Submicromolar Aβ42 reduces hippocampal glutamate receptors and presynaptic markers in an aggregation-dependent manner

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 12, 2011, Pages 1664-1674

  Wisniewski, Meagan L ^a   Hwang, Jeannie ^a   Bahr, Ben A ^a  

^a UNIVERSITY OF NORTH CAROLINA AT PEMBROKE   (United States)

Author keywords

A 42; Aggregation; Alzheimer's disease; Amyloid beta; GluR1; Synaptic decline

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMYLOID BETA PROTEIN[1-42]; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PRESYNAPTIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL DEGENERATION; HIPPOCAMPUS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; RAT; TEMPERATURE;

AMYLOID BETA-PEPTIDES; ANALYSIS OF VARIANCE; ANIMALS; BIOLOGICAL MARKERS; HIPPOCAMPUS; KINETICS; MOLECULAR WEIGHT; PEPTIDE FRAGMENTS; PRESYNAPTIC TERMINALS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE; TISSUE CULTURE TECHNIQUES;

EID: 80054118121     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.09.011     Document Type: Article

References (66)

1. Welsh-Bohmer K.A., White C.L. Alzheimer disease: what changes in the brain cause dementia?. Neurology 2009, 72:354-360.
2. Walsh D.M., Selkoe D.J. Aβ oligomers - a decade of discovery. J. Neurochem. 2007, 101:1172-1184.
3. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
4. Kuo Y.M., Emmerling M.R., Vigo-Pelfrey C., Kasunic T.C., Kirkpatrick J.B., Murdoch G.H., Ball M.J., Roher A.E. Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 1996, 271:4077-4081.
5. Burdick D., Soreghan B., Kwon M., Kosmoski J., Knauer M., Henschen A., Yates J., Cotman C., Glabe C. Assembly and aggregation properties of synthetic Alzheimer's A4/β amyloid peptide analogs. J. Biol. Chem. 1992, 267:546-554.
6. Jarrett J.T., Berger E.P., Lansbury P.T. The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 1993, 32:4693-4697.
7. St.George-Hyslop P.H., Haines J., Rogaev E., Mortilla M., Vaula G., Pericak-Vance M., Foncin J.F., Montesi M., Bruni A., Sorbi S., Rainero I., Pinessi L., Pollen D., Polinsky R., Nee L., Kennedy J., Macciardi F., Rogaeva E., Liang Y., Alexandrova N., Lukiw W., Schlumpf K., Tanzi R., Tsuda T., Farrer L., Cantu J.M., Duara R., Amaducci L., Bergamini L., Gusella J., Roses A., McLachlan D.C. Genetic evidence for a novel familial Alzheimer's disease locus on chromosome 14. Nat. Genet. 1992, 2:330-334.
8. Sherrington R., Rogaev E.I., Liang Y., Rogaeva E.A., Levesque G., Ikeda M., Chi H., Lin C., Li G., Holman K., Tsuda T., Mar L., Foncin J.F., Bruni A.C., Montesi M.P., Sorbi S., Rainero I., Pinessi L., Nee L., Chumakov I., Pollen D., Brookes A., Sanseau P., Polinsky R.J., Wasco W., Da Silva H.A.R., Haines J.L., Pericak-Vance M.A., Tanzi R.E., Roses A.D., Fraser P.E., Rommens J.M., St.George-Hyslop P.H. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 1995, 375:754-760.
9. Goate A., Chartier-Harlin M.C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., Mant R., Newton P., Rooke K., Roques P., Talbot C., Pericak-Vance M., Roses A., Williamson R., Rossor M., Owen M., Hardy J. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 1991, 349:704-706.
10. Chartier-Harlin M.C., Crawford F., Houlden H., Warren A., Hughes D., Fidani L., Goate A., Rossor M., Roques P., Hardy J. Early-onset Alzheimer's disease caused by mutations at codon 717 of the β-amyloid precursor protein gene. Nature 1991, 353:844-846.
11. Kumar-Singh S., Theuns J., Van Broeck B., Pirici D., Vennekens K., Corsmit E., Cruts M., Dermaut B., Wang R., Van Broeckhoven C. Mean age-of-onset of familial Alzheimer disease caused by presenilin mutations correlates with both increased Aβ42 and decreased Aβ40. Hum. Mutat. 2006, 27:686-695.
12. Suzuki N., Cheung T.T., Cai X.D., Odaka A., Otvos L., Eckman C., Golde T.E., Younkin S.G. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science 1994, 264:1336-1340.
13. Kuo Y.M., Beach T.G., Sue L.I., Scott S., Layne K.J., Kokjohn T.A., Kalback W.M., Luehrs D.C., Vishnivetskaya T.A., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., Weller R.O., Roher A.E. The evolution of Aβ peptide burden in the APP23 transgenic mice: implications for Aβ deposition in Alzheimer disease. Mol. Med. 2001, 7:609-618.
14. Lord A., Kalimo H., Eckman C., Zhang X.Q., Lannfelt L., Nilsson L.N. The Arctic Alzheimer mutation facilitates early intraneuronal Aβ aggregation and senile plaque formation in transgenic mice. Neurobiol. Aging 2006, 27:67-77.
15. Borchelt D.R., Thinakaran G., Eckman C.B., Lee M.K., Davenport F., Ratovitsky T., Prada C.M., Kim G., Seekins S., Yager D., Slunt H.H., Wang R., Seeger M., Levey A.I., Gandy S.E., Copeland N.G., Jenkins N.A., Price D.L., Younkin S.G., Sisodia S.S. Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo. Neuron 1996, 17:1005-1013.
16. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-103.
17. McLean C.A., Cherny R.A., Fraser F.W., Fuller S.J., Smith M.J., Konrad V., Bush A.I., Masters C.L. Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 1999, 46:860-866.
18. 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 β peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 1999, 155:853-862.
19. Wang J., Dickson D.W., Trojanowski J.Q., Lee V.M. The levels of soluble versus insoluble brain Aβ distinguish Alzheimer's disease from normal and pathologic aging. Exp. Neurol. 1999, 158:328-337.
20. Gouras G.K., Tsai J., Naslund J., Vincent B., Edgar M., Checler F., Greenfield J.P., Haroutunian V., Buxbaum J.D., Xu H., Greengard P., Relkin N.R. Intraneuronal Aβ42 accumulation in human brain. Am. J. Pathol. 2000, 156:15-20.
21. 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-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842.
22. Lesné S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-β protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
23. Pike C.J., Walencewicz A.J., Glabe C.G., Cotman C.W. In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 1991, 563:311-314.
24. Chromy B.A., Nowak R.J., Lambert M.P., Viola K.L., Chang L., Velasco P.T., Jones B.W., Fernandez S.J., Lacor P.N., Horowitz P., Finch C.E., Krafft G.A., Klein W.L. Self-assembly of Aβ(1-42) into globular neurotoxins. Biochemistry 2003, 42:12749-12760.
25. Bernstein S.L., Dupuis N.F., Lazo N.D., Wyttenbach T., Condron M.M., Bitan G., Teplow D.B., Shea J.E., Ruotolo B.T., Robinson C.V., Bowers M.T. Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 2009, 1:326-331.
26. Parameshwaran K., Sims C., Kanju P., Vaithianathan T., Shonesy B.C., Dhanasekaran M., Bahr B.A., Suppiramaniam V. Amyloid β-peptide Aβ1-42 but not Aβ1-40 attenuates synaptic AMPA receptor function. Synapse 2007, 61:367-374.
27. 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-β. Nat. Neurosci. 2005, 8:1051-1058.
28. Ditaranto K., Tekirian T.L., Yang A.J. Lysosomal membrane damage in soluble Aβ-mediated cell death in Alzheimer's disease. Neurobiol. Dis. 2001, 8:19-31.
29. Bahr B.A. Long-term hippocampal slices: a model system for investigating synaptic mechanisms and pathologic processes. J. Neurosci. Res. 1995, 42:294-305.
30. Bahr B.A., Hoffman K.B., Yang A.J., Hess U.S., Glabe C.G., Lynch G. Amyloid β protein is internalized selectively by hippocampal field CA1 and causes neurons to accumulate amyloidogenic carboxyterminal fragments of the amyloid precursor protein. J. Comp. Neurol. 1998, 397:139-147.
31. Li M., Chen L., Lee D.H., Yu L.C., Zhang Y. The role of intracellular amyloid β in Alzheimer's disease. Prog. Neurobiol. 2007, 83:131-139.
32. Bendiske J., Caba E., Brown Q.B., Bahr B.A. Intracellular deposition, microtubule destabilization, and transport failure: an "early" pathogenic cascade leading to synaptic decline. J. Neuropathol. Exp. Neurol. 2002, 61:640-650.
33. Butler D., Brown Q.B., Chin D.J., Batey L., Karim S., Mutneja M.S., Karanian D.A., Bahr B.A. Cellular responses to protein accumulation involve autophagy and lysosomal enzyme activation. Rejuvenation Res. 2005, 8:227-237.
34. Karanian D.A., Brown Q.B., Makriyannis A., Bahr B.A. Blocking cannabinoid activation of FAK and ERK1/2 compromises synaptic integrity in hippocampus. Eur. J. Pharmacol. 2005, 508:47-56.
35. Karanian D.A., Brown Q.B., Makriyannis A., Kosten T.A., Bahr B.A. Dual modulation of endocannabinoid transport and fatty acid amide hydrolase protects against excitotoxicity. J. Neurosci. 2005, 25:7813-7820.
36. Bahr B.A., Bendiske J., Brown Q.B., Munirathinam S., Caba E., Rudin M., Urwyler S., Sauter A., Rogers G. Survival signaling and selective neuroprotection through glutamatergic transmission. Exp. Neurol. 2002, 174:37-47.
37. Bahr B.A., Hoffman K.B., Kessler M., Hennegriff M., Park G.Y., Yamamoto R.S., Kawasaki B.T., Vanderklish P.W., Hall R.A., Lynch G. Distinct distributions of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor subunits and a related 53,000 Mr antigen (GR53) in brain tissue. Neuroscience 1996, 74:707-721.
38. Brana C., Benham C., Sundstrom L. A method for characterising cell death in vitro by combining propidium iodide staining with immunohistochemistry. Brain Res. Brain Res. Protoc. 2002, 10:109-114.
39. Hilbich C., Kisters-Woike B., Reed J., Masters C.L., Beyreuther K. Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease. J. Mol. Biol. 1991, 218:149-163.
40. 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.
41. Stokin G.B., Lillo C., Falzone T.L., Brusch R.G., Rockenstein E., Mount S.L., Raman R., Davies P., Masliah E., Williams D.S., Goldstein L.S. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005, 307:1282-1288.
42. Shah S.B., Nolan R., Davis E., Stokin G.B., Niesman I., Canto I., Glabe C., Goldstein L.S. Examination of potential mechanisms of amyloid-induced defects in neuronal transport. Neurobiol. Dis. 2009, 36:11-25.
43. Sze C.I., Troncoso J.C., Kawas C., Mouton P., Price D.L., Martin L.J. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J. Neuropathol. Exp. Neurol. 1997, 56:933-944.
44. Heinonen O., Soininen H., Sorvari H., Kosunen O., Paljärvi L., Koivisto E., Riekkinen P.J. Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neuroscience 1995, 64:375-384.
45. Liu J., Chang L., Roselli F., Almeida O.F., Gao X., Wang X., Yew D.T., Wu Y. Amyloid-β induces caspase-dependent loss of PSD-95 and synaptophysin through NMDA receptors. J. Alzheimers Dis. 2010, 22:541-556.
46. O'Nuallain B., Freir D.B., Nicoll A.J., Risse E., Ferguson N., Herron C.E., Collinge J., Walsh D.M. Amyloid β-protein dimers rapidly form stable synaptotoxic protofibrils. J. Neurosci. 2010, 30:14411-14419.
47. Li S., Jin M., Koeglsperger T., Shepardson N.E., Shankar G.M., Selkoe D.J. Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J. Neurosci. 2011, 31:6627-6638.
48. Rammes G., Hasenjäger A., Sroka-Saidi K., Deussing J.M., Parsons C.G. Therapeutic significance of NR2B-containing NMDA receptors and mGluR5 metabotropic glutamate receptors in mediating the synaptotoxic effects of β-amyloid oligomers on long-term potentiation (LTP) in murine hippocampal slices. Neuropharmacology 2011, 60:982-990.
49. Czogalla A., Sikorski A.F. Spectrin and calpain: a 'target' and a 'sniper' in the pathology of neuronal cells. Cell. Mol. Life Sci. 2005, 62:1913-1924.
50. Miyamoto E. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J. Pharmacol. Sci. 2006, 100:433-442.
51. Proctor D.T., Coulson E.J., Dodd P.R. Post-synaptic scaffolding protein interactions with glutamate receptors in synaptic dysfunction and Alzheimer's disease. Prog. Neurobiol. 2011, 93:509-521.
52. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., 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.
53. DeKosky S.T., Scheff S.W. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann. Neurol. 1990, 27:457-464.
54. DeKosky S.T., Scheff S.W., Styren S.D. Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration 1996, 5:417-421.
55. Almeida C.G., Tampellini D., Takahashi R.H., Greengard P., Lin M.T., Snyder E.M., Gouras G.K. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol. Dis. 2005, 20:187-198.
56. Verges D.K., Restivo J.L., Goebel W.D., Holtzman D.M., Cirrito J.R. Opposing synaptic regulation of amyloid-β metabolism by NMDA receptors in vivo. J. Neurosci. 2011, 31:11328-11337.
57. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., Sabatini B.L. Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 2007, 27:2866-2875.
58. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42:631-639.
59. Giannakopoulos P., Hof P.R., Michel J.P., Guimon J., Bouras C. Cerebral cortex pathology in aging and Alzheimer's disease: a quantitative survey of large hospital-based geriatric and psychiatric cohorts. Brain Res. Brain Res. Rev. 1997, 25:217-245.
60. Crystal H., Dickson D., Fuld P., Masur D., Scott R., Mehler M., Masdeu J., Kawas C., Aronson M., Wolfson L. Clinico-pathologic studies in dementia: nondemented subjects with pathologically confirmed Alzheimer's disease. Neurology 1988, 38:1682-1687.
61. Dickson D.W., Crystal H.A., Mattiace L.A., Masur D.M., Blau A.D., Davies P., Yen S.H., Aronson M.K. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol. Aging 1992, 13:179-189.
62. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
63. Lacor P.N., Buniel M.C., Furlow P.W., Sanz Clemente A., Velasco P.T., Wood M., Viola K.L., Klein W.L. Aβ 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.
64. Rebolledo D.L., Aldunate R., Kohn R., Neira I., Minniti A.N., Inestrosa N.C. Copper reduces Aβ oligomeric species and ameliorates neuromuscular synaptic defects in a C. elegans model of inclusion body myositis. J. Neurosci. 2011, 31:10149-10158.
65. 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. β-Amyloid monomers are neuroprotective. J. Neurosci. 2009, 29:10582-10587.
66. Butler D., Hwang J., Estick C., Nishiyama A., Kumar S.S., Baveghems C., Young-Oxendine H.B., Wisniewski M.L., Charalambides A., Bahr B.A. Protective effects of positive lysosomal modulation in Alzheimer's disease transgenic mouse models. PLoS One 2011, 6:e20501.