Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1801, Issue 8, 2010, Pages 791-798

  Oster, Thierry ^a   Pillot, Thierry ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Alzheimer's disease; Cognition; Docosahexaenoic acid; Membrane lipids; Neuroprotection; Nutrition; Synapse

Indexed keywords

AMYLOID BETA PROTEIN; ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; LINOLEIC ACID; LIPID; OMEGA 3 FATTY ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE A2; SORTILIN;

ALZHEIMER DISEASE; ANTIINFLAMMATORY ACTIVITY; BRAIN FUNCTION; CELL SURVIVAL; DIET SUPPLEMENTATION; DIETARY INTAKE; ENZYME ACTIVATION; HUMAN; LONG TERM POTENTIATION; MEMORY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; SYNAPTOGENESIS;

MUS;

EID: 77953248904     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2010.02.011     Document Type: Review

References (102)

1. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Beyreuther K., Bush A.I., and Masters C.L. Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46 (1999) 860-866
2. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., and Klein W.L. Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci. 27 (2007) 796-807
3. Chui D.H., Tanahashi H., Ozawa K., Ikeda S., Checler F., Ueda O., Suzuki H., Araki W., Inoue H., Shirotani K., Takahashi K., Gallyas F., and Tabira T. Transgenic mice with Alzheimer presenilin 1 mutations show accelerated neurodegeneration without amyloid plaque formation. Nat. Med. 5 (1999) 540-544
4. Rowan M.J., Klyubin I., Wang Q., and Anwyl R. Synaptic plasticity disruption by amyloid-β protein: modulation by potential Alzheimer's disease modifying therapies. Biochem. Soc. Trans. 33 (2005) 563-567
5. Youssef I., Florent-Béchard S., Malaplate-Armand C., Koziel V., Bihain B., Olivier J.L., Leininger-Muller B., Kriem B., Oster T., and Pillot T. N-truncated amyloid-β oligomers induce learning impairment and neuronal apoptosis. Neurobiol. Aging 29 (2008) 1319-1333
6. Green R.C., Schneider L.S., Amato D.A., Beelen A.P., Wilcock G., Swabb E.A., Zavitz K.H., and Tarenflurbil Phase 3 Study Group. Effect of tarenflurbil on cognitive decline and activities of daily living in patients with mild Alzheimer disease: a randomized controlled trial. JAMA 302 (2009) 2557-2564
7. Kukar T., Prescott S., Eriksen J.L., Holloway V., Murphy M.P., Koo E.H., Golde T.E., and Nicolle M.M. Chronic administration of R-flurbiprofen attenuates learning impairments in transgenic amyloid precursor protein mice. BMC Neurosci. 8 54 (2007) 1-12
8. Luchsinger J.A., and Mayeux R. Dietary factors and Alzheimer's disease. Lancet Neurol. 3 (2004) 579-587
9. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., and Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261 (1993) 921-923
10. Purnell C., Gao S., Callahan C.M., and Hendrie H.C. Cardiovascular risk factors and incident Alzheimer disease: a systematic review of the literature. Alzheimer Dis. Assoc. Disord. 23 (2009) 1-10
11. Whitmer R.A., Sidney S., Selby J., Johnston S.C., and Yaffe K. Midlife cardiovascular risk factors and risk of dementia in late life. Neurology 64 (2005) 277-281
12. Luchsinger J.A., and Gustafson D.R. Adiposity, type 2 diabetes, and Alzheimer's disease. J. Alzheimers Dis. 16 (2009) 693-704
13. Luchsinger J.A., Reitz C., Honig L.S., Tang M.X., Shea S., and Mayeux R. Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 65 (2005) 545-551
14. Pasinetti G.M., and Eberstein J.A. Metabolic syndrome and the role of dietary lifestyles in Alzheimer's disease. J. Neurochem. 106 (2008) 1503-1514
15. Florent-Béchard S., Desbène C., Garcia P., Allouche A., Youssef I., Escanyé M.C., Koziel V., Hanse M., Malaplate-Armand C., Stenger C., Kriem B., Yen-Potin F.T., Olivier J.L., Pillot T., and Oster T. The essential role of lipids in Alzheimer's disease. Biochimie 91 (2009) 804-809
16. Craft S. The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged. Arch. Neurol. 66 (2009) 300-305
17. Erol A. An integrated and unifying hypothesis for the metabolic basis of sporadic Alzheimer's disease. J. Alzheimers Dis. 13 (2008) 241-253
18. Hooijmans C.R., and Kiliaan A.J. Fatty acids, lipid metabolism and Alzheimer pathology. Eur. J. Pharmacol. 585 (2008) 176-196
19. Pillot T., Goethals M., Vanloo B., Talussot C., Brasseur R., Vandekerckhove J., Rosseneu M., and Lins L. Fusogenic properties of the C-terminal domain of the Alzheimer β-amyloid peptide. J. Biol. Chem. 271 (1996) 28757-28765
20. Ege C., and Lee K.Y.C. Insertion of Alzheimer's Aβ40 peptide into lipid monolayers. Biophys. J. 87 (2004) 1732-1740
21. Sponne I., Fifre A., Kriem B., Oster T., Olivier J.L., and Pillot T. Membrane cholesterol interferes with neuronal apoptosis induced by soluble oligomers but not fibrils of the amyloid-β peptide. FASEB J. 18 (2004) 836-838
22. Florent S., Malaplate-Armand C., Youssef I., Kriem B., Koziel V., Escanyé M.C., Fifre A., Sponne I., Leininger-Muller B., Olivier J.L., Pillot T., and Oster T. Docosahexaenoic acid prevents neuronal apoptosis induced by soluble amyloid-β oligomers. J. Neurochem. 96 (2006) 385-395
23. Cheng H., Vetrivel K.S., Gong P., Meckler X., Parent A., and Thinakaran G. Mechanisms of disease: new therapeutic strategies for Alzheimer's disease/targeting APP processing in lipid rafts. Nat. Clin. Pract. Neurol. 3 (2007) 374-382
24. Sakurai T., Kaneko K., Okuno M., Wada K., Kashiyama T., Shimizu H., Akagi T., Hashikawa T., and Nukina N. Membrane microdomain switching: a regulatory mechanism of amyloid precursor protein processing. J. Cell Biol. 183 (2008) 339-352
25. Sastre M., Klockgether T., and Heneka M.T. Contribution of inflammatory processes to Alzheimer's disease: molecular mechanisms. Int. J. Dev. Neurosci. 24 (2006) 167-176
26. 2) immunoreactivity is elevated in Alzheimer's disease brain. Neurobiol. Dis. 3 (1996) 51-63
27. 2 mediates neuronal apoptosis induced by soluble oligomers of the amyloid-β peptide. FASEB J. 19 (2004) 85-87
28. He X., Huang Y., Li B., Gong C.X., and Schuchman E.H. Deregulation of sphingolipid metabolism in Alzheimer's disease. Neurobiol. Aging 31 (2010) 398-408
29. Zhang Y., Li X., Becker K.A., and Gulbins E. Ceramide-enriched membrane domains-structure and function. Biochim. Biophys. Acta 1788 (2009) 178-183
30. 2-dependent sphingomyelinase-ceramide pathway. Neurobiol. Dis. 23 (2006) 178-189
31. Tixier-Vidal A., Picart R., Loudes C., and Bauman A.F. Effects of polyunsaturated fatty acids and hormones on synaptogenesis in serum-free medium cultures of mouse fetal hypothalamic cells. Neuroscience 17 (1986) 115-132
32. Greiner R.S., Moriguchi T., Hutton A., Slotnick B.M., and Salem Jr. N. Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 34 (1999) S239-S243
33. Gamoh S., Hashimoto M., Sugioka K., Shahdat Hossain M., Hata N., Misawa Y., and Masumura S. Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats. Neuroscience 93 (1999) 237-241
34. Lauritzen I., Blondeau N., Heurteaux C., Widmann C., Romey G., and Lazdunski M. Polyunsaturated fatty acids are potent neuroprotectors. EMBO J. 19 (2000) 1784-1793
35. Hashimoto M., Hossain S., Shimada T., Sugioka K., Yamasaki H., Fujii Y., Ishibashi Y., Oka J., and Shido O. Docosahexaenoic acid provides protection from impairment of learning ability in Alzheimer's disease model rats. J. Neurochem. 81 (2002) 1084-1091
36. Crawford M.A. The early development and evolution of the human brain. Ups. J. Med. Sci. 48 (1990) 43-78
37. Schmitz G., and Ecker J. The opposing effects of n-3 and n-6 fatty acids. Prog. Lipid Res. 47 (2008) 147-155
38. 2-treated presynaptic membranes in vitro. Biochem. J. 318 (1996) 981-987
39. Nishizaki T., Nomura T., Matsuoka T., and Tsujishita Y. Arachidonic acid as a messenger for the expression of long-term potentiation. Biochem. Biophys. Res. Commun. 254 (1999) 446-449
40. Kotani S., Sakaguchi E., Warashina S., Matsukawa N., Ishikura Y., Kiso Y., Sakakibara M., Yoshimoto T., Guo J., and Yamashima T. Dietary supplementation of arachidonic and docosahexaenoic acids improves cognitive dysfunction. Neurosci. Res. 56 (2006) 159-164
41. 2 activation as a therapeutic approach for cognitive enhancement in early-stage Alzheimer disease. Psychopharmacology 202 (2009) 37-51
42. Cole G.M., Ma Q.L., and Frautschy S.A. Omega-3 fatty acids and dementia. Prostaglandins Leukot. Essent. Fatty Acids 81 (2009) 213-221
43. 2/3. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4046-4049
44. Hulbert A.J., and Else P.L. Membranes as possible pacemakers of metabolism. J. Theor. Biol. 199 (1999) 257-274
45. Barceló-Coblijn G., and Murphy E.J. Alpha-linolenic acid and its conversion to longer chain n-3 fatty acids: benefits for human health and a role in maintaining tissue n-3 fatty acid levels. Prog. Lipid Res. 48 (2009) 355-374
46. Plourde M., and Cunnane S.C. Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl. Physiol. Nutr. Metab. 32 (2007) 619-634
47. Kaduce T.L., Chan Y., Hell J.W., and Spector A.A. Docosahexaenoic acid synthesis from n-3 fatty acid precursors in rat hippocampal neurons. J. Neurochem. 105 (2008) 1525-1535
48. Cunnane S.C., Plourde M., Stewart K., and Crawford M.A. Docosahexaenoic acid and shore-based diets in hominin encephalization: a rebuttal. Am. J. Hum. Biol. 19 (2007) 578-581
49. Urano S., Sato Y., Otonari T., Makabe S., Suzuki S., Ogata M., and Endo T. Aging and oxidative stress in neurodegeneration. Biofactors 7 (1998) 103-112
50. Petursdottir A.L., Farr S.A., Morley J.E., Banks W.A., and Skuladottir G.V. Effect of dietary n-3 polyunsaturated fatty acids on brain lipid fatty acid composition, learning ability, and memory of senescence-accelerated mouse. J. Gerontol. A Biol. Sci. Med. Sci. 63 (2008) 1153-1160
51. Kalmijn S., van Boxtel M.P., Ocké M., Verschuren W.M., Kromhout D., and Launer L.J. Dietary intake of fatty acids and fish in relation to cognitive performance at middle age. Neurology 62 (2004) 275-280
52. Morris M.C., Evans D.A., Tangney C.C., Bienias J.L., and Wilson R.S. Fish consumption/ intake and cognitive decline with age in a large community study. Arch. Neurol. 62 (2005) 1849-1853
53. Calon F., and Cole G. Neuroprotective action of ω-3 polyunsaturated fatty acids against neurodegenerative diseases: evidence from animal studies. Prostaglandins Leukot. Essent. Fatty Acids 77 (2007) 287-293
54. Conquer J.A., Tierney M.C., Zecevic J., Bettger W.J., and Fisher R.H. Fatty acid analysis of blood plasma of patients with Alzheimer's disease, other types of dementia, and cognitive impairment. Lipids 35 (2000) 1305-1312
55. Söderberg M., Edlund C., Alafuzoff I., Kristensson K., and Dallner G. Lipid composition in different regions of the brain in Alzheimer's disease/senile dementia of Alzheimer's type. J. Neurochem. 59 (1992) 1646-1653
56. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., Rostaing P., Triller A., Salem Jr. N., Ashe K.H., Frautschy S.A., and Cole G.M. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43 (2004) 633-645
57. Yao J.K., Wengenack T.M., Curran G.L., and Poduslo J.F. Reduced membrane lipids in the cortex of Alzheimer's disease transgenic mice. Neurochem. Res. 34 (2009) 102-108
58. Jiang L.H., Shi Y., Wang L.S., and Yang Z.R. The influence of orally administered docosahexaenoic acid on cognitive ability in aged mice. J. Nutr. Biochem. 20 (2009) 735-741
59. Martin D.S., Spencer P., Horrobin D.F., and Lynch M.A. 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 67 (2002) 121-130
60. Ikemoto A., Ohishi M., Sato Y., Hata N., Misawa Y., Fujii Y., and Okuyama H. Reversibility of n-3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n-6 fatty acids as another critical factor. J. Lipid Res. 42 (2001) 1655-1663
61. Connor W.E., Neuringer M., and 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. 31 (1990) 237-247
62. Hashimoto M., Hossain S., Agdul H., and Shido O. Docosahexaenoic acid-induced amelioration on impairment of memory learning in amyloid β-infused rats relates to the decreases of amyloid β and cholesterol levels in detergent-insoluble membrane fractions. Biochim. Biophys. Acta 1738 (2005) 91-98
63. Lim G.P., Calon F., Morihara T., Yang F., Teter B., Ubeda O., Salem Jr. N., Frautschy S.A., and Cole G.M. A diet enriched with the ω3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J. Neurosci. 25 (2005) 3032-3040
64. Hashimoto M., Hossain S., Shimada T., and Shido O. Docosahexaenoic acid-induced protective effect against impaired learning in amyloid β-infused rats is associated with increased synaptosomal membrane fluidity. Clin. Exp. Pharmacol. Physiol. 33 (2006) 934-939
65. Wassall S.R., and Stillwell W. Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes. Biochim. Biophys. Acta 1788 (2009) 24-32
66. Little S.J., Lynch M.A., Manku M., and Nicolaou A. Docosahexaenoic acid-induced changes in phospholipids in cortex of young and aged rats: a lipidomic analyses. Prostaglandins Leukot. Essent. Fatty Acids 77 (2007) 155-162
67. 2 in releasing docosahexaenoic acid from brain phospholipids. J. Lipid Res. 49 (2008) 939-944
68. 2-mediated fatty acid release from brain phospholipids. Biochim. Biophys. Acta 1791 (2009) 697-705
69. Niemoller T.D., and Bazan N.G. Docosahexaenoic acid neurolipidomics. Prostaglandins Other Lipid Mediat. 91 (2010) 85-89
70. Itoh T., and Yamamoto K. Peroxisome proliferator activated receptor γ and oxidized docosahexaenoic acids as new class of ligand. Naunyn Schmiedebergs Arch. Pharmacol. 377 (2008) 541-547
71. Lengqvist J., Mata De Urquiza A., Bergman A.C., Willson T.M., Sjövall J., Perlmann T., and Griffiths W.J. Polyunsaturated fatty acids including docosahexaenoic and arachidonic acid bind to the retinoid X receptor α ligand-binding domain. Mol. Cell. Proteomics 3 (2004) 692-703
72. Puskás L.G., and Kitajka K. Nutrigenomic approaches to study the effects of n-3 PUFA diet in the central nervous system. Nutr. Health 18 (2006) 227-232
73. Hashimoto M., Hossain S., Tanabe Y., Kawashima A., Harada T., Yano T., Mizuguchi K., and Shido O. The protective effect of dietary eicosapentaenoic acid against impairment of spatial cognition learning ability in rats infused with amyloid β(1-40). J. Nutr. Biochem. 20 (2009) 965-973
74. He C., Qu X., Cui L., Wang J., and Kang J.X. Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 11370-11375
75. Sakamoto T., Cansev M., and Wurtman R.J. Oral supplementation with docosahexaenoic acid and uridine-5'-monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res. 1182 (2007) 50-59
76. Cansev M., and Wurtman R.J. 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 148 (2007) 421-431
77. Scheltens P., Kamphuis P.J., Verhey F.R., Olde Rikkert M.G., Wurtman R.J., Wilkinson D., Twisk J.W., and Kurz A. Efficacy of a medical food in mild Alzheimer's disease: a randomized, controlled trial. Alzheimers Demen. 6 (2010) 1-10
78. Freund-Levi Y., Eriksdotter-Jönhagen M., Cederholm T., Basun H., Faxén-Irving G., Garlind A., Vedin I., Vessby B., Wahlund L.O., and Palmblad J. Omega-3 fatty acid treatment in 174 patients with mild to moderate Alzheimer disease: OmegAD study: a randomized double-blind trial. Arch. Neurol. 63 (2006) 1402-1408
79. Green K.N., Martinez-Coria H., Khashwji H., Hall E.B., Yurko-Mauro K.A., Ellis L., and LaFerla F.M. Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-β and tau pathology via a mechanism involving presenilin 1 levels. Neurobiol. Dis. 27 (2007) 4385-4395
80. Arendash G.W., Jensen M.T., Salem Jr. N., Hussein N., Cracchiolo J., Dickson A., Leighty R., and Potter H. A diet high in omega-3 fatty acids does not improve or protect cognitive performance in Alzheimer's transgenic mice. Neuroscience 149 (2007) 286-302
81. Sahlin C., Pettersson F.E., Nilsson L.N., Lannfelt L., and Johansson A.S. Docosahexaenoic acid stimulates non-amyloidogenic APP processing resulting in reduced Aβ levels in cellular models of Alzheimer's disease. Eur. J. NeuroSci. 26 (2007) 882-889
82. Ma Q.L., Teter B., Ubeda O.J., Morihara T., Dhoot D., Nyby M.D., Tuck M.L., Frautschy S.A., and 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. 27 (2007) 14299-14307
83. Ma Q.L., Galasko D.R., Ringman J.M., Vinters H.V., Edland S.D., Pomakian J., Ubeda O.J., Rosario E.R., Teter B., Frautschy S.A., and Cole G.M. Reduction of SorLA/LR11, a sorting protein limiting β-amyloid production, in Alzheimer disease cerebrospinal fluid. Arch. Neurol. 66 (2009) 448-457
84. Rogaeva E., Meng Y., Lee J.H., Gu Y., Kawarai T., Zou F., Katayama T., Baldwin C.T., Cheng R., Hasegawa H., Chen F., Shibata N., Lunetta K.L., Pardossi-Piquard R., Bohm C., Wakutani Y., Cupples L.A., Cuenco K.T., Green R.C., Pinessi L., Rainero I., Sorbi S., Bruni A., Duara R., Friedland R.P., Inzelberg R., Hampe W., Bujo H., Song Y.Q., Andersen O.M., Willnow T.E., Graff-Radford N., Petersen R.C., Dickson D., Der S.D., Fraser P.E., Schmitt-Ulms G., Younkin S., Mayeux R., Farrer L.A., and St George-Hyslop P. The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat. Genet. 39 (2007) 168-177
85. Oda A., Tamaoka A., and Araki W. Oxidative stress up-regulates presenilin 1 in lipid rafts in neuronal cells. J. Neurosci. Res. 88 (2010) 1137-1145
86. Puskás L.G., Kitajka K., Nyakas C., Barcelo-Coblijn G., and 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. 100 (2003) 1580-1585
87. Kalinin S., Richardson J.C., and Feinstein D.L. A PPARdelta agonist reduces amyloid burden and brain inflammation in a transgenic mouse model of Alzheimer's disease. Curr. Alzheimer Res. 6 (2009) 431-437
88. Hooijmans C.R., Van der Zee C.E., Dederen P.J., Brouwer K.M., Reijmer Y.D., van Groen T., Broersen L.M., Lütjohann D., Heerschap A., and Kiliaan A.J. DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol. Dis. 33 (2009) 482-498
89. Hossain S., Hashimoto M., Katakura M., Miwa K., Shimada T., and Shido O. Mechanism of docosahexaenoic acid-induced inhibition of in vitro Aβ1-42 fibrillation and Aβ1-42-induced toxicity in SH-S5Y5 cells. J. Neurochem. 111 (2009) 568-579
90. Johansson A.S., Garlind A., Berglind-Dehlin F., Karlsson G., Edwards K., Gellerfors P., Ekholm-Pettersson F., Palmblad J., and Lannfelt L. Docosahexaenoic acid stabilizes soluble amyloid-β protofibrils and sustains amyloid-β-induced neurotoxicity in vitro. FEBS J. 274 (2007) 990-1000
91. Bate C., Marshall V., Colombo L., Diomede L., Salmona M., and Williams A. Docosahexaenoic and eicosapentaenoic acids increase neuronal death in response to HuPrP82-146 and Aβ 1-42. Neuropharmacology 54 (2008) 934-943
92. Sponne I., Fifre A., Koziel V., Oster T., Olivier J.L., and Pillot T. Membrane cholesterol interferes with neuronal apoptosis induced by soluble oligomers but not fibrils of amyloid-β peptide. FASEB J. 18 (2004) 836-838
93. Abad-Rodriguez J., Ledesma M.D., Craessaerts K., Perga S., Medina M., Delacourte A., Dingwall C., De Strooper B., and Dotti C.G. Neuronal membrane cholesterol loss enhances amyloid peptide generation. J. Cell Biol. 167 (2004) 953-960
94. Guo M., Stockert L., Akbar M., and Kim H.Y. Neuronal specific increase of phosphatidylserine by docosahexaenoic acid. J. Mol. Neurosci. 33 (2007) 67-73
95. Akbar M., Calderon F., Wen Z., and Kim H.Y. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 10858-10863
96. Nassif M., Hoppe J., Santin K., Frozza R., Zamin L.L., Simão F., Horn A.P., and Salbego C. β-Amyloid peptide toxicity in organotypic hippocampal slice culture involves Akt/PKB, GSK-3β, and PTEN. Neurochem. Int. 50 (2007) 229-235
97. Rao J.S., Ertley R.N., Lee H.J., DeMar Jr. J.C., Arnold J.T., Rapoport S.I., and Bazinet R.P. n-3 polyunsaturated fatty acid deprivation in rats decreases frontal cortex BDNF via a p38 MAPK-dependent mechanism. Mol. Psychiatry 12 (2007) 36-46
98. Pomponi M., Di Gioia A., Bria P., and Pomponi M.F. Fatty aspirin: a new perspective in the prevention of dementia of Alzheimer's type?. Curr. Alzheimer Res. 5 (2008) 422-431
99. Kawakita E., Hashimoto M., and Shido O. Docosahexaenoic acid promotes neurogenesis in vitro and in vivo. Neuroscience 139 (2006) 991-997
100. Islam O., Loo T.X., and Heese K. Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor, MAP kinase, AKT, and STAT-3 signaling pathways. Curr. Neurovasc. Res. 6 (2009) 42-53
101. Oksman M., Iivonen H., Hogyes E., Amtul A., Penke B., Leenders I., Broersen L., Lütjohann D., Hartmann T., and Tanila H. Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on β-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol. Dis. 23 (2006) 563-572
102. Florent-Béchard S., Malaplate-Armand C., Koziel V., Kriem B., Olivier J.L., Pillot T., and Oster T. Towards a nutritional approach for prevention of Alzheimer's disease: biochemical and cellular aspects. J. Neurol. Sci. 262 (2007) 27-36