Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease

Nature Neuroscience

Volumn 9, Issue 2, 2006, Pages 234-242

  Zhao, Lixia ^a,b   Ma, Qiu Lan ^a,b   Calon, Frédéric ^c,d   Harris White, Marni E ^a,b,e   Yang, Fusheng ^a,b   Lim, Giselle P ^a,b   Morihara, Takashi ^f   Ubeda, Oliver J ^a,b   Ambegaokar, Surendra ^a,b   Hansen, James E ^a,b   Weisbart, Richard H ^a,b   Teter, Bruce ^a,b,e   Frautschy, Sally A ^a,b,e,g   Cole, Greg M ^a,b,e,g  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAVAL UNIVERSITY   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

^e GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^f OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA SECRETASE; COFILIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; DREBRIN; OLIGOMER; REGULATOR PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DNA FLANKING REGION; ENZYME ACTIVITY; HIPPOCAMPUS; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ACTIN DEPOLYMERIZING FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; CELLS, CULTURED; COGNITION DISORDERS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; NEUROPEPTIDES; PROTEIN-SERINE-THREONINE KINASES; RATS;

EID: 31544476561     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1630     Document Type: Article

References (50)

1. Purpura, D.P. Dendritic spine "dysgenesis" and mental retardation. Science 186, 1126-1128 (1974).
2. Ferrer, I. & Gullotta, F. Down's syndrome and Alzheimer's disease: dendritic spine counts in the hippocampus. Acta Neuropathol. (Berl.) 79, 680-685 (1990).
3. Blanpied, T.A. & Ehlers, M.D. Microanatomy of dendritic spines: emerging principles of synaptic pathology in psychiatric and neurological disease. Biol. Psychiatry 55, 1121-1127 (2004).
4. Selkoe, D.J. Alzheimer's disease is a synaptic failure. Science 298, 789-791 (2002).
5. Moolman, D.L., Vitolo, O.V., Vonsattel, J.P. & Shelanski, M.L. Dendrite and dendritic spine alterations in Alzheimer models. J. Neurocytol. 33, 377-387 (2004).
6. Coleman, P., Federoff, H. & Kurlan, R. A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 63, 1155-1162 (2004).
7. Wisniewski, K.E., Wisniewski, H.M. & Wen, G.Y. Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome. Ann. Neurol. 17, 278-282 (1985).
8. Fiala, J.C., Spacek, J. & Harris, K.M. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res. Brain Res. Rev. 39, 29-54 (2002).
9. Ramakers, G.J. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 25, 191-199 (2002).
10. Bienvenu, T. et al. Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am. J. Med. Genet. 93, 294-298 (2000).
11. Allen, K.M. et al. PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 20, 25-30 (1998).
12. Hayashi, M.L. et al. Altered cortical synaptic morphology and impaired memory consolidation in forebrain- specific dominant-negative PAK transgenic mice. Neuron 42, 773-787 (2004).
13. Meng, Y. et al. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35, 121-133 (2002).
14. Ong, W. Y., Wang, X.S. & Manser, E. Differential distribution of alpha and beta isoforms of p21-activated kinase in the monkey cerebral neocortex and hippocampus. Exp. Brain Res. 144, 189-199 (2002).
15. Simic, G., Kostovic, I., Winblad, B. & Bogdanovic, N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 379, 482-494 (1997).
16. 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, 87-92 (1996).
17. Calon, F. et al. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43, 633-645 (2004).
18. 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, 209-212 (2002).
19. 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, 637-643 (1999).
20. Hayashi, K. et al. Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J. Neurosci. 16, 7161-7170 (1996).
21. Takahashi, H. et al. Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J. Neurosci. 23, 6586-6595 (2003).
22. Aoki, C. et al. Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J. Comp. Neurol. 483, 383-402 (2005).
23. Lacor, P.N. et al. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J. Neurosci. 24, 10191-10200 (2004).
24. Janz, R. et al. Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24, 687-700 (1999).
25. Chelly, J. & Mandel, J.L. Monogenic causes of X-linked mental retardation. Nat. Rev. Genet. 2, 669-680 (2001).
26. Gedeon, A.K., Nelson, J., Gecz, J. & Mulley, J.C. X-linked mild non-syndromic mental retardation with neuropsychiatric problems and the missense mutation A365E in PAK3. Am. J. Med. Genet. A 120, 509-517 (2003).
27. Chong, C., Tan, L., Lim, L. & Manser, E. The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J. Biol. Chem. 276, 17347-17353 (2001).
28. Singh, R.R., Song, C., Yang, Z. & Kumar, R. Nuclear localization and chromatin targets of p21-activated kinase 1. J. Biol. Chem. 280, 18130-18137 (2005).
29. Yang, A.J., Knauer, M., Burdick, D.A. & Glabe, C. Intracellular Aβ1-42 aggregates stimulate the accumulation of stable, insoluble amyloidogenic fragments of the amyloid precursor protein in transfected cells. J. Biol. Chem. 270, 14786-14792 (1995).
30. Cataldo, A.M. et al. Abeta localization in abnormal endosomes: association with earliest Abeta elevations in AD and Down syndrome. Neurobiol. Aging 25, 1263-1272 (2004).
31. McPhie, D.L. et al. DNA synthesis and neuronal apoptosis caused by familial Alzheimer disease mutants of the amyloid precursor protein are mediated by the p21 activated kinase PAK3. J. Neurosci. 23, 6914-6927 (2003).
32. Ichetovkin, I., Han, J., Pang, K.M., Knecht, D.A. & Condeelis, J.S. Actin filaments are severed by both native and recombinant dictyostelium cofilin but to different extents. Cell Motil. Cytoskeleton 45, 293-306 (2000).
33. Yang, N. et al. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated act in reorganization. Nature 393, 809-812 (1998).
34. Arber, S. et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805-809 (1998).
35. Mitake, S., Ojika, K. & Hirano, A. Hirano bodies and Alzheimer's disease. Kaohsiung J. Med. Sci. 13, 10-18 (1997).
36. Bamburg, J.R. & Wiggan, O.P. ADF/cofilin and actin dynamics in disease. Trends Cell Biol. 12, 598-605 (2002).
37. Minamide, L.S., Striegl, A.M., Boyle, J.A., Meberg, P.J. & Bamburg, J.R. Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell Biol. 2, 628-636 (2000).
38. Lappalainen, P., Kessels, M.M., Cope, M.J. & Drubin, D.G. The ADF homology (ADF-H) domain: a highly exploited actin-binding module. Mol. Biol. Cell 9, 1951-1959 (1998).
39. McGough, A., Pope, B., Chiu, W. & Weeds, A. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138, 771-781 (1997).
40. Morgan, D. et al. Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408, 982-985 (2000).
41. Kotilinek, L. A. et al. Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J. Neurosci. 22, 6331-6335 (2002).
42. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003).
43. Kuo, Y.M. et al. Water-soluble Aβ (N-40.N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 271, 4077-4081 (1996).
44. Frautschy, S.A. et al. Phenolic anti-inflammatory antioxidant reversal of Aβ-induced cognitive deficits and neuropathology. Neurobiol. Aging 22, 993-1005 (2001).
45. Maruta, H., He, H. & Nheu, T. Interfering with Ras signaling using membrane-permeable peptides or drugs. Methods Mol. Biol. 189, 75-85 (2002).
46. Rossiter, J.P., Anderson, L.L., Yang, F. & Cole, G.M. Caspase-cleaved actin (fractin) immunolabelliing of Hirano bodies. Neuropathol. Appl. Neurobiol. 26, 342-346 (2000).
47. Kogan, J.H., Frankland, P.W. & Silva, A.J. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10, 47-56 (2000).
48. Yang, F. et al. Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and neurons and plaque associated neurons and microglia in Alzheimer's disease. Am. J. Pathol. 152, 379-389 (1998).
49. Zhao, L. et al. Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer's disease intervention. J. Neurosci. 24, 11120-11126 (2004).
50. Ma, Q.-L. et al. Antibodies against β-amyloid rapidly neutralize Aβ oligomers and inhibit GSK-3β activation and tau phosphorylation in vivo and in vitro. J. Neurosci. Res. 83 (2005) (in the press).