Differential loss of synaptic proteins in Alzheimer's disease: Implications for synaptic dysfunction

Journal of Alzheimer's Disease

Volumn 7, Issue 2, 2005, Pages 103-117

  Reddy, P Hemachandra ^a   Mani, Geethalakshmi ^a   Park, Byung S ^a   Jacques, Joline ^a   Murdoch, Geoffrey ^b   Whetsell Jr , William ^c   Kaye, Jeffrey ^b   Manczak, Maria ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Cognitive decline; Synaptic protein; Synaptophysin; Synaptopodin

Indexed keywords

NEUROGRANIN; NEUROMODULIN; RAB PROTEIN; SYNAPTOBREVIN; SYNAPTOPHYSIN; SYNAPTOPODIN; SYNAPTOTAGMIN;

ADULT; AGE DISTRIBUTION; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN NERVE CELL; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE VESICLE;

EID: 17844378691     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2005-7203     Document Type: Article

References (71)

1. S.E. Ahmari, J. Buchanan and S.J. Smith, Assembly of presynaptic active zones from cytoplasmic transport packets, Nature Neuroscience. 3 (2000), 445-451.
2. M.J. Ball, M. Fisman, V. Hachinski, W. Blume, A. Fox, V.A. Kral, A.J. Kirshen, H. Fox and H. Merskey, A new definition of Alzheimer's disease: a hippocampal dementia, Lancet 1 (1985), 14-16.
3. G.S. Basi, R.D. Jacobson, I. Virag, J. Schilling and J.H. Skene, Primary structure and transcriptional regulation of GAP-43, a protein associated with nerve growth, Cell 49 (1987), 785-791.
4. M. Baumert, P.R. Maycox, F. Navone, P. De Camilli and R. Jahnm Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain, EMBO Journal 8 (1989), 379-384.
5. L.I. Benowitz, V.E. Shashoua and M.G. Yoon, Specific changes in rapidly transported proteins during regeneration of the goldfish optic nerve, Journal of Neuroscience 1 (1981), 300-307.
6. L.I. Benowitz, W. Rodriguez, P. Paskevich, E.J. Mufson, D. Schenk and R.L. Neve, The amyloid precursor protein is concentrated in neuronal lysosomes ??? in normal and Alzheimer disease subjects, Experimental Neurology 106 (1989), 237-250.
7. K. Blennow, N. Bogdanovic, I. Alafuzoff, R. Ekman and P. Davidsson, Synaptic pathology in Alzheimer's disease: relation to severity of dementia, but not to senile plaques, neurofibrillary tangles, or the ApoE4 allele, Journal of Neural Transmission 103 (1996), 603-618.
8. N. Bogdanovic, P. Davidsson, N. Volkmann, B. Winblad and K. Blennow, Growth associated protein GAP-43 in the frontal cortex and in the hippocampus in Alzheimer's disease: an Immunohistochemical and quantitative study, Journal of Neural Transmission 107 (2000), 463-478.
9. H. Braak and E. Braak, Neuropathological staging of Alzheimer-related changes, Acta Neuropathologica 82 (1991), 239-359.
10. N. Brose, A.G. Petrenko, T.C. Sudhof and R. Jahn, Synaptotagmin: a calcium sensor on the synaptic vesicle surface, Science 256 (1992), 1021-1025.
11. S.J. Buell and P.D. Coleman, Dendritic growth in aged human brain and failure of growth in senile dementia, Science 206 (1979), 854-856.
12. P.D. Coleman, A.M. Kazee, L. Lapham, T. Eskin, K. Rogers and K. Reduced, GAP-43 message levels are associated with increased neurofibrillary tangle density in the frontal association cortex (area 9) in Alzheimer's disease, Neurobiology of Aging 13 (1992), 631-639.
13. P. Davidsson and K. Blennow, Neurochemical dissection of synaptic pathology in Alzheimer's disease, International Psychogeriatrics 10 (1998), 11-23.
14. P. Davies and A.J. Malony, Selective loss of central cholinergic neurons in Alzheimer's disease, Lancet 2 (1976), 1403.
15. C.A. Davies, D.M.A. Mann, P.Q. Sumpter and P.O. Yates, A quantitative morphometric analysis of the synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease, Journal of Neurological Sciences 78 (1987), 151-164.
16. S.M. de la Monte, S.C. Ng and D.W. Hsu, Aberrant GAP-43 gene expression in Alzheimer's disease, American Journal of Pathology 147 (1995), 934-946.
17. T. Deller, P. Mundel and M. Frotscher, Potential role of synaptopodin in spine motility by coupling actin to the spine apparatus, Hippocampus 10 (2000), 569-581.
18. S.T. DeKosky and S.W. Scheff, Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity, Annals of Neurology 5 (1990), 457-464.
19. S.T. Dekosky, S.W. Scheff and S.D. Styren, Structural correlates of cognition in dementia: quantification and assessment of synapse change, Neurodegeneration 5 (1996), 417-421.
20. D.W. Dickson, H.A. Crystal, C. Benova, W. Honer, I. Vincent and P. Davies, Correlations of synaptic and pathological markers with the cognition of the elderly, Neurobiology of Aging 16 (1995), 285-304.
21. L.A. Elferink, M.R. Peterson and R.H. Scheller, A role for synaptotagmin (p65) in regulated exocytosis, Cell 72 (1993), 153-159.
22. N. Emptage, T.V. Bliss and A. Fine, Single synaptic event evoke NMDA receptor - mediated release of calcium from internal stores in hippocampal dendritic spines, Neuron 22 (1999), 115-124.
23. E. Fifkova, J.A. Markham and R.J. Delay, Calcium in the spine apparatus of dendritic spines in the dentate molecular layer, Brain Research 266 (1983), 163-168.
24. C.E. Finch and R.E. Tanzi, Genetics of Aging, Science 278 (1997), 407-411.
25. G. Fischer von Mollard, G.A. Mignery, M. Baumert, M.S. Perin, T.J. Hanson, P.M. Burger et al., Rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles, Proceedings of National Academy of Sciences USA 87 (1990), 19888-19892.
26. S.M. Gabriel, V. Haroutunian, P. Powchik, W.G. Honver, M. Davidson, P. Davies et al., Increased concentrations of presynaptic proteins in the cingulated cortex of subjects with schizophrenia, Archives of General Psychiatry 54 (1997), 559-566.
27. W.H. Gispen, J.L. Leunissen, A.B. Oestreicher, A.J. Verkleij and H. Zwiers, Presynaptic localization of B-50 phosphoprotein: the (ACTH)-sensitive protein kinase substrate involved in rat brain polyphosphoinositide metabolism, Brain Research 328 (1985), 381-385.
28. N.K. Gonatas and A. Moss, Pathologic axons and synapses in human Neuropsychiatric disorders, Human Pathology 6 (1975), 571-582.
29. J. Hardy and D. Allsop, Amyloid deposition as the central event in the etiology of Alzheimer's disease, Trends in Pharmacological Sciences 12 (1991), 383-399.
30. O. Heinonen, H. Soininen, H. Sorvari, O. Kosunen, E. Paljarvi Koivisto and P.J. Riekkinen, Loss of synaptophysin like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease, Neuroscience 74 (1995), 375-384.
31. W.G. Honer, Pathology of presynaptic proteins in Alzheimer's disease: more than simple loss of terminals, Neurobiology of Aging 24 (2003), 1047-1062.
32. W.G. Honer, D.W. Dickson, J. Gleeson and P. Davies, Regional synaptic pathology in Alzheimer's disease, Neurobiology of Aging 13 (1992), 375-382.
33. W.G. Honer, L. Hu and P. Davies, Human synaptic proteins with a heterogeneous distribution in cerebellum and visual cortex, Brain Research. 609 (1993), 9-20.
34. A.Y. Hsia, E. Masliah, L. McConlogue, G.Q. Yu, G. Tatsuno, K. Hu, D. Kholodenko et al., Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models, Proceedings of National Academy of Sciences USA 96 (1999), 3228-3233.
35. R. Jahn and T.C. Sudhof, Synaptic vesicle traffic: rush hour in the nerve terminal, Journal of Neurochemistry 61 (1993), 12-21.
36. J. Kang, H.G. Lemaire, A. Unterbeck, J.M. Salbaum, C.L. Masters, K.H. Grzeschik et al., The precursor Alzheimer's disease amyloid A4 protein resembles a cell surface receptor, Nature 325 (1987), 733-736.
37. L.R. Karns, S.C. Ng, J.A. Freeman and M.C. Fishman, Cloning of complementary DNA for GAP-43, a neuronal growth-related protein, Science 236 (1987), 597-600.
38. A.Y. Kots, A.V. Skurat, E.A. Sergienko, T.V. Bulargina and E.V. Severin, Nitroprusside stimulates the cysteine-specific mono(ADP-ribosylation) of glyceraldehyde-3-phosphate dehydrogenase from human erythrocytes, FEBS Letters. 300 (1992), 9-12.
39. 2+ signals in spines of hippocampal neurons, Journal of Neuroscience 20 (2000), 1791-1799.
40. N.W. Kowall and K.S. Kosik, Axonal disruption and aberrant localization of tau protein characterize neurophil pathology of Alzheimer's disease, Annals of Neurology 22 (1987), 639-643.
41. H. Lassmann, R. Weiler, P. Fischer, C. Bancher, K. Jellinger, E. Floor et al., Synaptic pathology in Alzheimer's disease: immunological data for markers of synaptic and large densecore vesicles, Neuroscience 46 (1992), 1-8.
42. E. Masliah, R.D. Terry, R.M. DeTeresa and L.A. Hansen, Immunohistochemical quantification of the synapse-related protein synaptophysin in Alzheimer disease, Neuroscience Letters 103 (1989), 234-239.
43. E. Masliah, B.O. Carragher, M. Mallory, T. Deerinck, R.D. Terry and M. Ellisman, 3-D reconstruction of the synapse dystrophic neurite relationship in Alzheimer's disease, Journal of Neuropathology and Experimental Neurology 50 (1991), 304.
44. E. Masliah, M. Mallory, L. Hansen, R. De Teresa, M. Alford and R. Terry, Synaptic and neuritic alterations during the progression of Alzheimer's disease, Neuroscience Letters 174 (1994), 67-72.
45. E. Masliah, M. Mallory, N. Ge, M. Alford, I. Veinbergs and A.D. Roses, Neurodegeneration in the central nervous system of apo E-deficient mice, Experimental Neurology 136 (1995), 107-22.
46. E. Masliah, M. Mallory, M. Alford, R. DeTeresa, L.A. Hansen, D.W. McKeel and J.C. Morris, Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease, Neurology 56 (2001), 127-129.
47. H. McIntosh and D. Parkinson, GAP-43 in adult visual cortex, Brain Research 518 (1990), 324-328.
48. H. McIntosh, N. Daw and D. Parkinson, GAP-43 in the cat visual cortex during postnatal development, Visual Neuroscience 4 (1990), 585-593.
49. H.T. McMahon and T.C. Sudhof, Synaptic core complex of synaptobrevin, syntaxin, and SNAP25 forms high affinity alpha-SNAP binding site, Journal of Biological Chemistry. 270 (1995), 2213-2217.
50. M. Mercken, U. Lubke, M. Vandermeeren, J. Gheuens and B. Oestreicher, Immunocytochemical detection of the growth-associated protein B-50 by newly characterized monoclonal antibodies in human brain and muscle, Journal of Neurobiology 23 (1992), 309-321.
51. L. Mucke, E. Masliah, G.-Q. Yu, M. Mallory, E.M. Rockenstein, G. Tatsuno, K, Hu, D. Kholodenko, K. Johnson-Wood and L. McConlogue, High-level neuronal expression of abeta 1-42 in wild type human amyloid precursor transgenic mice: synaptotoxicity without plaque formation, Journal of neuroscience 20 (2000), 4050-4058.
52. P. Mundel, H.W. Heid, T.M. Mundel, M. Kruger, J. Reiser and W. Kriz, Synaptopodin: an actin associated protein in telencephalic dendrites and renal podocytes, Journal of Cell Biology 139 (1997), 198-204.
53. F. Navone, R. Jahn, G. Di Gioia, H. Stukenbrok, P. Greengard and P. De Camilli, Protein p38: an integral membrane protein specific for small vesicles of neurons and neuroendocrine cells, Journal of Cell Biology 103 (1986), 2511-2527.
54. J.L. Phillips, D.R. Tolan and R.E. Hausman, Antisense inhibition of R-cognin expression modulates differentiation of retinal neurons in vitro, Molecular Vision 3 (1997), 12.
55. C.J. Provoda, M.T. Waring and K.M. Buckley, Evidence for a primary endocytic vesicle involved in synaptic vesicle biogenesis, Journal of Biological Chemistry 275 (2000), 7004-7012.
56. S.W. Scheff, S.T. Dekosky and D.A. Price, Quantitative assessment of cortical synaptic density in Alzheimer's disease, Neurobiology of Aging 11 (1990), 29-37.
57. D.J. Selkoe, Alzheimer's disease: genes, proteins, and therapy, Physiological Reviews 81 (2001), 741-766.
58. D.J. Selkoe, Alzheimer's Disease is a synaptic failure, Science 298 (2002), 789-791.
59. S. Shimohama, S. Fujimoto, Y. Sumida, K. Akagawa, T. Shirao, Y. Matsuoka and T. Taniguchi, Differential expression of rat brain synaptic proteins in development and aging, Biochemical Biophysical Research Communication 251 (1998), 394-398.
60. D.H. Small, S.S. Mock and J.C. Bornstein, Alzheimer's disease and Abeta toxicity: from top to bottom, Nature Reviews in Neurosciences 2 (2001), 595-898.
61. T.C. Sudhof, P. De Camilli, H. Niemann and R. Jahn, Membrane fusion machinery: insights from synaptic proteins, Cell 8 (1993), 1-4.
62. T.C. Sudhof, The synaptic vesicle cycle: a cascade of protein-protein interactions, Nature 375 (1995), 645-653.
63. C.I. Sze, J.C. Troncoso, C. Kawas, P. Mouton, D.L. Price and L.J. Martin, Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease, Journal of Neuropathology and Experimental Neurology 56 (1997), 933-944.
64. C.I. Sze, B. Hong, K. Bette, Kleinschmidt-Demasters, C.M. Filley and L.J. Martin, Selective regional loss of exocytotic presynaptic vesicle proteins in Alzheimer's disease brains, Journal of Neurological Sciences 175 (2000), 81-90.
65. R.D. Terry, E. Masliah, D.P. Salmon, N. Butters, R. DeTeresa, R. Hill, L.A. Hansen and R. Katzman, Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment, Annals of Neurology 30 (1991), 572-580.
66. C. Walch-Solimena, K. Takei, K.L. Marek, K. Midyett, T.C. Sudhof, P. De Camilli and R. Jahn, Synaptotagmin: a membrane constituent of neuropeptide-containing large dense-core vesicles, Journal of Neurosciences 13 (1993), 3895-3903.
67. J.B. Watson, E.F. Battenberg, K.K. Wong, F.E. Bloom and J.G. Sutcliffe, Subtractive cDNA cloning of RC3, a rodent cortex-enriched mRNA encoding a novel 78 residue protein, Journal of Neuroscience Research 26 (1990), 397-408.
68. J.B. Watson, I. Szijan and P.M. Coulter, Localization of RC3 (neurogranin) in rat brain subcellular fractions, Brain Research and Molecular Brain Research 27 (1994), 323-328.
69. B. Wiedenman and W.W. Franke, Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr. 38,000 characteristic of presynaptic vesicles, Cell 41 (1985), 1017-1028.
70. P.J. Yao, M. Zhu, E.I. Pyun, A.I. Brooks, S. Therianos, V. Meyers and P.D. Coleman, Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease, Neurobiology of Disease 12 (2002), 97-109.
71. B.C. Yoo, N. Cairns, M. Fountoulakis and G. Lubec, Synaptosomal proteins, beta-soluble N-ethylmaleimide-sensitive factor attachment protein (beta-SNAP), gamma-SNAP and synaptotagmin I in brain of patients with Down syndrome and Alzheimer's disease, Dementia Geriatrics Cognition Disorders 12 (2001), 219-225.