High throughput monitoring of amyloid-β42 assembly into soluble oligomers achieved by sensitive conformation state-dependent immunoassays

Journal of Alzheimer's Disease

Volumn 25, Issue 4, 2011, Pages 655-669

  Zhao, Wei Qin ^a   Toolan, Dawn ^a   Hepler, Robert W ^a   Wolfe, Abigail L ^a   Yu, Yuanjiang ^a   Price, Eric ^a   Uebele, Victor N ^a   Schachter, Joel B ^a   Reynolds, Ian J ^a   Renger, John J ^a   McCampbell, Alexander ^a   Ray, William J ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Alzheimer's disease; drug development; oligomer inhibitor

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; EPITOPE; MONOMER; OLIGOMER;

AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DYNAMIC LIGHT SCATTERING; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN TISSUE; IMMUNOASSAY; IMMUNOREACTIVITY; LIGHT SCATTERING; NERVE CELL; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREDICTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; WESTERN BLOTTING;

EID: 80052838813     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-102022     Document Type: Article

References (48)

1. Gandy S, Caporaso G, Buxbaum J, Frangione B, Greengard P (1994) APP processing, A beta-amyloidogenesis, and the pathogenesis of Alzheimer's disease. Neurobiol Aging 15, 253-256. (Pubitemid 24120839)
2. Marotta CA, Majocha RE, Tate B (1992) Molecular and cellular biology ofAlzheimer amyloid. J Mol Neurosci3, 111-125.
3. Selkoe DJ, Yamazaki T, Citron M, Podlisny MB, Koo EH, Teplow DB, Haass C (1996) The role of APP processing and trafficking pathways in the formation of amyloid beta-protein. Ann N Y Acad Sci 777, 57-64. (Pubitemid 26149170)
4. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, Lambert MP, Velasco PT, Bigio EH, Finch CE, Krafft GA, Klein WL (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 24, 10191-10200. (Pubitemid 39492046)
5. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocam-pal long-term potentiation in vivo. Nature 416, 535-539. (Pubitemid 34288854)
6. Selkoe DJ (2008) Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 192, 106-113.
7. Tomiyama T, Matsuyama S, Iso H, Umeda T, Takuma H, Ohnishi K, Ishibashi K, Teraoka R, Sakama N, Yamashita T, Nishitsuji K, Ito K, Shimada H, Lambert MP, Klein WL, Mori H (2010) A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphory-lation, glial activation, and neuronal loss in vivo. J Neurosci 30, 4845-4856.
8. Balducci C, Beeg M, Stravalaci M, Bastone A, Sclip A, Biasini E, Tapella L, Colombo L, Manzoni C, Borsello T, Chiesa R, Gobbi M, Salmona M, Forloni G (2010) Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc Natl Acad Sci USA 107, 2295-2300.
9. Dosanjh LE, Brown MK, Rao G, Link CD, Luo Y (2010) Behavioral phenotyping of a transgenic Caenorhabditis ele-gans expressing neuronal amyloid-beta. J Alzheimers Dis 19, 681-690.
10. Head E, Pop V, Vasilevko V, Hill M, Saing T, Sarsoza F, Nistor M, Christie LA, Milton S, Glabe C, Barrett E, Cribbs D (2008) Atwo-year study withfibrillar beta-amyloid (Abeta) immunization in aged canines: effects on cognitive function and brain Abeta. J Neurosci 28, 3555-3566.
11. Lesne S, Kotilinek L, Ashe KH (2008) Plaque-bearing mice with reduced levels of oligomeric amyloid-beta assemblies have intact memory function. Neuroscience 151, 745-749.
12. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27, 2866-2875. (Pubitemid 46438992)
13. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14, 837-842.
14. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocam-pal long-term potentiation in vivo. Nature 416, 535-539. (Pubitemid 34288854)
15. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52, 831-843. (Pubitemid 44828454)
16. Zempel H, Thies E, Mandelkow E, Mandelkow EM (2010) Abeta oligomers cause localized Ca (2 +) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30, 11938-11950.
17. Zhao WQ, Santini F, Breese R, Ross D, Zhang XD, Stone DJ, Ferrer M, Townsend M, Wolfe AL, Seager MA, Kinney GG, Shughrue PJ, Ray WJ (2010) Inhibition of calcineurin-mediated endocytosis and alpha-amino-3-hydroxy-5- methyl-4-isoxazolepropionic acid (AMPA) receptors prevents amyloid beta oligomer-induced synaptic disruption. J Biol Chem 285, 7619-7632.
18. Hawkes CA, Deng LH, Shaw JE, Nitz M, McLaurin J (2010) Small molecule beta-amyloid inhibitors that stabilize protofibrillar structures in vitro improve cognition and pathology in a mouse model of Alzheimer's disease. Eur J Neurosci 31, 203-213.
19. Townsend M, Cleary JP, Mehta T, Hofmeister J, Lesne S, O'Hare E, Walsh DM, Selkoe DJ (2006) Orally available compound prevents deficits in memory caused by the Alzheimer amyloid-beta oligomers. Ann Neurol 60, 668-676. (Pubitemid 46048484)
20. McLaurin J, Golomb R, Jurewicz A, Antel JP, Fraser PE (2000) Inositol stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid beta peptide and inhibit abeta-induced toxicity. J Biol Chem 275, 18495-18502. (Pubitemid 30414810)
21. Teplow DB, Lazo ND, Bitan G, Bernstein S, Wyttenbach T, Bowers MT, Baumketner A, Shea JE, Urbanc B, Cruz L, Borreguero J, Stanley HE (2006) Elucidating amyloid beta-protein folding and assembly: A multidisciplinary approach. Acc Chem Res 39, 635-645.
22. Urbanc B, Betnel M, Cruz L, Bitan G, Teplow DB (2010) Elucidation of amyloid beta-protein oligomerization mechanisms: discrete molecular dynamics study. J Am Chem Soc 132, 4266-4280.
23. Teplow DB (2006) Preparation of amyloid beta-protein for structural and functional studies. Methods Enzymol 413, 20-33. (Pubitemid 44528683)
24. Lee VM (2002) Amyloid binding ligands as Alzheimer's disease therapies. Neurobiol Aging 23, 1039-1042. (Pubitemid 35447785)
25. LeVine H III (2006) Biotin-avidin interaction-based screening assay for Alzheimer's beta-peptide oligomer inhibitors. Anal Biochem 356, 265-272.
26. LeVine H III, Ding Q, Walker JA, Voss RS, Augelli-Szafran CE (2009) Clioquinol and other hydroxyquinoline derivatives inhibit Abeta (1-42) oligomer assembly. Neurosci Lett 465, 99-103.
27. Bitan G, Lomakin A, Teplow DB (2001) Amyloid beta-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking ofunmodified proteins. J Biol Chem 276, 35176-35184.
28. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, Teplow DB (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc Natl Acad Sci USA 100, 330-335. (Pubitemid 36078074)
29. Bitan G, Vollers SS, Teplow DB (2003) Elucidationofprimary structure elements controlling early amyloid beta-protein oligomerization. J Biol Chem 278, 34882-34889. (Pubitemid 37102247)
30. Urbanc B, Cruz L, Yun S, Buldyrev SV, Bitan G, Teplow DB, Stanley HE (2004) In silico study of amyloid beta-protein folding and oligomerization. Proc Natl Acad Sci USA 101, 17345-17350. (Pubitemid 39657406)
31. Baumketner A, Bernstein SL, Wyttenbach T, Bitan G, Teplow DB, Bowers MT, Shea JE (2006) Amyloid beta-protein monomer structure: a computational and experimental study. Protein Sci 15, 420-428.
32. Bernstein SL, Dupuis NF, Lazo ND, Wyttenbach T, Condron MM, Bitan G, Teplow DB, Shea JE, Ruotolo BT, Robinson CV, Bowers MT (2009) Amyloid-beta protein oligomeriza-tion and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat Chem 1, 326-331.
33. Barghorn S, Nimmrich V, Striebinger A, Krantz C, Keller P, Janson B, Bahr M, Schmidt M, Bitner RS, Harlan J, Barlow E, Ebert U, Hillen H (2005) Globular amyloid beta-peptide oligomer-a homogenous and stable neuropathological protein in Alzheimer's disease. J Neurochem 95, 834-847. (Pubitemid 41567174)
34. Ahmed M, Davis J, Aucoin D, Sato T, Ahuja S, Aimoto S, Elliott JI, Van Nostrand WE, Smith SO (2010) Structural conversion of neurotoxic amyloid-beta (1-42) oligomers to fibrils. Nat Struct Mol Biol 17, 561-567.
35. Eglen RM, Reisine T, Roby P, Rouleau N, Illy C, Bosse R, Bielefeld M (2008) The Use of Alpha Screen Technology in HTS: Current Status. Curr Chem Genomics 1, 2-10.
36. El-Agnaf OM, Mahil DS, Patel BP, Austen BM (2000) Oligomerization and toxicity of beta-amyloid-42 implicated in Alzheimer's disease. Biochem Biophys Res Commun 273, 1003-1007. (Pubitemid 30481069)
37. Gandy S, Simon AJ, Steele JW, Lublin AL, Lah JJ, Walker LC, Levey AI, Krafft GA, Levy E, Checler F, Glabe C, Bilker WB, Abel T, Schmeidler J, Ehrlich ME (2010) Days to criterion as an indicator of toxicity associated with human Alzheimer amyloid-beta oligomers. Ann Neurol 68, 220-230.
38. Hepler RW, Grimm KM, Nahas DD, Breese R, Dodson EC, Acton P, Keller PM, Yeager M, Wang H, Shughrue P, Kin-ney G, Joyce JG (2006) Solution state characterization of amyloid beta-derived diffusible ligands. Biochemistry 45, 15157-15167. (Pubitemid 46032442)
39. Zhao WQ, Santini F, Breese R, Ross D, Zhang XD, Stone DJ, Ferrer M, Townsend M, Wolfe AL, Seager MA, Kinney GG, Shughrue PJ, Ray WJ (2010) Inhibition of calcineurin-mediated endocytosis and alpha-amino-3-hydroxy-5- methyl-4-isoxazolepropionic acid (AMPA) receptors prevents amyloid beta oligomer-induced synaptic disruption. J Biol Chem 285, 7619-7632.
40. 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) Self-assembly of Abeta (1-42) into globular neurotoxins. Biochemistry 42, 12749-12760. (Pubitemid 37385806)
41. 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 Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95, 6448-6453.
42. Bitan G, Teplow DB (2005) Preparation of aggregate-free, low molecular weight amyloid-beta for assembly and toxicity assays. Methods Mol Biol 299, 3-9.
43. Finder VH, Glockshuber R (2007) Amyloid-beta aggregation. Neurodegener Dis 4, 13-27.
44. Adessi C, Frossard MJ, Boissard C, Fraga S, Bieler S, Ruckle T, Vilbois F, Robinson SM, Mutter M, Banks WA, Soto C (2003) Pharmacological profiles of peptide drug candidates for the treatment of Alzheimer's disease. J Biol Chem 278, 13905-13911. (Pubitemid 36799931)
45. Zhang JH, Chung TD, Oldenburg KR (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4, 67-73. (Pubitemid 29278954)
46. Fukumoto H, Tokuda T, Kasai T, Ishigami N, Hidaka H, Kondo M, Allsop D, Nakagawa M (2010) High-molecular-weight {beta}-amyloid oligomers are elevated in cerebro-spinal fluid of Alzheimer patients. FASEB J 24, 2716-2726.
47. Moore BD, Rangachari V, Tay WM, Milkovic NM, Rosenberry TL (2009) Biophysical analyses of synthetic amyloid-beta (1-42) aggregates before and after cova-lent cross-linking. Implications for deducing the structure of endogenous amyloid-beta oligomers. Biochemistry 48, 11796-11806.
48. Murphy MP, LeVine H III (2010) Alzheimer's disease and the amyloid-beta peptide. J Alzheimers Dis 19, 311-323.