Amyloid-β1-40 inhibits amyloid-β1-42 induced activation of cytoplasmic phospholipase A2 and synapse degeneration

Journal of Alzheimer's Disease

Volumn 21, Issue 3, 2010, Pages 985-993

  Bate, Clive ^a   Williams, Alun ^a,b  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Alzheimer's disease; amyloid; oligomers; synapses; synaptophysin

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; FLUORESCENT DYE; OLIGOMER; PHOSPHOLIPASE A2; SYNAPTOPHYSIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENZYME ACTIVATION; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONTENT; SYNAPSE; SYNAPSE VESICLE; SYNAPTOSOME;

EID: 77957261220     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100528     Document Type: Article

References (48)

1. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298, 789791.
2. Coleman PD,Yao PJ (2003) Synaptic slaughter inAlzheimer's disease. Neurobiol Aging 24, 10231027.
3. Heinonen O, Soininen H, Sorvari H, Kosunen O, Paljarvi L, Koivisto E, Riekkinen, Sr. (1995) Loss of synaptophysinlike immunoreactivity in the hippocampal formation is an early phenomenon in alzheimer's disease. Neuroscience 64, 375384.
4. Reddy PH,Mani G, Park BS, Jacques J,Murdoch G,Whetsell W, Jr., Kaye J, Manczak M (2005) Differential loss of synaptic proteins in Alzheimer's disease: Implications for synaptic dysfunction. J Alzheimers Dis 7, 103117. (Pubitemid 40592184)
5. Elferink LA, Scheller RH (1993) Synaptic vesicle proteins and regulated exocytosis. J Cell Sci 17, 7579. (Pubitemid 24041282)
6. Vassar R, Citron M (2000) A-generating enzymes: Recent advances in- and secretase research. Neuron 27, 419422.
7. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353356. (Pubitemid 34790756)
8. 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 (1998) Diffusible, nonfibrillar ligands derived from A-1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95, 64486453.
9. Chromy BA, Nowak RJ, Lambert MP, Viola KL, Chang L, Velasco PT, Jones BW, Fernandez SJ, Lacor PN, Horowitz P, Finch CE, Krafft GA, Klein WL (2003) Selfassembly of A-1-42 into globular neurotoxins. Biochemistry 42, 1274912760.
10. GeorganopoulouDG, Chang L,NamJM, ThaxtonCS,Mufson EJ, Klein WL, Mirkin CA (2005) Nanoparticlebased detection in cerebral spinal fluid of a soluble pathogenic biomarker for Alzheimer's disease. Proc Natl Acad Sci U S A 102, 22732276. (Pubitemid 40279365)
11. Cheng IH, ScearceLevie K, Legleiter J, Palop JJ, Gerstein H, BienLy N, Puolivali J, Lesne S, Ashe KH, Muchowski PJ, Mucke L (2007) Accelerating amyloid- fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem 282, 2381823828.
12. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE,KrafftGA,KleinWL (2003)Alzheimer's diseaseaffected brain: Presence of oligomeric A- ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci U S A 100, 1041710422.
13. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, LambertMP,Velasco PT, Bigio EH, Finch CE, Krafft GA, Klein WL (2004) Synaptic Targeting by Alzheimer'sRelated Amyloid b Oligomers. J Neurosci 24, 1019110200. (Pubitemid 39492046)
14. Terry RD,Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30, 572580.
15. DeKosky ST, Scheff SW(1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 27, 457464.
16. Hamos JE, DeGennaro LJ, Drachman DA (1989) Synaptic loss in Alzheimer's disease and other dementias. Neurology 39, 355361. (Pubitemid 19094725)
17. Bate C, Tayebi M, Williams A (2008) Ginkgolides protect against amyloid-1-42mediated synapse damage in vitro. Mol Neurodegen 3, 1.
18. Dahlgren KN, Manelli AM, Stine WB, Jr., Baker LK, Krafft GA, LaDu MJ (2002) Oligomeric and fibrillar species of amyloid- peptides differentially affect neuronal viability. J Biol Chem 277, 3204632053.
19. Yan Y, Wang C (2007) A-40 protects nontoxic A-42 monomer from aggregation. J Mol Biol 369, 909916.
20. Murray MM, Bernstein SL, Nyugen V, Condron MM, Teplow DB, Bowers MT (2009) Amyloid- protein: A-40 inhibits A-42 oligomerization. J Am Chem Soc 131, 63166317.
21. Bate C, TayebiM, SalmonaM,Diomede L,Williams A (2010) Polyunsaturated fatty acids protect against prionmediated synapse damage in vitro. Neurotox Res 17, 203214.
22. Thais ME, Carqueja CL, Santos TG, Silva RV, Stroeh E, Machado RS, Wahlheim DO, Bianchin MM, Sakamoto AC, Brentani RR, Martins VR, Walz R, Tasca CI (2006) Synaptosomal glutamate release and uptake inmice lacking the cellular prion protein. Brain Res 1075, 1319.
23. Podlisny MB, Ostaszewski BL, Squazzo SL, Koo EH, Rydell RE, Teplow DB, Selkoe DJ (1995) Aggregation of secreted amyloid-protein into sodium dodecyl sulfatestable oligomers in cell culture. J Biol Chem 270, 95649570.
24. Cleary JP,WalshDM,Hofmeister JJ, Shankar GM,Kuskowski MA, Selkoe DJ, Ashe KH (2005) Natural oligomers of the amyloidb protein specifically disrupt cognitive function. Nat Neurosci 8, 7984.
25. Jan A, Gokce O, LuthiCarter R, Lashuel HA (2008) The ratio of monomeric to aggregated forms of A-40 and A-42 is an important determinant of amyloid- aggregation, fibrillogenesis, and toxicity. J Biol Chem 283, 2817628189.
26. Jeffrey M, Halliday WG, Bell J, Johnston AR, MacLeod NK, Ingham C, Sayers AR, Brown DA, Fraser JR (2000) Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapieinfected murine hippocampus. Neuropath Appl Neurobiol 26, 4154. (Pubitemid 30145305)
27. Ferrer I (2002) Synaptic pathology and cell death in the cerebellum in CreutzfeldtJakob disease. Cerebellum 1, 213222. (Pubitemid 44133831)
28. Klingauf J, Kavalali ET, Tsien RW (1998) Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394, 581585. (Pubitemid 28366833)
29. CousinMA,Robinson PJ (1999)Mechanisms of synaptic vesicle recycling illuminated by fluorescent dyes. J Neurochem 73, 22272239.
30. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid- protein potently inhibit hippocampal longterm potentiation in vivo. Nature 416, 535539.
31. Moskowitz N, Schook W, Puszkin S (1984) Regulation of endogenous calciumdependent synaptic membrane phospholipase A2. Brain Res 290, 273279. (Pubitemid 14216989)
32. MoskowitzN, SchookW, Puszkin S (1982) Interaction of brain synaptic vesicles induced by endogenous Ca2+dependent phospholipase A2. Science 216, 305307.
33. Kriem B, Sponne I, Fifre A, MalaplateArmand C, Lozac'hPillot K, Koziel V, YenPotin FT, Bihain B, Oster T, Olivier JL, Pillot T (2005) Cytosolic phospholipase A2 mediates neuronal apoptosis induced by soluble oligomers of the amyloid- peptide. FASEB J 19, 8587.
34. SanchezMejia RO, Newman JW, Toh S, Yu GQ, Zhou Y, Halabisky B, Cisse M, ScearceLevie K, Cheng IH, Gan L, Palop JJ, Bonventre JV, Mucke L (2008) Phospholipase A2 reduction ameliorates cognitive deficits in a mouse model of Alzheimer's disease. Nat Neurosci 11, 13111318.
35. Lacor PN, Buniel MC, Furlow PW, Sanz Clemente A, Velasco PT, Wood M, Viola KL, Klein WL (2007) A- oligomerinduced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's Disease. J Neurosci 27, 796807.
36. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid- protein induce reversible synapse loss by modulating an NMDAtype glutamate receptordependent signaling pathway. J Neurosci 27, 28662875.
37. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid-peptide. Nat Rev Mol Cell Biol 8, 101112. (Pubitemid 46432529)
38. Passer B, Pellegrini L, Russo C, Siegel RM, Lenardo MJ, Schettini G, Bachmann M, Tabaton M, D'Adamio L (2000) Generation of an Apoptotic Intracellular Peptide by Secretase Cleavage of Alzheimer's Amyloid- Protein Precursor. J Alzheimers Dis 2, 289301.
39. Borchelt DR, Thinakaran G, Eckman CB, Lee MK, Davenport F, Ratovitsky T, Prada CM, Kim G, Seekins S, Yager D, Slunt HH,Wang R, Seeger M, Levey AI, Gandy SE, Copeland NG, Jenkins NA, Price DL, Younkin SG, Sisodia SS (1996) Familial Alzheimer's diseaselinked presenilin 1 variants elevate A-1-42/1-40 ratio in vitro and in vivo. Neuron 17, 10051013.
40. Salmona M, Morbin M, Massignan T, Colombo L,Mazzoleni G, Capobianco R, Diomede L, Thaler F, Mollica L, Musco G, Kourie JJ, Bugiani O, Sharma D, Inouye H, Kirschner DA, Forloni G, Tagliavini F (2003) Structural properties of GerstmannStrausslerScheinker disease amyloid protein. J Biol Chem 278, 4814648153. (Pubitemid 37523267)
41. Darios F, Connell E, Davletov B (2007) Phospholipases and fatty acid signalling in exocytosis. J Physiol 585, 699704. (Pubitemid 350278708)
42. Stephenson DT, Lemere CA, Selkoe DJ, Clemens JA (1996) Cytosolic phospholipase A2 (cPLA2) immunoreactivity is elevated in Alzheimer's disease brain. Neurobiol Dis 3, 5163. (Pubitemid 26145405)
43. Lehtonen JY, Holopainen JM,Kinnunen PK (1996) Activation of phospholipase A2 by amyloid-peptides in vitro. Biochemistry 35, 94079414.
44. Bate C, Williams A (2007) Squalestatin protects neurons and reduces the activation of cytoplasmic phospholipase A2 by A-1-42. Neuropharmacology 53, 222231.
45. Bate C, Tayebi M, Williams A (2010) Phospholipase A2 inhibitors protect against prion and A- mediated synapse degeneration. Mol Neurodegen 5, 13.
46. Pike CJ, Burdick D,Walencewicz AJ, Glabe CG, Cotman CW (1993) Neurodegeneration induced by bamyloid peptides in vitro: The role of peptide assembly state. J Neurosci 13, 16761687. (Pubitemid 23095409)
47. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, Bird TD, Hardy J, Hutton M, Kukull W, Larson E, Levy Lahad E, Viitanen M, Peskind E, Poorkaj P, Schellenberg G, Tanzi R, Wasco W, Lannfelt L, Selkoe D, Younkin S (1996) Secreted amyloid bprotein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 2, 864870. (Pubitemid 26296755)
48. Kim J, Onstead L, Randle S, Price R, Smithson L, Zwizinski C, Dickson DW, Golde T, McGowan E (2007) A-40 inhibits amyloid deposition in vivo. J Neurosci 27, 627633.