Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model

Neuron

Volumn 43, Issue 5, 2004, Pages 633-645

  Calon, Frédéric ^a,c   Lim, Giselle P ^a,c   Yang, Fusheng ^a,c   Morihara, Takashi ^a,c   Teter, Bruce ^a,c   Ubeda, Oliver ^a,c   Rostaing, Phillippe ^d   Triller, Antoine ^d   Salem Jr , Norman ^e   Ashe, Karen H ^f   Frautschy, Sally A ^a,b,c   Cole, Greg M ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d INSERM   (France)

^e Division of Intramural Research   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DOCOSAHEXAENOIC ACID; DREBRIN; PHOSPHATIDYLINOSITOL 3 KINASE; POLYUNSATURATED FATTY ACID;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DIET RESTRICTION; ENZYME SUBUNIT; FEMALE; HUMAN; HUMAN TISSUE; MALE; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; BRAIN; CARRIER PROTEINS; DENDRITES; DIETARY FATS, UNSATURATED; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; DOWN-REGULATION; FEMALE; FOOD, FORMULATED; HUMANS; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; NEUROPEPTIDES; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN SUBUNITS; SYNAPSES;

EID: 4444223956     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2004.08.013     Document Type: Article

References (81)

1. Akbar M., Kim H.Y. Protective effects of docosahexaenoic acid in staurosporine-induced apoptosis. involvement of phosphatidylinositol-3 kinase pathway J. Neurochem. 82:2002;655-665
2. Aksenov M.Y., Aksenova M.V., Butterfield D.A., Geddes J.W., Markesbery W.R. Protein oxidation in the brain in Alzheimer's disease. Neuroscience. 103:2001;373-383
3. Attwell D., Iadecola C. The neural basis of functional brain imaging signals. Trends Neurosci. 25:2002;621-625
4. Barberger-Gateau P., Letenneur L., Deschamps V., Peres K., Dartigues J.F., Renaud S. Fish, meat, and risk of dementia. cohort study BMJ. 325:2002;932-933
5. Bazan N.G. Synaptic lipid signaling. significance of polyunsaturated fatty acids and platelet-activating factor J. Lipid Res. 44:2003;2221-2233
6. Behl C., Davis J.B., Lesley R., Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell. 77:1994;817-827
7. Borchelt D.R., Ratovitski T., van Lare J., Lee M.K., Gonzales V., Jenkins N.A., Copeland N.G., Price D.L., Sisodia S.S. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron. 19:1997;939-945
8. Breckenridge W.C., Gombos G., Morgan I.G. The lipid composition of adult rat brain synaptosomal plasma membranes. Biochim. Biophys. Acta. 266:1972;695-707
9. Butterfield D.A., Castegna A., Lauderback C.M., Drake J. Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol. Aging. 23:2002;655-664
10. Callahan L.M., Vaules W.A., Coleman P.D. Quantitative decrease in synaptophysin message expression and increase in cathepsin D message expression in Alzheimer disease neurons containing neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 58:1999;275-287
11. Cole G.M., Yang F., Chen P.P., Frautschy S., Hsiao K. Caspase activation in dystrophic neurites in Alzheimer's disease and aged HuAPPsw transgenic mice. Iqbal K., Swaab D.F., Winblad B., Wisniewski H.M. Alzheimer's Disease and Related Disorders. 1999;363-369 Wiley, Chichester, UK
12. Conquer J.A., Tierney M.C., Zecevic J., Bettger W.J., 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
13. Dalle-Donne I., Rossi R., Giustarini D., Gagliano N., Di Simplicio P., Colombo R., Milzani A. Methionine oxidation as a major cause of the functional impairment of oxidized actin. Free Radic. Biol. Med. 32:2002;927-937
14. Datta S.R., Katsov A., Hu L., Petros A., Fesik S.W., Yaffe M.B., Greenberg M.E. 14-3-3 proteins and survival kinases cooperate to inactivate BAD by BH3 domain phosphorylation. Mol. Cell. 6:2000;41-51
15. Dickey C.A., Loring J.F., Montgomery J., Gordon M.N., Eastman P.S., Morgan D. Selectively reduced expression of synaptic plasticity-related genes in amyloid precursor protein + presenilin-1 transgenic mice. J. Neurosci. 23:2003;5219-5226
16. Dineley K.T., Xia X., Bui D., Sweatt J.D., Zheng H. Accelerated plaque accumulation, associative learning deficits, and up-regulation of alpha 7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J. Biol. Chem. 277:2002;22768-22780
17. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science. 290:2000;1364-1368
18. Etminan M., Gill S., Samii A. Effect of non-steroidal anti-inflammatory drugs on risk of Alzheimer's disease. systematic review and meta-analysis of observational studies BMJ. 327:2003;128
19. Everall I.P., DeTeresa R., Terry R., Masliah E. Comparison of two quantitative methods for the evaluation of neuronal number in the frontal cortex in Alzheimer disease. J. Neuropathol. Exp. Neurol. 56:1997;1202-1206
20. Favrelere S., Stadelmann-Ingrand S., Huguet F., De Javel D., Piriou A., Tallineau C., Durand G. Age-related changes in ethanolamine glycerophospholipid fatty acid levels in rat frontal cortex and hippocampus. Neurobiol. Aging. 21:2000;653-660
21. Fukazawa Y., Saitoh Y., Ozawa F., Ohta Y., Mizuno K., Inokuchi K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron. 38:2003;447-460
22. Gamblin T.C., King M.E., Kuret J., Berry R.W., Binder L.I. Oxidative regulation of fatty acid-induced tau polymerization. Biochemistry. 39:2000;14203-14210
23. Gong Y., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., Krafft G.A., Klein W.L. Alzheimer's disease-affected brain. Presence of oligomeric A{beta} ligands (ADDLs) suggests a molecular basis for reversible memory loss Proc. Natl. Acad. Sci. USA. 100:2003;10417-10422
24. Grant W.B., Campbell A., Itzhaki R.F., Savory J. The significance of environmental factors in the etiology of Alzheimer's disease. J. Alzheimers Dis. 4:2002;179-189
25. Guan Z., Wang Y., Cairns N.J., Lantos P.L., Dallner G., Sindelar P.J. Decrease and structural modifications of phosphatidylethanolamine plasmalogen in the brain with Alzheimer disease. J. Neuropathol. Exp. Neurol. 58:1999;740-747
26. Harigaya Y., Shoji M., Shirao T., Hirai S. Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J. Neurosci. Res. 43:1996;87-92
27. Hashimoto M., Hossain S., Shimada T., Sugioka K., Yamasaki H., Fujii Y., Ishibashi Y., Oka J., Shido O. Docosahexaenoic acid provides protection from impairment of learning ability in Alzheimer's disease model rats. J. Neurochem. 81:2002;1084-1091
28. Hatanpaa K., Isaacs K.R., Shirao T., Brady D.R., Rapoport S.I. Loss of proteins regulating synaptic plasticity in normal aging of the human brain and in Alzheimer disease. J. Neuropathol. Exp. Neurol. 58:1999;637-643
29. Holcomb L., Gordon M.N., McGowan E., Yu X., Benkovic S., Jantzen P., Wright K., Saad I., Mueller R., Morgan D., et al. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med. 4:1998;97-100
30. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science. 274:1996;99-102
31. Husi H., Ward M.A., Choudhary J.S., Blackstock W.P., Grant S.G. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3:2000;661-669
32. Irizarry M.C., McNamara M., Fedorchak K., Hsiao K., Hyman B.T. APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J. Neuropathol. Exp. Neurol. 56:1997;965-973
33. Jolles J., Bothmer J., Markerink M., Ravid R. Phosphatidylinositol kinase is reduced in Alzheimer's disease. J. Neurochem. 58:1992;2326-2329
34. Joseph J.A., Denisova N.A., Arendash G., Gordon M., Diamond D., Shukitt-Hale B., Morgan D. Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr. Neurosci. 6:2003;153-162
35. Kihara T., Shimohama S., Sawada H., Honda K., Nakamizo T., Shibasaki H., Kume T., Akaike A. alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity. J. Biol. Chem. 276:2001;13541-13546
36. King D.L., Arendash G.W. Maintained synaptophysin immunoreactivity in Tg2576 transgenic mice during aging. correlations with cognitive impairment Brain Res. 926:2002;58-68
37. Krishnan S., Chi E.Y., Wood S.J., Kendrick B.S., Li C., Garzon-Rodriguez W., Wypych J., Randolph T.W., Narhi L.O., Biere A.L., et al. Oxidative dimer formation is the critical rate-limiting step for Parkinson's disease alpha-synuclein fibrillogenesis. Biochemistry. 42:2003;829-837
38. Kyle D.J., Schaefer E., Patton G., Beiser A. Low serum docosahexaenoic acid is a significant risk factor for Alzheimer's dementia. Lipids. 34:1999;S245
39. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA. 95:1998;6448-6453
40. Lim G.P., Chu T., Yang F., Beech W., Frautschy S.A., Cole G.M. The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J. Neurosci. 21:2001;8370-8377
41. Liolitsa D., Powell J., Lovestone S. Genetic variability in the insulin signalling pathway may contribute to the risk of late onset Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry. 73:2002;261-266
42. Mattson M.P., Duan W. Apoptotic biochemical cascades in synaptic compartments. roles in adaptive plasticity and neurodegenerative disorders J. Neurosci. Res. 58:1999;152-166
43. Matus A. Actin-based plasticity in dendritic spines. Science. 290:2000;754-758
44. Migaud M., Charlesworth P., Dempster M., Webster L.C., Watabe A.M., Makhinson M., He Y., Ramsay M.F., Morris R.G., Morrison J.H., et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 396:1998;433-439
45. Montine K.S., Quinn J.F., Zhang J., Fessel J.P., Roberts L.J. 2nd, Morrow J.D., Montine T.J. Isoprostanes and related products of lipid peroxidation in neurodegenerative diseases. Chem. Phys. Lipids. 128:2004;117-124
46. Moriguchi T., Greiner R.S., Salem N. Jr. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 75:2000;2563-2573
47. Morris M.C., Evans D.A., Bienias J.L., Tangney C.C., Bennett D.A., Wilson R.S., Aggarwal N., Schneider J. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch. Neurol. 60:2003;940-946
48. Nagele R.G., D'Andrea M.R., Anderson W.J., Wang H.Y. Intracellular accumulation of beta-amyloid(1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer's disease. Neuroscience. 110:2002;199-211
49. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles. Intracellular abeta and synaptic dysfunction. Neuron. 39:2003;409-421
50. Okabe S., Miwa A., Okado H. Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J. Neurosci. 21:2001;6105-6114
51. Opazo P., Watabe A.M., Grant S.G., O'Dell T.J. Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J. Neurosci. 23:2003;3679-3688
52. Pratico D., Uryu K., Leight S., Trojanoswki J.Q., Lee V.M. Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci. 21:2001;4183-4187
53. Ramakers G.J. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 25:2002;191-199
54. Rossiter J.P., Anderson L.L., Yang F., Cole G.M. Caspase-cleaved actin (fractin) immunolabelling of Hirano bodies. Neuropathol. Appl. Neurobiol. 26:2000;342-346
55. Saji, M., Akiba, L., Tanaka, S., Suzuki, N., Sekino, Y., and Shirao, T. (2002). Impaired spatial learning and intact adaptation in rats with antisense hippocampal knockdown of drebrin A. Paper presented at: Society for Neuroscience meeting.
56. Salem N. Jr., Litman B., Kim H.Y., Gawrisch K. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids. 36:2001;945-959
57. Schurmann A., Mooney A.F., Sanders L.C., Sells M.A., Wang H.G., Reed J.C., Bokoch G.M. p21-activated kinase 1 phosphorylates the death agonist bad and protects cells from apoptosis. Mol. Cell. Biol. 20:2000;453-461
58. Selkoe D.J. Alzheimer's disease. genes, proteins, and therapy Physiol. Rev. 81:2001;741-766
59. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science. 298:2002;789-791
60. Shaw S., Bencherif M., Marrero M.B. Janus kinase 2, an early target of alpha 7 nicotinic acetylcholine receptor-mediated neuroprotection against Abeta-(1-42) amyloid. J. Biol. Chem. 277:2002;44920-44924
61. Shim K.S., Lubec G. Drebrin, a dendritic spine protein, is manifold decreased in brains of patients with Alzheimer's disease and Down syndrome. Neurosci. Lett. 324:2002;209-212
62. Shirao T., Sekino Y. Clustering and anchoring mechanisms of molecular constituents of postsynaptic scaffolds in dendritic spines. Neurosci. Res. 40:2001;1-7
63. Shirazi S.K., Wood J.G. The protein tyrosine kinase, fyn, in Alzheimer's disease pathology. Neuroreport. 4:1993;435-437
64. Shoop R.D., Yamada N., Berg D.K. Cytoskeletal links of neuronal acetylcholine receptors containing alpha 7 subunits. J. Neurosci. 20:2000;4021-4029
65. Star E.N., Kwiatkowski D.J., Murthy V.N. Rapid turnover of actin in dendritic spines and its regulation by activity. Nat. Neurosci. 5:2002;239-246
66. Stein T.D., Johnson J.A. Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J. Neurosci. 22:2002;7380-7388
67. Suh Y.H., Checler F. Amyloid precursor protein, presenilins, and alpha-synuclein. molecular pathogenesis and pharmacological applications in Alzheimer's disease Pharmacol. Rev. 54:2002;469-525
68. Takahashi R.H., Milner T.A., Li F., Nam E.E., Edgar M.A., Yamaguchi H., Beal M.F., Xu H., Greengard P., Gouras G.K. Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am. J. Pathol. 161:2002;1869-1879
69. Takahashi H., Sekino Y., Tanaka S., Mizui T., Kishi S., Shirao T. Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J. Neurosci. 23:2003;6586-6595
70. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K., Imahori K. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci. Lett. 203:1996;33-36
71. Taouis M., Dagou C., Ster C., Durand G., Pinault M., Delarue J. N-3 polyunsaturated fatty acids prevent the defect of insulin receptor signaling in muscle. Am. J. Physiol. Endocrinol. Metab. 282:2002;E664-E671
72. Taubes G. Neuroscience. Insulin insults may spur Alzheimer's disease. Science. 301:2003;40-41
73. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer's disease. synapse loss is the major correlate of cognitive impairment Ann. Neurol. 30:1991;572-580
74. Tully A.M., Roche H.M., Doyle R., Fallon C., Bruce I., Lawlor B., Coakley D., Gibney M.J. Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer's disease. a case-control study Br. J. Nutr. 89:2003;483-490
75. Westerman M.A., Cooper-Blacketer D., Mariash A., Kotilinek L., Kawarabayashi T., Younkin L.H., Carlson G.A., Younkin S.G., Ashe K.H. The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer's disease. J. Neurosci. 22:2002;1858-1867
76. Yang F., Sun X., Beech W., Teter B., Wu S., Sigel J., Vinters H.V., Frautschy S.A., Cole G.M. Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer's disease. Am. J. Pathol. 152:1998;379-389
77. Yavin E., Brand A., Green P. Docosahexaenoic acid abundance in the brain. a biodevice to combat oxidative stress Nutr. Neurosci. 5:2002;149-157
78. Yehuda S., Rabinovitz S., Carasso R.L., Mostofsky D.I. The role of polyunsaturated fatty acids in restoring the aging neuronal membrane. Neurobiol. Aging. 23:2002;843-853
79. Youdim K.A., Martin A., Joseph J.A. Essential fatty acids and the brain. possible health implications Int. J. Dev. Neurosci. 18:2000;383-399
80. Yuan J., Yankner B.A. Apoptosis in the nervous system. Nature. 407:2000;802-809
81. Zubenko G.S., Stiffler J.S., Hughes H.B., Martinez A.J. Reductions in brain phosphatidylinositol kinase activities in Alzheimer's disease. Biol. Psychiatry. 45:1999;731-736