Snaptic changes in alzheimer's disease: Increased amyloid-β and gliosis in surviving terminals is accompanied by decreased PSD-95 fluorescence

American Journal of Pathology

Volumn 165, Issue 5, 2004, Pages 1809-1817

  Gylys, Karen Hoppens ^a,c   Fein, Jeffrey A ^a   Yang, Fusheng ^a   Wiley, Dorothy J ^a   Miller, Carol A ^b   Cole, Gregory M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CALCEIN; POSTSYNAPTIC DENSITY PROTEIN 95; GLIAL FIBRILLARY ACIDIC PROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN; POSTSYNAPTIC DENSITY PROTEINS; SNAP25 PROTEIN, HUMAN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

AGED; ALZHEIMER DISEASE; ANTIBODY LABELING; ARTICLE; ASSOCIATION CORTEX; BRAIN SYNAPTOSOME; CONTROLLED STUDY; CRYOPRESERVATION; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; GLIOSIS; HUMAN; HUMAN TISSUE; MALE; NERVE ENDING; PRIORITY JOURNAL; SYNAPSE; BIOLOGICAL MODEL; BIOSYNTHESIS; BRAIN; CHEMISTRY; METABOLISM; NERVE CELL; PATHOLOGY; TIME; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; BLOTTING, WESTERN; BRAIN; FEMALE; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HUMANS; MALE; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURONS; SYNAPSES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; TIME FACTORS;

EID: 7244223228     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0002-9440(10)63436-0     Document Type: Article

References (58)

1. Hardy J, Selkoe DJ: The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356
2. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R: Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991, 30:572-580
3. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J: Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 1999, 155:853-862
4. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L: High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 2000, 20:4050-4058
5. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR: Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 2000, 156:15-20
6. Takahashi RH, Milner TA, Li F, Nam EE, Edgar MA, Yamaguchi H, Beal MF, Xu H, Greengard P, Gouras GK: Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 2002, 161:1869-1879
7. Lazarov O, Lee M, Peterson DA, Sisodia SS: Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 2002, 22:9785-9793
8. Sheng JG, Price DL, Koliatsos VE: Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J Neurosci 2002, 22:9794-9799
9. Selkoe DJ: Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791
10. Mukaetova-Ladinska EB, Garcia-Siera F, Hurt J, Gertz HJ, Xuereb JH, Hills R, Brayne C, Huppert FA, Paykel ES, McGee M, Jakes R, Honer WG, Harrington CR, Wischik CM: Staging of cytoskeletal and beta-amyloid changes in human isocortex reveals biphasic synaptic protein response during progression of Alzheimer's disease. Am J Pathol 2000, 157:623-636
11. King DL, Arendash GW: Maintained synaptophysin immunoreactivity in Tg2576 transgenic mice during aging: correlations with cognitive impairment. Brain Res 2002, 926:58-68
12. Hu L, Wong TP, Cote SL, Bell KF, Cuello AC: The impact of Abeta-plaques on cortical cholinergic and non-cholinergic presynaptic boutons in Alzheimer's disease-like transgenic mice. Neuroscience 2003, 121:421-432
13. Harigaya Y, Shoji M, Shirao T, Hirai S: Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J Neurosci Res 1996, 43:87-92
14. Hatanpaa K, Isaacs KR, Shirao T, Brady DR, Rapoport SI: Loss of proteins regulating synaptic plasticity in normal aging of the human brain and in Alzheimer disease. J Neuropathol Exp Neurol 1999 58:637-643
15. Shim KS, Lubec G: Drebrin, a dendritic spine protein, is manifold decreased in brains of patients with Alzheimer's disease and Down syndrome. Neurosci Lett 2002, 324:209-212
16. Yang F, Sun X, Beech W, Teter B, Wu S, Sigel J, Vinters HV, Frautschy SA, Cole GM: Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer's disease. Am J Pathol 1998, 152:379-389
17. Ivins KJ, Bui ET, Cotman CW: Beta-amyloid induces local neurite degeneration in cultured hippocampal neurons: evidence for neuritic apoptosis. Neurobiol Dis 1998, 5:365-378
18. Mattson MP, Duan W: "Apoptotic" biochemical cascades in synaptic compartments: roles in adaptive plasticity and neurodegenerative disorders. J Neurosci Res 1999, 58:152-166
19. Mak K, Yang F, Vinters HV, Frautschy SA, Cole GM: Polyclonals to beta-amyloid(1-42) identify most plaque and vascular deposits in Alzheimer cortex, but not striatum. Brain Res 1994, 667:138-142
20. Zhang C, Ao Z, Seth A, Schlossman SF: A mitochondrial membrane protein defined by a novel monoclonal antibody is preferentially detected in apoptotic cells. J Immunol 1996, 157:3980-3987
21. Dodd PR, Hardy JA, Oakley AE, Edwardson JA, Perry EK, Delaunoy JP: A rapid method for preparing synaptosomes: comparison, with alternative procedures. Brain Res 1981, 226:107-118
22. Weiler MH, Gundersen CB, Jenden DJ: Choline uptake and acetylcholine synthesis in synaptosomes: investigations using two different labeled variants of choline. J Neurochem 1981, 36:1802-1812
23. Schmid I, Uittenbogaart CH, Giorgi JV: A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry 1991, 12:279-285
24. Lim GP, Yang F, Chu T, Chen P, Beech W, Teter B, Tran T, Ubeda O, Ashe KH, Frautschy SA, Cole GM: Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 2000, 20:5709-5714
25. Gylys KH, Fein JA, Cole GM: Quantitative characterization of crude synaptosomal fraction (P-2) components by flow cytometry. J Neurosci Res 2000, 61:186-192
26. Gylys KH, Fein JA, Tan AM, Cole GM: Apolipoprotein E enhances uptake of soluble but not aggregated amyloid-beta protein into synaptic terminals. J Neurochem 2003, 84:1442-1451
27. Gylys KH, Fein JA, Yang F, Cole GM: Enrichment of presynaptic and postsynaptic markers by size-based gating analysis of synaptosomes preparations from rat and human cortex. Cytometry 2004, 60A:90-96
28. Johnson MW, Chotiner JK, Watson JB: Isolation and characterization of synaptoneurosomes from single rat hippocampal slices. J Neurosci Methods 1997, 77:151-156
29. Wechsler A, Teichberg VI: Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin. EMBO J 1998, 17:3931-3939
30. Chicurel ME, Terrian DM, Potter H: mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines. J Neurosci 1993, 13:4054-4063
31. Nicholls DG: The glutamatergic nerve terminal. Eur J Biochem 1993, 212:613-631
32. Gylys KH, Fein JA, Cole GM: Caspase inhibition protects nerve terminals from in vitro degradation. Neurochem Res 2002, 27:465-472
33. Sudhof TC: The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 1995, 375:645-653
34. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH: Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995, 269:1737-1740
35. Xue M, Zhang B: Do SNARE proteins confer specificity for vesicle fusion? Proc Natl Acad Sci USA 2002, 99:13359-13361
36. Slezak M, Pfrieger FW: New roles for astrocytes: regulation of CNS synaptogenesis. Trends Neurosci 2003, 26:531-535
37. Derouiche A, Anlauf E, Aumann G, Muhlstadt B, Lavialle M: Anatomical aspects of glia-synapse interaction: the perisynaptic glial sheath consists of a specialized astrocyte compartment. J Physiol Paris 2002, 96:177-182
38. Masliah E, Mallory M, Hansen L, DeTeresa R, Alford M, Terry R: Synaptic and neuritic alterations during the progression of Alzheimer's disease. Neurosci Lett 1994, 174:67-72
39. DeKosky ST, Scheff SW: Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990, 27:457-464
40. Masliah E, Mallory M, Alford M, DeTeresa R, Hansen LA, McKeel Jr DW, Morris JC: Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 2001, 56:127-129
41. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG: Age-dependent changes in brain CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 2001, 21:372-381
42. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL: Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 1998, 95:6448-6453
43. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, Teplow DB: Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 1999, 274:25945-25952
44. Klein WL, Krafft GA, Finch CE: Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci 2001, 24:219-224
45. Davies CA, Mann DM: Is the "preamyloid" of diffuse plaques in Alzheimer's disease really nonfibrillar? Am J Pathol 1993, 143:1594-1605
46. Kakio A, Nishimoto S, Yanagisawa K, Kozutsumi Y, Matsuzaki K: Interactions of amyloid beta-protein with various gangliosides in raft-like membranes: importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid. Biochemistry 2002, 41:7385-7390
47. Yanagisawa K, Odaka A, Suzuki N, Ihara Y: GM1 ganglioside-bound amyloid beta-protein (A beta): a possible form of preamyloid in Alzheimer's disease. Nat Med 1995, 1:1062-1066
48. Kawarabayashi T, Shoji M, Younkin LH, Wen-Lang L, Dickson DW, Murakami T, Matsubara E, Abe K, Ashe KH, Younkin SG: Dimeric amyloid beta protein rapidly accumulates in lipid rafts followed by apolipoprotein E and phosphorylated tau accumulation in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 2004, 24:3801-3809
49. Li R, Lindholm K, Yang LB, Yue X, Citron M, Yan R, Beach T, Sue L, Sabbagh M, Cai H, Wong P, Price D, Shen Y: Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci USA 2004, 101:3632-3637
50. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evi G: Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Ann Neurol 2002, 51:783-786
51. Fukumoto H, Rosene DL, Moss MB, Raj S, Hyman BT, Irizarry MC: Beta-secretase activity increases with aging in human, monkey, and mouse brain. Am J Pathol 2004, 164:719-725
52. Pfrieger FW, Barres BA: Synaptic efficacy enhanced by glial cells in vitro. Science 1997, 277:1684-1687
53. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA: Control of synapse number by glia. Science 2001, 291:657-661
54. Adams I, Jones DG: Synaptic remodelling and astrocytic hypertrophy in rat cerebral cortex from early to late adulthood. Neurobiol Aging 1982, 3:179-186
55. Roth KA: Caspases, apoptosis, and Alzheimer disease: causation, correlation, and confusion. J Neuropathol Exp Neurol 2001, 60:829-838
56. Calon F, Lim GP, Yang F, Morihora T, Teter B, Ubeda O, Rostaing P, Triller A, Salem Jr N, Ashe KH, Frautschy SA, Cole GM: Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43:633-645
57. Shirao T, Sekino Y: Clustering and anchoring mechanisms of molecular constituents of postsynaptic scaffolds in dendritic spines. Neurosci Res 2001, 40:1-7
58. Dickey CA, Loring JF, Montgomery J, Gordon MN, Eastman PS, Morgan D: Selectively reduced expression of Synaptic plasticityrelated genes in amyloid precursor protein + presenilin-1 transgenic mice. J Neurosci 2003, 23:5219-5226