AD synapses contain abundant Aβ monomer and multiple soluble oligomers, including a 56-kDa assembly

Neurobiology of Aging

Volumn 33, Issue 8, 2012, Pages 1545-1555

  Sokolow, Sophie ^a   Henkins, Kristen M ^b   Bilousova, Tina ^a   Miller, Carol A ^c   Vinters, Harry V ^b   Poon, Wayne ^d   Cole, Gregory M ^b   Gylys, Karen Hoppens ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

A11 antibody; Flow cytometry; OC antibody; Parkinson's disease; PSD 95; Synaptophysin; Synaptosome

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; BRAIN EXTRACT; DODECYL SULFATE SODIUM; MONOMER; OLIGOMER; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; MALE; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SYNAPSE; SYNAPTOSOME; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; DIMERIZATION; HUMANS; MOLECULAR WEIGHT; PARIETAL LOBE; SOLUBILITY; SYNAPSES; TISSUE DISTRIBUTION;

EID: 84861913912     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.05.011     Document Type: Article

References (52)

1. Bitan G., Fradinger E.A., Spring S.M., Teplow D.B. Neurotoxic protein oligomers-what you see is not always what you get. Amyloid 2005, 12:88-95.
2. Bitan G., Kirkitadze M.D., Lomakin A., Vollers S.S., Benedek G.B., Teplow D.B. Amyloid beta -protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:330-335.
3. Boland B., Kumar A., Lee S., Platt F.M., Wegiel J., Yu W.H., Nixon R.A. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci 2008, 28:6926-6937.
4. Brody D.L., Magnoni S., Schwetye K.E., Spinner M.L., Esparza T.J., Stocchetti N., Zipfel G.J., Holtzman D.M. Amyloid-beta dynamics correlate with neurological status in the injured human brain. Science 2008, 321:1221-1224.
5. Butler D., Nixon R.A., Bahr B.A. Potential compensatory responses through autophagic/lysosomal pathways in neurodegenerative diseases. Autophagy 2006, 2:234-237.
6. Cataldo A.M., Barnett J.L., Pieroni C., Nixon R.A. Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: neuropathologic evidence for a mechanism of increased beta-amyloidogenesis. J. Neurosci 1997, 17:6142-6151.
7. Cirrito J.R., Kang J.E., Lee J., Stewart F.R., Verges D.K., Silverio L.M., Bu G., Mennerick S., Holtzman D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron 2008, 58:42-51.
8. Cirrito J.R., Yamada K.A., Finn M.B., Sloviter R.S., Bales K.R., May P.C., Schoepp D.D., Paul S.M., Mennerick S., Holtzman D.M. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 2005, 48:913-922.
9. Cleary J.P., Walsh D.M., Hofmeister J.J., Shankar G.M., Kuskowski M.A., Selkoe D.J., Ashe K.H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci 2005, 8:79-84.
10. Dunkley P.R., Jarvie P.E., Robinson P.J. A rapid Percoll gradient procedure for preparation of synaptosomes. Nat. Protoc 2008, 3:1718-1728.
11. Fein J.A., Sokolow S., Miller C.A., Vinters H.V., Yang F., Cole G.M., Gylys K.H. Co-localization of amyloid beta and tau pathology in Alzheimer's disease synaptosomes. Am. J. Pathol 2008, 172:1683-1692.
12. Frykman S., Hur J.Y., Frånberg J., Aoki M., Winblad B., Nahalkova J., Behbahani H., Tjernberg L.O. Synaptic and endosomal localization of active gamma-secretase in rat brain. PLoS One 2010, 5:e8948.
13. Giuffrida M.L., Caraci F., Pignataro B., Cataldo S., De Bona P., Bruno V., Molinaro G., Pappalardo G., Messina A., Palmigiano A., Garozzo D., Nicoletti F., Rizzarelli E., Copani A. Beta-amyloid monomers are neuroprotective. J. Neurosci 2009, 29:10582-10587.
14. Gouras G.K., Almeida C.G., Takahashi R.H. Intraneuronal Abeta accumulation and origin of plaques in Alzheimer's disease. Neurobiol. Aging 2005, 26:1235-1244.
15. Gylys K.H., Fein J.A., Tan A.M., Cole G.M. Apolipoprotein E enhances uptake of soluble but not aggregated amyloid-beta protein into synaptic terminals. J. Neurochem 2003, 84:1442-1451.
16. Gylys K.H., Fein J.A., Yang F., Cole G.M. Enrichment of presynaptic and postsynaptic markers by size-based gating analysis of synaptosome preparations from rat and human cortex. Cytometry A 2004, 60:90-96.
17. Gylys K.H., Fein J.A., Yang F., Miller C.A., Cole G.M. Increased cholesterol in Abeta-positive nerve terminals from Alzheimer's disease cortex. Neurobiol. Aging 2007, 28:8-17.
18. Gylys K.H., Fein J.A., Yang F., Wiley D.J., Miller C.A., Cole G.M. Synaptic changes in Alzheimer's disease: increased amyloid-beta and gliosis in surviving terminals is accompanied by decreased PSD-95 fluorescence. Am. J. Pathol 2004, 165:1809-1817.
19. Inoue E., Deguchi-Tawarada M., Togawa A., Matsui C., Arita K., Katahira-Tayama S., Sato T., Yamauchi E., Oda Y., Takai Y. Synaptic activity prompts gamma-secretase-mediated cleavage of EphA4 and dendritic spine formation. J. Cell Biol 2009, 185:551-564.
20. Kayed R., Head E., Sarsoza F., Saing T., Cotman C.W., Necula M., Margol L., Wu J., Breydo L., Thompson J.L., Rasool S., Gurlo T., Butler P., Glabe C.G. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol. Neurodegener 2007, 2:18.
21. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003, 300:486-489.
22. Kim S.H., Fraser P.E., Westaway D., St.George-Hyslop P.H., Ehrlich M.E., Gandy S. Group II metabotropic glutamate receptor stimulation triggers production and release of Alzheimer's amyloid {beta}42 from isolated intact nerve terminals. J. Neurosci 2010, 30:3870-3875.
23. Klyubin I., Betts V., Welzel A.T., Blennow K., Zetterberg H., Wallin A., Lemere C.A., Cullen W.K., Peng Y., Wisniewski T., Selkoe D.J., Anwyl R., Walsh D.M., Rowan M.J. Amyloid beta protein dimer-containing human CSF disrupts synaptic plasticity: prevention by systemic passive immunization. J. Neurosci 2008, 28:4231-4237.
24. Kornau H.C., Schenker L.T., Kennedy M.B., Seeburg P.H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995, 269:1737-1740.
25. Lacor P.N., Buniel M.C., Chang L., Fernandez S.J., Gong Y., Viola K.L., Lambert M.P., Velasco P.T., Bigio E.H., Finch C.E., Krafft G.A., Klein W.L. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J. Neurosci 2004, 24:10191-10200.
26. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., Klein W.L. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci 2007, 27:796-807.
27. Lazarov O., Lee M., Peterson D.A., Sisodia S.S. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci 2002, 22:9785-9793.
28. Lesné S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
29. Lue L.F., Kuo Y.M., Roher A.E., Brachova L., Shen Y., Sue L., Beach T., Kurth J.H., Rydel R.E., Rogers J. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol 1999, 155:853-862.
30. Mak K., Yang F., Vinters H.V., Frautschy S.A., Cole G.M. Polyclonals to beta-amyloid(1-42) identify most plaque and vascular deposits in Alzheimer cortex, but not striatum. Brain Res 1994, 667:138-142.
31. Mc Donald J.M., Savva G.M., Brayne C., Welzel A.T., Forster G., Shankar G.M., Selkoe D.J., Ince P.G., Walsh D.M. The presence of sodium dodecyl sulphate-stable Abeta dimers is strongly associated with Alzheimer-type dementia. Brain 2010, 133:1328-1341. Medical Research Council Cognitive Function and Ageing Study.
32. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Beyreuther K., Bush A.I., Masters C.L. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol 1999, 46:860-866.
33. Näslund J., Haroutunian V., Mohs R., Davis K.L., Davies P., Greengard P., Buxbaum J.D. Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 2000, 283:1571-1577.
34. Nixon R.A., Wegiel J., Kumar A., Yu W.H., Peterhoff C., Cataldo A., Cuervo A.M. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol 2005, 64:113-122.
35. Permanne B., Perez C., Soto C., Frangione B., Wisniewski T. Detection of apolipoprotein E/dimeric soluble amyloid beta complexes in Alzheimer's disease brain supernatants. Biochem. Biophys. Res. Commun 1997, 240:715-720.
36. Rozkalne A., Spires-Jones T.L., Stern E.A., Hyman B.T. A single dose of passive immunotherapy has extended benefits on synapses and neurites in an Alzheimer's disease mouse model. Brain Res 2009, 1280:178-185.
37. Schmid I., Uittenbogaart C.H., Giorgi J.V. A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry 1991, 12:279-285.
38. Selkoe D.J. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav. Brain Res 2008, 192:106-113.
39. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., Selkoe D.J. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med 2008, 14:837-842.
40. Sheng J.G., Price D.L., Koliatsos V.E. Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J. Neurosci 2002, 22:9794-9799.
41. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nat. Neurosci 2005, 8:1051-1058.
42. Spires-Jones T.L., Mielke M.L., Rozkalne A., Meyer-Luehmann M., de Calignon A., Bacskai B.J., Schenk D., Hyman B.T. Passive immunotherapy rapidly increases structural plasticity in a mouse model of Alzheimer disease. Neurobiol. Dis 2009, 33:213-220.
43. Südhof T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 1995, 375:645-653.
44. Takahashi R.H., Capetillo-Zarate E., Lin M.T., Milner T.A., Gouras G.K. Co-occurrence of Alzheimer's disease β-amyloid and τ pathologies at synapses. Neurobiol. Aging 2010, 31:1145-1152.
45. 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 2002, 161:1869-1879.
46. Tomic J.L., Pensalfini A., Head E., Glabe C.G. Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction. Neurobiol. Dis 2009, 35:352-358.
47. Townsend M., Shankar G.M., Mehta T., Walsh D.M., Selkoe D.J. Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J. Physiol 2006, 572:477-492.
48. Tsigelny I.F., Crews L., Desplats P., Shaked G.M., Sharikov Y., Mizuno H., Spencer B., Rockenstein E., Trejo M., Platoshyn O., Yuan J.X., Masliah E. Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PLoS One 2008, 3:e3135.
49. Walsh D.M., Selkoe D.J. A beta oligomers - a decade of discovery. J. Neurochem 2007, 101:1172-1184.
50. Williams C., Mehrian Shai R., Wu Y., Hsu Y.H., Sitzer T., Spann B., McCleary C., Mo Y., Miller C.A. Transcriptome analysis of synaptoneurosomes identifies neuroplasticity genes overexpressed in incipient Alzheimer's disease. PLoS One 2009, 4:e4936.
51. Wolf M.E., Kapatos G. Flow cytometric analysis of rat striatal nerve terminals. J. Neurosci 1989, 9:94-105.
52. Zou K., Gong J.S., Yanagisawa K., Michikawa M. A novel function of monomeric amyloid beta-protein serving as an antioxidant molecule against metal-induced oxidative damage. J. Neurosci 2002, 22:4833-4841.