011, 6:e24325.
30. Dinh L., Dumont O., Durand G. Comparison of liver microsome enzyme and fatty acid composition recovery in adult and old rats deficient in 18:3n-3 refed a diet containing 18:3n-3. Biochem. Mol. Biol. Int. 1994, 32:869-877.
31. Dyall S.C., Michael G.J., Whelpton R., Scott A.G., Michael-Titus A.T. 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, 28:424-439.
32. Enslen M., Milon H., Malnoe A. Effect of low intake of n-3 fatty acids during development on brain phospholipid fatty acid composition and exploratory behavior in rats. Lipids 1991, 26:203-208.
33. Favreliere S., Perault M.C., Huguet F., De Javel D., Bertrand N., Piriou A., Durand G. DHA-enriched phospholipid diets modulate age-related alterations in rat hippocampus. Neurobiol. Aging 2003, 24:233-243.
34. Feart C., Peuchant E., Letenneur L., Samieri C., Montagnier D., Fourrier-Reglat A., Barberger-Gateau P. Plasma eicosapentaenoic acid is inversely associated with severity of depressive symptomatology in the elderly: data from the Bordeaux sample of the Three-City Study. Am. J. Clin. Nutr. 2008, 87:1156-1162.
35. Feart C., Torres M.J., Samieri C., Jutand M.A., Peuchant E., Simopoulos A.P., Barberger-Gateau P. Adherence to a Mediterranean diet and plasma fatty acids: data from the Bordeaux sample of the Three-City study. Br. J. Nutr. 2011, 106:149-158.
36. Fedorova I., Hussein N., Di Martino C., Moriguchi T., Hoshiba J., Majchrzak S., Salem N. An n-3 fatty acid deficient diet affects mouse spatial learning in the Barnes circular maze. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77:269-277.
37. Fedorova I., Salem N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot. Essent. Fatty Acids 2006, 75:271-289.
38. Frasure-Smith N., Lesperance F., Julien P. Major depression is associated with lower omega-3 fatty acid levels in patients with recent acute coronary syndromes. Biol. Psychiatry 2004, 55:891-896.
39. Frenois F., Moreau M., O'Connor J., Lawson M., Micon C., Lestage J., Kelley K.W., Dantzer R., Castanon N. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 2007, 32:516-531.
40. Galli C., White H.B., Paoletti R. Lipid alterations and their reversion in the central nervous system of growing rats deficient in essential fatty acids. Lipids 1971, 6:378-387.
41. 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, 28:266-270.
42. Gamoh S., Hashimoto M., Sugioka K., Shahdat Hossain M., Hata N., Misawa Y., Masumura S. Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats. Neuroscience 1999, 93:237-241.
43. Gao Q., Niti M., Feng L., Yap K.B., Ng T.P. Omega-3 polyunsaturated fatty acid supplements and cognitive decline: Singapore Longitudinal Aging Studies. J. Nutr. Health Aging 2011, 15:32-35.
44. Godbout J.P., Johnson R.W. Interleukin-6 in the aging brain. J. Neuroimmunol. 2004, 147:141-144.
45. Green P., Yavin E. Mechanisms of docosahexaenoic acid accretion in the fetal brain. J. Neurosci. Res. 1998, 52:129-136.
46. Greiner R.S., Moriguchi T., Hutton A., Slotnick B.M., Salem N. Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 1999, 34(Suppl.):S239-S243.
47. Griffin R., Nally R., Nolan Y., McCartney Y., Linden J., Lynch M.A. The age-related attenuation in long-term potentiation is associated with microglial activation. J. Neurochem. 2006, 99:1263-1272.
48. 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, 135:549-555.
49. Huang S.Y., Yang H.T., Chiu C.C., Pariante C.M., Su K.P. Omega-3 fatty acids on the forced-swimming test. J. Psychiatry Res. 2008, 42:58-63.
50. Kavanagh T., Lonergan P.E., Lynch M.A. Eicosapentaenoic acid and gamma-linolenic acid increase hippocampal concentrations of IL-4 and IL-10 and abrogate lipopolysaccharide-induced inhibition of long-term potentiation. Prostaglandins Leukot. Essent. Fatty Acids 2004, 70:391-397.
51. Kesse-Guyot E., Peneau S., Ferry M., Jeandel C., Hercberg S., Galan P. Thirteen-year prospective study between fish consumption, long-chain n-3 fatty acids intakes and cognitive function. J. Nutr. Health Aging 2011, 15:115-120.
52. Khalfoun B., Thibault F., Watier H., Bardos P., Lebranchu Y. Docosahexaenoic and eicosapentaenoic acids inhibit in vitro human endothelial cell production of interleukin-6. Adv. Exp. Med. Biol. 1997, 400B:589-597.
53. Kiecolt-Glaser J.K. Stress, food, and inflammation: psychoneuroimmunology and nutrition at the cutting edge. Psychosom. Med. 2010, 72:365-369.
54. Labrousse V.F., Costes L., Aubert A., Darnaudery M., Ferreira G., Amedee T., Laye S. Impaired interleukin-1beta and c-Fos expression in the hippocampus is associated with a spatial memory deficit in P2X(7) receptor-deficient mice. PLoS One 2009, 4:e6006.
55. Lafourcade M., Larrieu T., Mato S., Duffaud A., Sepers M., Matias I., De Smedt-Peyrusse V., Labrousse V.F., Bretillon L., Matute C., Rodriguez-Puertas R., Laye S., Manzoni O.J. Nutritional omega-3 deficiency abolishes endocannabinoid-mediated neuronal functions. Nat. Neurosci. 2011, 14:345-350.
56. Laye S., Parnet P., Goujon E., Dantzer R. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Brain Res. Mol. Brain Res. 1994, 27:157-162.
57. Layé S. Polyunsaturated fatty acids, neuroinflammation and well being. Prostaglandins Leukot Essent Fatty Acids 2010, 82:295-303.
58. Lin Q., Ruuska S.E., Shaw N.S., Dong D., Noy N. Ligand selectivity of the peroxisome proliferator-activated receptor alpha. Biochemistry 1999, 38:185-190.
59. Lu D.Y., Tsao Y.Y., Leung Y.M., Su K.P. Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for omega-3 fatty acids. Neuropsychopharmacology 2010, 35:2238-2248.
60. Lukiw W.J., Cui J.G., Marcheselli V.L., Bodker M., Botkjaer A., Gotlinger K., Serhan C.N., Bazan N.G. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J. Clin. Invest. 2005, 115:2774-2783.
61. Lyons A., Lynch A.M., Downer E.J., Hanley R., O'Sullivan J.B., Smith A., Lynch M.A. Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attenuates microglial activation in vivo and in vitro. J. Neurochem. 2009, 110:1547-1556.
62. Marcheselli V.L., Mukherjee P.K., Arita M., Hong S., Antony R., Sheets K., Winkler J.W., Petasis N.A., Serhan C.N., Bazan N.G. Neuroprotectin D1/protectin D1 stereoselective and specific binding with human retinal pigment epithelial cells and neutrophils. Prostaglandins Leukot. Essent. Fatty Acids 2010, 82:27-34.
63. McNamara R.K., Jandacek R., Rider T., Tso P., Cole-Strauss A., Lipton J.W. Omega-3 fatty acid deficiency increases constitutive pro-inflammatory cytokine production in rats: relationship with central serotonin turnover. Prostaglandins Leukot. Essent. Fatty Acids 2010, 83:185-191.
64. Michaeli B., Berger M.M., Revelly J.P., Tappy L., Chiolero R. Effects of fish oil on the neuro-endocrine responses to an endotoxin challenge in healthy volunteers. Clin. Nutr. 2007, 26:70-77.
65. Mingam R., Moranis A., Bluthe R.M., De Smedt-Peyrusse V., Kelley K.W., Guesnet P., Lavialle M., Dantzer R., Laye S. Uncoupling of interleukin-6 from its signalling pathway by dietary n-3-polyunsaturated fatty acid deprivation alters sickness behaviour in mice. Eur. J. Neurosci. 2008, 28:1877-1886.
66. Minogue A.M., Lynch A.M., Loane D.J., Herron C.E., Lynch M.A. Modulation of amyloid-beta-induced and age-associated changes in rat hippocampus by eicosapentaenoic acid. J. Neurochem. 2007, 103:914-926.
67. Moriguchi T., Greiner R.S., Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 2000, 75:2563-2573.
68. Mukherjee P.K., Chawla A., Loayza M.S., Bazan N.G. Docosanoids are multifunctional regulators of neural cell integrity and fate: significance in aging and disease. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77:233-238.
69. Murray C.A., Lynch M.A. Evidence that increased hippocampal expression of the cytokine interleukin-1 beta is a common trigger for age- and stress-induced impairments in long-term potentiation. J. Neurosci. 1998, 18:2974-2981.
70. O'Connor J.C., Lawson M.A., Andre C., Moreau M., Lestage J., Castanon N., Kelley K.W., Dantzer R. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol. Psychiatry 2009, 14:511-522.
71. Petursdottir D.H., Olafsdottir I., Hardardottir I. Dietary fish oil increases tumor necrosis factor secretion but decreases interleukin-10 secretion by murine peritoneal macrophages. J. Nutr. 2002, 132:3740-3743.
72. Pluess T.T., Hayoz D., Berger M.M., Tappy L., Revelly J.P., Michaeli B., Carpentier Y.A., Chiolero R.L. Intravenous fish oil blunts the physiological response to endotoxin in healthy subjects. Intensive Care Med. 2007, 33:789-797.
73. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
74. Rao J.S., Ertley R.N., Lee H.J., DeMar J.C., Arnold J.T., Rapoport S.I., Bazinet R.P. N-3 polyunsaturated fatty acid deprivation in rats decreases frontal cortex BDNF via a p38 MAPK-dependent mechanism. Mol. Psychiatry 2007, 12:36-46.
75. Rapoport S.I. Brain arachidonic and docosahexaenoic acid cascades are selectively altered by drugs, diet and disease. Prostaglandins Leukot. Essent. Fatty Acids 2008, 79:153-156.
76. Rapoport S.I., Rao J.S., 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.
77. Richwine A.F., Sparkman N.L., Dilger R.N., Buchanan J.B., Johnson R.W. Cognitive deficits in interleukin-10-deficient mice after peripheral injection of lipopolysaccharide. Brain Behav. Immun. 2009, 23:794-802.
78. Samieri C., Feart C., Proust-Lima C., Peuchant E., Dartigues J.F., Amieva H., Barberger-Gateau P. Omega-3 fatty acids and cognitive decline: modulation by ApoEepsilon4 allele and depression. Neurobiol. Aging 2011, 32(2317):e13-22.
79. Song C., Manku M.S., Horrobin D.F. Long-chain polyunsaturated fatty acids modulate interleukin-1beta-induced changes in behavior, monoaminergic neurotransmitters, and brain inflammation in rats. J. Nutr. 2008, 138:954-963.
80. Song C., Phillips A.G., Leonard B.E., Horrobin D.F. Ethyl-eicosapentaenoic acid ingestion prevents corticosterone-mediated memory impairment induced by central administration of interleukin-1beta in rats. Mol. Psychiatry 2004, 9:630-638.
81. Sparkman N.L., Buchanan J.B., Heyen J.R., Chen J., Beverly J.L., Johnson R.W. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J. Neurosci. 2006, 26:10709-10716.
82. Takeuchi T., Iwanaga M., Harada E. Possible regulatory mechanism of DHA-induced anti-stress reaction in rats. Brain Res. 2003, 964:136-143.
83. Tanabe Y., Hashimoto M., Sugioka K., Maruyama M., Fujii Y., Hagiwara R., Hara T., Hossain S.M., Shido O. 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, 31:700-703.
84. Tancredi V., D'Antuono M., Cafe C., Giovedi S., Bue M.C., D'Arcangelo G., Onofri F., Benfenati F. The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogen-activated protein kinase ERK. J. Neurochem. 2000, 75:634-643.
85. Tancredi V., D'Arcangelo G., Grassi F., Tarroni P., Palmieri G., Santoni A., Eusebi F. Tumor necrosis factor alters synaptic transmission in rat hippocampal slices. Neurosci. Lett. 1992, 146:176-178.
86. Wainwright P.E., Huang Y.S., Bulman-Fleming B., Levesque S., McCutcheon D. The effects of dietary fatty acid composition combined with environmental enrichment on brain and behavior in mice. Behav. Brain Res. 1994, 60:125-136.
87. Wainwright P.E., Huang Y.S., Coscina D.V., Levesque S., McCutcheon D. Brain and behavioral effects of dietary n-3 deficiency in mice. A three generational study. Dev. Psychobiol. 1994, 27:467-487.
88. Weldon S.M., Mullen A.C., Loscher C.E., Hurley L.A., Roche H.M. Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharide-stimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J. Nutr. Biochem. 2007, 18:250-258.
89. Wietrzych-Schindler M., Szyszka-Niagolov M., Ohta K., Endo Y., Perez E., de Lera A.R., Chambon P., Krezel W. Retinoid x receptor gamma is implicated in docosahexaenoic acid modulation of despair behaviors and working memory in mice. Biol. Psychiatry 2011, 69:788-794.
90. Wynne A.M., Henry C.J., Huang Y., Cleland A., Godbout J.P. Protracted downregulation of CX3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav. Immun. 2010, 24:1190-1201.
91. Xiao Y.F., Ma L., Wang S.Y., Josephson M.E., Wang G.K., Morgan J.P., Leaf A. Potent block of inactivation-deficient Na+ channels by n-3 polyunsaturated fatty acids. Am. J. Physiol. Cell Physiol. 2006, 290:C362-C370.
92. Yates M., Leake A., Candy J.M., Fairbairn A.F., McKeith I.G., Ferrier I.N. 5HT2 receptor changes in major depression. Biol. Psychiatry 1990, 27:489-496.
93. Ye S.M., Johnson R.W. An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 2001, 9:183-192.
94. Yehuda S., Rabinovitz S., Carasso R.L., Mostofsky D.I. The role of polyunsaturated fatty acids in restoring the aging neuronal membrane. Neurobiol. Aging 2002, 23:843-853.
95. Yehuda S., Rabinovitz S., Mostofsky D.I. Essential fatty acids are mediators of brain biochemistry and cognitive functions. J. Neurosci. Res. 1999, 56:565-570.
96. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun. 2011, 25:181-213.
97. Zujovic V., Benavides J., Vige X., Carter C., Taupin V. Fractalkine modulates TNF-alpha secretion and neurotoxicity induced by microglial activation. Glia 2000, 29:305-315.