Development and validation of a yeast high-throughput screen for inhibitors of Aβ 42 oligomerization

DMM Disease Models and Mechanisms

Volumn 4, Issue 6, 2011, Pages 822-831

  Park, Sei Kyoung ^a   Pegan, Scott D ^b   Mesecar, Andrew D ^c   Jungbauer, Lisa M ^a,d   LaDu, Mary Jo ^a   Liebman, Susan W ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF DENVER   (United States)

^c PURDUE UNIVERSITY   (United States)

^d MEDTRONIC INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,3 DIMETHYLPHENYL) 4 (2 FUROYL) PIPERAZINE; 2 (4 METHOXYPHENYL) 1,3 BENZOXAZOL 5 AMINE; AMYLOID BETA PROTEIN[1-42]; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; FUNGUS GROWTH; GROWTH INHIBITION; HIGH THROUGHPUT SCREENING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; YEAST;

AMYLOID BETA-PEPTIDES; DRUG EVALUATION, PRECLINICAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HIGH-THROUGHPUT SCREENING ASSAYS; MODELS, BIOLOGICAL; PEPTIDE FRAGMENTS; PILOT PROJECTS; POLYMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; REPRODUCIBILITY OF RESULTS; SACCHAROMYCES CEREVISIAE;

EID: 81455128231     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.007963     Document Type: Article

References (70)

1. Adlard, P. A., Cherny, R. A., Finkelstein, D. I., Gautier, E., Robb, E., Cortes, M., Volitakis, I., Liu, X., Smith, J. P., Perez, K. et al. (2008). Rapid restoration of cognition in Alzheimer's transgenic mice with 8-hydroxy quinoline analogs is associated with decreased interstitial Abeta. Neuron 59, 43-55. (Pubitemid 351905863)
2. Alavez, S., Vantipalli, M. C., Zucker, D. J. S., Klang, I. M. and Lithgow, G. J. (2011). Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472, 226-230.
3. Amijee, H. and Scopes, D. I. (2009). The quest for small molecules as amyloid inhibiting therapies for Alzheimer's disease. J. Alzheimers Dis. 17, 33-47.
4. Amijee, H., Madine, J., Middleton, D. A. and Doig, A. J. (2009). Inhibitors of protein aggregation and toxicity. Biochem. Soc. Trans. 37, 692-696.
5. Bagriantsev, S. and Liebman, S. (2006). Modulation of Abeta42 low-n oligomerization using a novel yeast reporter system. BMC Biol. 4, 32.
6. Bharadwaj, P., Martins, R. and Macreadie, I. (2010). Yeast as a model for studying Alzheimer's disease. FEMS Yeast Res. 10, 961-969.
7. Bitan, G., Fradinger, E. A., Spring, S. M. and Teplow, D. B. (2005). Neurotoxic protein oligomers-what you see is not always what you get. Amyloid 12, 88-95. (Pubitemid 40978716)
8. Bradley, M. E., Bagriantsev, S., Vishveshwara, N. and Liebman, S. W. (2003). Guanidine reduces stop codon read-through caused by missense mutations in SUP35 or SUP45. Yeast 20, 625-632. (Pubitemid 36603569)
9. Caine, J., Sankovich, S., Antony, H., Waddington, L., Macreadie, P., Varghese, J. and Macreadie, I. (2007). Alzheimer's Abeta fused to green fluorescent protein induces growth stress and a heat shock response. FEMS Yeast Res. 7, 1230-1236. (Pubitemid 47622047)
10. Chang, L., Bakhos, L., Wang, Z., Venton, D. L. and Klein, W. L. (2003). Femtomole immunodetection of synthetic and endogenous amyloid-beta oligomers and its application to Alzheimer's disease drug candidate screening. J. Mol. Neurosci. 20, 305-313. (Pubitemid 38146987)
11. Chen, J., Armstrong, A. H., Koehler, A. N. and Hecht, M. H. (2010). Small molecule microarrays enable the discovery of compounds that bind the Alzheimer's Ab peptide and reduce its cytotoxicity. J. Am. Chem. Soc. 132, 17015-17022.
12. Cheng, I. H., Scearce-Levie, K., Legleiter, J., Palop, J. J., Gerstein, H., Bien-Ly, N., Puolivali, J., Lesne, S., Ashe, K. H., Muchowski, P. J. et al. (2007). Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J. Biol. Chem. 282, 23818-23828. (Pubitemid 47328006)
13. Chernoff, Y. O., Derkach, I. L. and Inge-Vechtomov, S. G. (1993). Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr. Genet. 24, 268-270. (Pubitemid 23294059)
14. 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. et al. (2003). Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 42, 12749-12760.
15. Congreve, M., Carr, R., Murray, C. and Jhoti, H. (2003). A 'rule of three' for fragment based lead discovery? Drug Discov. Today 8, 876-877.
16. Dahlgren, K. N., Manelli, A. M., Stine, W. B., Jr, Baker, L. K., Krafft, G. A. and LaDu, M. J. (2002). Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 277, 32046-32053. (Pubitemid 34969015)
17. De Felice, F. G. and Ferreira, S. T. (2002). Beta-amyloid production, aggregation, and clearance as targets for therapy in Alzheimer's disease. Cell. Mol. Neurobiol. 22, 545-563. (Pubitemid 36169208)
18. Derkatch, I. L., Chernoff, Y. O., Kushnirov, V. V., Inge-Vechtomov, S. G. and Liebman, S. W. (1996). Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144, 1375-1386. (Pubitemid 26427888)
19. Dunstan, H. M., Ludlow, C., Goehle, S., Cronk, M., Szankasi, P., Evans, D. R., Simon, J. A. and Lamb, J. R. (2002). Cell-based assays for identification of novel doublestrand break-inducing agents. J. Natl. Cancer Inst. 94, 88-94. (Pubitemid 34121287)
20. Estrada, L. D. and Soto, C. (2007). Disrupting beta-amyloid aggregation for Alzheimer disease treatment. Curr. Top. Med. Chem. 7, 115-126. (Pubitemid 46062400)
21. Faux, N. G., Ritchie, C. W., Gunn, A., Rembach, A., Tsatsanis, A., Bedo, J., Harrison, J., Lannfelt, L., Blennow, K., Zetterberg, H. et al. (2010). PBT2 rapidly improves cognition in Alzheimer's Disease: additional phase II analyses. J. Alzheimers Dis. 20, 509-516.
22. Glabe, C. C. (2005). Amyloid accumulation and pathogensis of Alzheimer's disease: significance of monomeric, oligomeric and fibrillar Abeta. Subcell. Biochem. 38, 167-177.
23. Gong, Y., Chang, L., Viola, K. L., Lacor, P. N., Lambert, M. P., Finch, C. E., Krafft, G. A. and Klein, W. L. (2003). Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. USA 100, 10417-10422. (Pubitemid 37071893)
24. Hamaguchi, T., Ono, K., Murase, A. and Yamada, M. (2009). Phenolic compounds prevent Alzheimer's pathology through different effects on the amyloid-{beta} aggregation pathway. Am. J. Pathol. 63, 1538-1552.
25. Hardy, J. A. and Higgins, G. A. (1992). Alzheimer's disease: the amyloid cascade hypothesis. Science 256, 184-185.
26. Harper, J. D., Wong, S. S., Lieber, C. M. and Lansbury, P. T., Jr (1999). Assembly of A beta amyloid protofibrils: an in vitro model for a possible early event in Alzheimer's disease. Biochemistry 38, 8972-8980.
27. Hepler, R. W., Grimm, K. M., Nahas, D. D., Breese, R., Dodson, E. C., Acton, P., Keller, P. M., Yeager, M., Wang, H., Shughrue, P. et al. (2006). Solution state characterization of amyloid beta-derived diffusible ligands. Biochemistry 45, 15157-15167. (Pubitemid 46032442)
28. Hilbich, C., Kisters-Woike, B., Reed, J., Masters, C. L. and Beyreuther, K. (1992). Substitutions of hydrophobic amino acids reduce the amyloidogenicity of Alzheimer's disease beta A4 peptides. J. Mol. Biol. 228, 460-473. (Pubitemid 23007569)
29. Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F. and Cole, G. (1996). Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102. (Pubitemid 26332733)
30. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W. and Glabe, C. G. (2003). Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489. (Pubitemid 36444329)
31. Kim, W., Kim, Y., Min, J., Kim, D. J., Chang, Y. T. and Hecht, M. H. (2006). A highthroughput screen for compounds that inhibit aggregation of the Alzheimer's peptide. ACS Chem. Biol. 1, 461-469.
32. Klein, W. L., Krafft, G. A. and Finch, C. E. (2001). Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci. 24, 219-224. (Pubitemid 32204378)
33. Klyubin, I., Betts, V., Welzel, A. T., Blennow, K., Zetterberg, H., Wallin, A., Lemere, C. A., Cullen, W. K., Peng, Y., Wisniewski, T. et al. (2008). Amyloid beta protein dimer-containing human CSF disrupts synaptic plasticity: prevention by systemic passive immunization. J. Neurosci. 28, 4231-4237.
34. Kokkoni, N., Stott, K., Amijee, H., Mason, J. M. and Doig, A. J. (2006). N-Methylated peptide inhibitors of beta-amyloid aggregation and toxicity. Optimization of the inhibitor structure. Biochemistry 45, 9906-9918. (Pubitemid 44257436)
35. Lambert, M. P., Barlow, A. K., Chromy, B. A., Edwards, C., Freed, R., Liosatos, M., Morgan, T. E., Rozovsky, I., Trommer, B., Viola, K. L. et al. (1998). Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 95, 6448-6453.
36. Lambert, M. P., Viola, K. L., Chromy, B. A., Chang, L., Morgan, T. E., Yu, J., Venton, D. L., Krafft, G. A., Finch, C. E. and Klein, W. L. (2001). Vaccination with soluble Abeta oligomers generates toxicity-neutralizing antibodies. J. Neurochem. 79, 595-605. (Pubitemid 33029933)
37. Lee, E. B., Leng, L. Z., Zhang, B., Kwong, L., Trojanowski, J. Q., Abel, T. and Lee, V. M. (2006). Targeting amyloid-beta peptide (Abeta) oligomers by passive immunization with a conformation-selective monoclonal antibody improves learning and memory in Abeta precursor protein (APP) transgenic mice. J. Biol. Chem. 281, 4292-4299. (Pubitemid 43847859)
38. Lee, L. L., Ha, H., Chang, Y. T. and DeLisa, M. P. (2009). Discovery of amyloid-beta aggregation inhibitors using an engineered assay for intracellular protein folding and solubility. Protein Sci. 18, 277-286.
39. Lesne, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M. and Ashe, K. H. (2006). A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357.
40. Liu, Y. and Schubert, D. (2006). Treating Alzheimer's disease by inactivating bioactive amyloid beta peptide. Curr. Alzheimer Res. 3, 129-135.
41. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961. (Pubitemid 28328001)
42. Macreadie, I., Lotfi-Miri, M., Mohotti, S., Shapira, D., Bennett, L. and Varghese, J. (2008). Validation of folate in a convenient yeast assay suited for identification of inhibitors of Alzheimer's amyloid-beta aggregation. J. Alzheimers Dis. 15, 391-396.
43. McLaurin, J., Golomb, R., Jurewicz, A., Antel, J. P. and Fraser, P. E. (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)
44. McLaurin, J., Kierstead, M. E., Brown, M. E., Hawkes, C. A., Lambermon, M. H., Phinney, A. L., Darabie, A. A., Cousins, J. E., French, J. E., Lan, M. F. et al. (2006). Cyclohexanehexol inhibitors of Abeta aggregation prevent and reverse Alzheimer phenotype in a mouse model. Nat. Med. 12, 801-808. (Pubitemid 44050070)
45. Morimoto, A., Irie, K., Murakami, K., Masuda, Y., Ohigashi, H., Nagao, M., Fukuda, H., Shimizu, T. and Shirasawa, T. (2004). Analysis of the secondary structure of beta-amyloid (Abeta42) fibrils by systematic proline replacement. J. Biol. Chem. 279, 52781-52788. (Pubitemid 39656654)
46. Nakagami, Y., Nishimura, S., Murasugi, T., Kubo, T., Kaneko, I., Meguro, M., Marumoto, S., Kogen, H., Koyama, K. and Oda, T. (2002). A novel compound RS- 0466 reverses beta-amyloid-induced cytotoxicity through the Akt signaling pathway in vitro. Eur. J. Pharmacol. 457, 11-17. (Pubitemid 35379970)
47. Nakayashiki, T., Ebihara, K., Bannai, H. and Nakamura, Y. (2001). Yeast [PSI+] "prions" that are crosstransmissible and susceptible beyond a species barrier through a quasi-prion state. Mol. Cell 7, 1121-1130. (Pubitemid 32607347)
48. Necula, M., Breydo, L., Milton, S., Kayed, R., van der Veer, W. E., Tone, P. and Glabe, C. G. (2007a). Methylene blue inhibits amyloid Abeta oligomerization by promoting fibrillization. Biochemistry 46, 8850-8860. (Pubitemid 47208418)
49. Necula, M., Kayed, R., Milton, S. and Glabe, C. G. (2007b). Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J. Biol. Chem. 282, 10311-10324. (Pubitemid 47093410)
50. O'Hare, E., Scopes, D. I., Treherne, J. M., Norwood, K., Spanswick, D. and Kim, E. M. (2010). RS-0406 arrests amyloid-beta oligomer-induced behavioural deterioration in vivo. Behav. Brain Res. 210, 32-37.
51. Ratia, K., Pegan, S., Takayama, J., Sleeman, K., Coughlin, M., Baliji, S., Chaudhuri, R., Fu, W., Prabhakar, B. S., Johnson, M. E. et al. (2008). A noncovalent class of papain-like protease/deubiquitinase inhibitors blocks SARS virus replication. Proc. Natl. Acad. Sci. USA 105, 16119-16124.
52. Rishton, G. M. (2003). Nonleadlikeness and leadlikeness in biochemical screening. Drug Discov. Today 8, 86-96.
53. Scherzer-Attali, R., Pellarin, R., Convertino, M., Frydman-Marom, A., Egoz-Matia, N., Peled, S., Levy-Sakin, M., Shalev, D. E., Caflisch, A., Gazit, E. et al. (2010). Complete phenotypic recovery of an Alzheimer's disease model by a Quinone- Tryptophan hybrid aggregation inhibitor. Plos ONE 5, 1-15.
54. Selkoe, D. J. (1991). The molecular pathology of Alzheimer's disease. Neuron 6, 487-498.
55. 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. et al. (2008). Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842.
56. Sharma, S. C. (2006). Implications of sterol structure for membrane lipid composition, fluidity and phospholipid asymmetry in Saccharomyces cerevisiae. FEMS Yeast Res. 6, 1047-1051.
57. Sherman, F. (2002). Getting started with yeast. Methods Enzymol. 350, 3-41.
58. Soto, C., Sigurdsson, E. M., Morelli, L., Kumar, R. A., Castano, E. M. and Frangione, B. (1998). Beta-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy. Nat. Med. 4, 822-826. (Pubitemid 28331024)
59. Stine, W. B., Jr, Dahlgren, K. N., Krafft, G. A. and LaDu, M. J. (2003). In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J. Biol. Chem. 278, 11612-11622. (Pubitemid 36792723)
60. Ter-Avanesyan, M. D., Kushnirov, V. V., Dagkesamanskaya, A. R., Didichenko, S. A., Chernoff, Y. O., Inge-Vechtomov, S. G. and Smirnov, V. N. (1993). Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two nonoverlapping functional regions in the encoded protein. Mol. Microbiol. 7, 683-692. (Pubitemid 23090350)
61. Townsend, M., Cleary, J. P., Mehta, T., Hofmeister, J., Lesne, S., O'Hare, E., Walsh, D. M. and Selkoe, D. J. (2006). Orally available compound prevents deficits in memory caused by the Alzheimer amyloid-beta oligomers. Ann. Neurol. 60, 668-676. (Pubitemid 46048484)
62. Treusch, S., Cyr, D. M. and Lindquist, S. (2009). Amyloid deposits: protection against toxic protein species? Cell Cycle 8, 1668-1674.
63. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J. and Selkoe, D. J. (2002a). Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539. (Pubitemid 34288854)
64. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Rowan, M. J. and Selkoe, D. J. (2002b). Amyloid-beta oligomers: their production, toxicity and therapeutic inhibition. Biochem. Soc. Trans. 30, 552-557. (Pubitemid 35001597)
65. Walsh, D. M., Townsend, M., Podlisny, M. B., Shankar, G. M., Fadeeva, J. V., El Agnaf, O., Hartley, D. M. and Selkoe, D. J. (2005). Certain inhibitors of synthetic amyloid beta-peptide (Abeta) fibrillogenesis block oligomerization of natural Abeta and thereby rescue long-term potentiation. J. Neurosci. 25, 2455-2462. (Pubitemid 40365155)
66. Welihinda, A. A., Beavis, A. D. and Trumbly, R. J. (1994). Mutations in LIS1 (ERG6) gene confer increased sodium and lithium uptake in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1193, 107-117. (Pubitemid 24234185)
67. Williams, A. D., Portelius, E., Kheterpal, I., Guo, J. T., Cook, K. D., Xu, Y. and Wetzel, R. (2004). Mapping abeta amyloid fibril secondary structure using scanning proline mutagenesis. J. Mol. Biol. 335, 833-842. (Pubitemid 38352823)
68. Yang, F., Lim, G. P., Begum, A. N., Ubeda, O. J., Simmons, M. R., Ambegaokar, S. S., Chen, P. P., Kayed, R., Glabe, C. G., Frautschy, S. A. et al. (2005). Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 280, 5892-5901. (Pubitemid 40280072)
69. Younkin, S. G. (1995). Evidence that A beta 42 is the real culprit in Alzheimer's disease. Ann. Neurol. 37, 287-288.
70. Zhang, J. H., Chung, T. D. and Oldenburg, K. R. (1999). A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen 4, 67-73. (Pubitemid 29278954)