Chaperone proteins select and maintain [PIN+] prion conformations in Saccharomyces cerevisiae

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 1266-1276

  Lancaster, David L ^a   Dobson, C Melissa ^a   Rachubinski, Richard A ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATE MORPHOLOGY; PHENOTYPIC CHANGES;

GENES; YEAST;

PROTEINS;

CHAPERONE; PRION PROTEIN; PROTEIN VARIANT; RNQ1P PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE DELETION; GENETIC VARIABILITY; INHERITANCE; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN INDUCTION; SACCHAROMYCES CEREVISIAE;

CHAPERONINS; GENE DELETION; MODELS, BIOLOGICAL; PLASMIDS; PRIONS; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 84872337201     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.377564     Document Type: Article

References (60)

1. Prusiner, S. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144
2. Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., and Cohen, F. E. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966
3. Colby, D. W., and Prusiner, S. B. (2011) Prions. Cold Spring Harb. Perspect. Biol. 3, a006833
4. Brown, K., and Mastrianni, J. A. (2010) The prion diseases. J. Geriatr. Psychiatry Neurol. 23, 277-298
5. Ohhashi, Y., Ito, K., Toyama, B. H., Weissman, J. S., and Tanaka, M. (2010) Differences in prion strain conformations result from non-native interactions in a nucleus. Nat. Chem. Biol. 6, 225-230
6. Fraser, H., and Dickinson, A. G. (1968) The sequential development of the brain lesion of scrapie in three strains of mice. J. Comp. Pathol. 78, 301-311
7. Bruce, M. E. (1993) Scrapie strain variation and mutation. Br. Med. Bull. 49, 822-838
8. Bessen, R. A., and Marsh, R. F. (1994) Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J. Virol. 68, 7859-7868 (Pubitemid 24362673)
9. Wickner, R. B. (1994) [URE3] as an altered URE2 protein. Evidence for a prion analog in Saccharomyces cerevisiae. Science 264, 566-569
10. +] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 15, 3127-3134
11. Sondheimer, N., and Lindquist, S. (2000) Rnq1. An epigenetic modifier of protein function in yeast. Mol. Cell 5, 163-172 (Pubitemid 30105445)
12. Alberti, S., Halfmann, R., King, O., Kapila, A., and Lindquist, S. (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137, 146-158
13. Halfmann, R., Jarosz, D. F., Jones, S. K., Chang, A., Lancaster, A. K., and Lindquist, S. (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482, 363-368
14. 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)
15. Schlumpberger, M., Prusiner, S. B., and Herskowitz, I. (2001) Induction of distinct [URE3] yeast prion strains. Mol. Cell. Biol. 21, 7035-7046 (Pubitemid 32911263)
16. Bradley, M. E., Edskes, H. K., Hong, J. Y., Wickner, R. B., and Liebman, S. W. (2002) Interactions among prions and prion "strains" in yeast. Proc. Natl. Acad. Sci. U.S.A. 99, 16392-16399 (Pubitemid 35470984)
17. Tanaka, M., Chien, P., Naber, N., Cooke, R., and Weissman, J. S. (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428, 323-328 (Pubitemid 38418803)
18. Tanaka, M., Collins, S. R., Toyama, B. H., and Weissman, J. S. (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442, 585-589 (Pubitemid 44167919)
19. Toyama, B. H., Kelly, M. J., Gross, J. D., and Weissman, J. S. (2007) The structural basis of yeast prion strain variants. Nature 449, 233-237 (Pubitemid 47402368)
20. +] prion in Saccharomyces cerevisiae. Genetics 147, 507-519
21. Derkatch, I. L., Bradley, M. E., Hong, J. Y., and Liebman, S. W. (2001) Prions affect the appearance of other prions. The story of [PIN+]. Cell 106, 171-182 (Pubitemid 32772628)
22. +] yeast prion variants. Genetics 165, 1675-1685
23. +] form separate structures in yeast. J. Biol. Chem. 279, 51042-51048
24. Liebman, S. W., Bagriantsev, S. N., and Derkatch, I. L. (2006) Biochemical and genetic methods for characterization of [PIN+] prions in yeast. Methods 39, 23-34 (Pubitemid 43994492)
25. Chien, P., and Weissman, J. S. (2001) Conformational diversity in a yeast prion dictates its seeding specificity. Nature 410, 223-227 (Pubitemid 32216596)
26. +] and their prion-specific effects. Curr. Biol. 10, 1443-1446
27. +] prion. EMBO J. 20, 2435-2442
28. Morano, K. A., Grant, C. M., and Moye-Rowley, W. S. (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190, 1157-1195
29. Masison, D. C., Kirkland, P. A., and Sharma, D. (2009) Influence of Hsp70s and their regulators on yeast prion propagation. Prion 3, 65-73
30. Romanova, N. V., and Chernoff, Y. O. (2009) Hsp104 and prion propagation. Protein Pept. Lett. 16, 598-605
31. Summers, D. W., Douglas, P. M., and Cyr, D. M. (2009) Prion propagation by Hsp40 molecular chaperones. Prion 3, 59-64
32. +] are regulated by the heat-shock transcription factor. Genetics 173, 35-47
33. Fan, Q., Park, K.-W., Du, Z., Morano, K. A., and Li, L. (2007) The role of Sse1 in the de novo formation and variant determination of the [PSI+] prion. Genetics 177, 1583-1593 (Pubitemid 350277054)
34. Gietz, R. D., and Woods, R. A. (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96 (Pubitemid 34619485)
35. Herskowitz, I., and Jensen, R. E. (1991) Putting the HO gene to work. Practical uses for mating-type switching. Methods Enzymol. 194, 132-146
36. Rose, M. D., Winston, F. M., and Heiter, P. (1990) Methods in Yeast Genetics: A Laboratory Course Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
37. Scholz, O., Thiel, A., Hillen, W., and Niederweis, M. (2000) Quantitative analysis of gene expression with an improved green fluorescent protein. Eur. J. Biochem. 267, 1565-1570 (Pubitemid 30165507)
38. Jansen, G., Wu, C., Schade, B., Thomas, D. Y., and Whiteway, M. (2005) Drag&Drop cloning in yeast. Gene 344, 43-51 (Pubitemid 40126791)
39. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580
40. +] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J. Biol. Chem. 278, 49636-49643
41. Feilotter, H. E., Hannon, G. J., Ruddell, C. J., and Beach, D. (1994) Construction of an improved host strain for two hybrid screening. Nucleic Acids Res. 22, 1502-1503 (Pubitemid 24166855)
42. +]. Science 268, 880-884
43. Yu, H., Braun, P., Yildirim, M. A., Lemmens, I., Venkatesan, K., Sahalie, J., Hirozane-Kishikawa, T., Gebreab, F., Li, N., Simonis, N., Hao, T., Rual, J.-F., Dricot, A., Vazquez, A., Murray, R. R., Simon, C., Tardivo, L., Tam, S., Svrzikapa, N., Fan, C., de Smet, A.-S., Motyl, A., Hudson, M. E., Park, J., Xin, X., Cusick, M. E., Moore, T., Boone, C., Snyder, M., Roth, F. P., Barabási, A.-L., Tavernier, J., Hill, D. E., and Vidal, M. (2008) High-quality binary protein interaction map of the yeast interactome network. Science 322, 104-110
44. Sindi, S. S., and Serio, T. R. (2009) Prion dynamics and the quest for the genetic determinant in protein-only inheritance. Curr. Opin. Microbiol. 12, 623-630
45. Derdowski, A., Sindi, S. S., Klaips, C. L., DiSalvo, S., and Serio, T. R. (2010) A size threshold limits prion transmission and establishes phenotypic diversity. Science 330, 680-683
46. Borchsenius, A. S., Müller, S., Newnam, G. P., Inge-Vechtomov, S. G., and Chernoff, Y. O. (2006) Prion variant maintained only at high levels of the Hsp104 disaggregase. Curr. Genet. 49, 21-29 (Pubitemid 43118774)
47. Taipale, M., Jarosz, D. F., and Lindquist, S. (2010) HSP90 at the hub of protein homeostasis. Emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 11, 515-528
48. Borkovich, K. A., Farrelly, F. W., Finkelstein, D. B., Taulien, J., and Lindquist, S. (1989) hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 9, 3919-3930 (Pubitemid 19216285)
49. Prodromou, C., Siligardi, G., O'Brien, R., Woolfson, D. N., Regan, L., Panaretou, B., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1999) Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain cochaperones. EMBO J. 18, 754-762 (Pubitemid 29057260)
50. Panaretou, B., Siligardi, G., Meyer, P., Maloney, A., Sullivan, J. K., Singh, S., Millson, S. H., Clarke, P. A., Naaby-Hansen, S., Stein, R., Cramer, R., Mollapour, M., Workman, P., Piper, P. W., Pearl, L. H., and Prodromou, C. (2002) Activation of the ATPase activity of Hsp90 by the stress-regulated cochaperone Aha1. Mol. Cell 10, 1307-1318 (Pubitemid 36050873)
51. McLaughlin, S. H., Sobott, F., Yao, Z.-P., Zhang, W., Nielsen, P. R., Grossmann, J. G., Laue, E. D., Robinson, C. V., and Jackson, S. E. (2006) The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J. Mol. Biol. 356, 746-758 (Pubitemid 43139334)
52. Duina, A. A., Chang, H. C., Marsh, J. A., Lindquist, S., and Gaber, R. F. (1996) A cyclophilin function in Hsp90-dependent signal transduction. Science 274, 1713-1715 (Pubitemid 26414903)
53. Mayr, C., Richter, K., Lilie, H., and Buchner, J. (2000) Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J. Biol. Chem. 275, 34140-34146
54. Kurahashi, H., Ishiwata, M., Shibata, S., and Nakamura, Y. (2008) A regulatory role of the Rnq1 nonprion domain for prion propagation and polyglutamine aggregates. Mol. Cell. Biol. 28, 3313-3323 (Pubitemid 351657095)
55. +] prion, has a parallel in-register β-sheet structure. Proc. Natl. Acad. Sci. U.S.A. 105, 2403-2408
56. Abbas-Terki, T., Donzé, O., Briand, P. A., and Picard, D. (2001) Hsp104 interacts with Hsp90 cochaperones in respiring yeast. Mol. Cell. Biol. 21, 7569-7575 (Pubitemid 32988768)
57. Mackay, R. G., Helsen, C. W., Tkach, J. M., and Glover, J. R. (2008) The C-terminal extension of Saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly. Biochemistry 47, 1918-1927 (Pubitemid 351287117)
58. +] prions by Hsp104. Mol. Cell. Biol. 30, 3542-3552
59. Shaner, L., Sousa, R., and Morano, K. A. (2006) Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. Biochemistry 45, 15075-15084 (Pubitemid 44937020)
60. +] prion variant establishment in yeast. Mol. Microbiol. 4, 866-881