Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease

Journal of Neuropathology and Experimental Neurology

Volumn 56, Issue 8, 1997, Pages 933-944

  Sze, Chun I ^a   Troncoso, Juan C ^b   Kawas, Claudia ^b   Mouton, Peter ^b   Price, Donald L ^b   Martin, Lee J ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Braak stage; CA1; Memory loss; Senile plaque; Synapse

Indexed keywords

BETA TUBULIN; SYNAPTOPHYSIN;

AGED; AGING; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DEGENERATIVE DISEASE; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MALE; NEUROPATHOLOGY; PRIORITY JOURNAL; SENILE PLAQUE; SYNAPSE VESICLE;

EID: 0030872413     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199708000-00011     Document Type: Article

References (50)

1. Katzman R. The prevalence and malignancy of Alzheimer's disease. A major killer. Arch Neurol 1976;33:217-18
2. Crook T, Bartus RT, Ferris SH, et al. Age-associated memory impairment: Proposed diagnostic criteria and measures of clinical change. Report of a National Institute of Mental Health work group. Dev Neuropsychol 1986;2:261-76
3. Evans DA, Funkenstein HH, Albert MS, et al. Prevalence of Alzheimer's disease in a community population of older persons. Higher than previously reported. JAMA 1989;262:2551-56
4. Bachman DL, Wolf PA, Linn RT, et al. Incidence of dementia and probable Alzheimer's disease in a general population: the Framingham study. Neurology 1993;43:515-19
5. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973;232:331-56
6. Nicoll RA, Kauer JA, Malenka RC. The current excitement in longterm potentiation. Neuron 1988;1:97-103
7. Adams I. Comparison of synaptic changes in the precentral and postcentral cerebral cortex of aging humans: A quantitative ultrastructural study. Neurobiol Aging 1987;8:203-12
8. Masliah E, Mallory M, Hansen L, et al. Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 1993;43:192-97
9. Davies CA, Mann DMA, Sumpter QP, Yates PO. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in paitents with Alzheimer's disease. J Neurol Sci 1987;78:151-64
10. Hamos JE, DeGennaro LJ, Drachman DA. Synaptic loss in Alzheimer's disease and other dementias. Neurology 1989;39:355-61
11. Masliah E, Terry RD, DeTeresa RM, Hansen LA. Immunohistochemical quantification of the synapse-related protein synaptophysin in Alzheimer disease. Neurosci Lett 1989;103:234-39
12. DeKosky ST, Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 1990;27:457-63
13. Scheff SW, DeKosky ST, Price DA. Quantitative assessment of cortical synaptic density in Alzheimer's disease. Neurobiol Aging 1990;11:29-37
14. Terry RD, Masliah E, Salmon DP, et al. Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991;30:572-80
15. Honer WG, Dickson DW, Gleeson J, Davies P. Regional synaptic pathology in Alzheimer's disease. Neurobiol Aging 1992;13:375-82
16. DeKosky ST, Harbaugh RE, Schmitt FA, et al. Cortical biopsy in Alzheimer's disease: Diagnostic accuracy and neurochemical, neuropathological, and cognitive correlations. Ann Neurol 1992;32: 625-32
17. Squire LR, Zola-Morgan S. Memory: Brain systems and behavior. TINS 1988;11:170-75
18. Zola-Morgan S, Squire LR, Amaral DG. Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys. J Neurosci 1989;9:898-13
19. Ball MJ, Hachinski V, Fox A, et al. A new definition of Alzheimer's disease: A hippocampal dementia. Lancet 1985;1:14-16
20. Samuel W, Masliah E, Hill LR, et al. Hippocampal connectivity and Alzheimer's dementia: Effects of synapse loss and tangle frequency in a two-component model. Neurology 1994;44:2081-88
21. Rothstein JD, Van Kammen M, Levey AI, et al. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 1995;38:73-84
22. Ginsberg SD, Rothstein JD, Price DL, Martin LJ. Fimbria-fornix transections selectively down-regulate subtypes of glutamate transporter and glutamate receptor proteins in septum and hippocampus. J Neurochem 1996;67:1208-16
23. Troncoso JC, Martin LJ, Dal Forno G, Kawas CH. Neuropathology in controls and demented subjects from the Baltimore Longitudinal Study of Aging. Neurobiol Aging 1996;17:365-71
24. Shock NW, Greulich RC, Costa PT Jr, et al. Normal human aging: The Baltimore longitudinal study of aging. Baltimore, MD: U.S. Department of Health & Human Services. 1984
25. Mirra SS, Gearing M, McKeel DW Jr., et al. Interlaboratory comparison of neuropathology assessments in Alzheimer's disease: A study of the consortium to establish a registry for Alzheimer's disease (CERAD). J Neuropathol Exp Neurol 1994;53:303-15
26. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991;82:239-59
27. Nieto A, Montejo de Garcini E, Avila J. Altered levels of microtubule proteins in brains of Alzheimer's disease patients. Acta Neuropathol 1989;78:47-51
28. Thai LJ, Grundman M, Golden R. Alzheimer's disease: A correlational analysis of the Blessed Information-Memory-Concentration Test and the Mini-Mental State Exam. Neurology 1986;36:262-64
29. Liao D, Jones A, Malinow R. Direct measurement of quantal changes underlying long-term potentiation in CA1 hippocampus. Neuron 1992;9:1089-97
30. Trimble WS, Linial M, Scheller RH. Cellular and molecular biology of the presynaptic nerve terminal. Ann Rev Neurosci 1991;14:93-122
31. Damer CK, Creutz CE. Secretory and synaptic vesicle membrane proteins and their possible roles in regulated exocytosis. Prog Neurobiol 1994;43:511-36
32. Sudhof TC. The synaptic vesicle cycle: A cascade of proteinprotein interactions. Nature 1995;375:645-53
33. r 38,000 characteristic of presynaptic vesicles. Cell 1985;41:1017-28
34. Navone F, Jahn R, DiGioia G, et al. Protein p38: An integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J Cell Biol 1986;103:2511-27
35. Caceres A, Binder LI, Payne MR, et al. Differential subcellular localization of tubulin and the microtubule-associated protein MAP2 in brain tissue as revealed by immunocytochemistry with monoclonal hybridoma antibodies. J Neurosci 1984;4;394-410
36. Gotow T, Miyaguchi K, Hashmioto PH. Cytoplasmic architecture of the axon terminal: Filamentous strands specifically associated with synaptic vesicles. Neuroscience 1991;40:587-98
37. Lassmann H, Weiler R, Fischer P, et al. Synaptic pathology in Alzheimer's disease: Immunological data for markers of synaptic and large dense-core vesicles. Neuroscience 1992;46:1-8
38. Heinonen O, Soininen H, Sorvari H, et al. Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neuroscience 1995;64:375-84
39. Alford MF, Masliah E, Hansen LA, Terry RD. A simple dot-immunobinding assay for quantification of synaptophysin-like immunoreactivity in human brain. J Histochem Cytochem 1994;42: 283-87
40. Masliah E, Terry RD, Alford M, et al. Cortical and subcortical patterns of synaptophysin-like immunoreactivity in Alzheimer's disease. Am J Pathol 1991;138:235-46
41. Dickson DW, Crystal HA, Bevona C, et al. Correlations of synaptic and pathological markers with cognition of the elderly. Neurobiol Aging 1995;16:285-304
42. Martin LJ, Sisodia SS, Koo EH, et al. Amyloid precursor protein in aged nonhuman primates. Proc Natl Acad Sci USA 1991;88: 1461-65
43. Martin LJ, Pardo CA, Cork LC, Price DL. Synaptic pathology and glial responses to neuronal injury precede the formation of senile plaques and amyloid deposits in the aging cerebral cortex. Am J Pathol 1994;145:1358-81
44. Masliah E, Honer WG, Mallory M, et al. Topographical distribution of synaptic-associated proteins in the neuritic plaques of Alzheimer's disease hippocampus. Acta Neuropathol 1994;87:135-42
45. Adams IM. Structural plasticity of synapses in Alzheimer's disease. Mol Neurobiol 1992;5:411-19
46. Scheff SW, Price DA. Synapse loss in the temporal lobe in Alzheimer's disease. Ann Neurol 1993;33:190-99
47. Scheff SW, Sparks DL, Price DA. Quantitative assessment of synaptic density in the entorhinal cortex in Alzheimer's disease. Ann Neurol 1993;34:356-61
48. Gomez-Isla T, Price JL, McKeel DW Jr, et al. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 1996;16:4491-4500
49. Flood DG, Coleman PD. Failed compensatory dendritic growth as a pathophysiological process in Alzheimer's disease. Le J Can Des Sci Neurologiques 1989;13:475-79
50. Jagadha V, Becker L. Dendritic pathology: An overview of Golgi studies in man. Can J Neurol Sci 1989;16:41-51