Influence of Hsp70s and their regulators on yeast prion propagation

Prion

Volumn 3, Issue 2, 2009, Pages 65-73

  Masison, Daniel C ^a   Kirkland, P Aaron ^a   Sharma, Deepak ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Chaperone; Hsp40; Hsp70; Prion; Yeast

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMYLOID; CHAPERONE; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; PRION PROTEIN; PROTEIN SIS1P; PROTEIN YDJ1; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CELL DIVISION; CELL GROWTH; GENETIC ANALYSIS; HYDROLYSIS; MAMMAL CELL; MUTATION; NONHUMAN; PHENOTYPE; PRION; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SACCHAROMYCES CEREVISIAE; SOLUBILIZATION; YEAST;

MAMMALIA;

EID: 67649361913     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.3.2.9134     Document Type: Review

References (102)

1. +] prion in yeast. Genetics 2003; 165:23-33.
2. Cox BS. "Y" a cytoplasmic suppressor of super-suppressor in yeast. Heredity 1965; 20:505-521
3. Aigle M, Lacroute F. Genetical aspects of [URE3], a non-mitochondrial, cytoplasmically inherited mutation in yeast. Mol Gen Genet 1975; 136:327-335
4. Wickner RB. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 1994; 264:566-569
5. +] prion in Saccharomyces cerevisiae. Genetics 1997; 147:507-519
6. Derkatch IL, Bradley ME, Hong JY, Liebman SW. Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 2001; 106:171-182 (Pubitemid 32772628)
7. Sondheimer N, Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 2000; 5:163-172 (Pubitemid 30105445)
8. King CY, Tittmann P, Gross H, Gebert R, Aebi M, Wuthrich K. Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. Proc Natl Acad Sci USA 1997; 94:6618-6622 (Pubitemid 27281913)
9. Baxa U, Speransky V, Steven AC, Wickner RB. Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc Natl Acad Sci USA 2002; 99:5253-5260
10. Bai M, Zhou JM, Perrett S. The yeast prion protein Ure2 shows glutathione peroxidase activity in both native and fibrillar forms. J Biol Chem 2004; 279:50025-50030 (Pubitemid 39577813)
11. +] and their prion-specific effects. Curr Biol 2000; 10:1443-1446
12. Osherovich LZ, Weissman JS. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 2001; 106:183-194 (Pubitemid 32772629)
13. Nemecek J, Nakayashiki T, Wickner RB. A prion of yeast metacaspase homolog (Mca1p) detected by a genetic screen. Proc Natl Acad Sci USA 2009; 106:1892-1896.
14. King CY, Diaz-Avalos R. Protein-only transmission of three yeast prion strains. Nature 2004; 428:319-323 (Pubitemid 38418802)
15. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS. Conformational variations in an infectious protein determine prion strain differences. Nature 2004; 428:323-328 (Pubitemid 38418803)
16. Brachmann A, Baxa U, Wickner RB. Prion generation in vitro: amyloid of Ure2p is infectious. EMBO J 2005; 24:3082-3092 (Pubitemid 41486344)
17. +]. J Mol Biol 2007; 365:773-782
18. Byrne LJ, Cole DJ, Cox BS, Ridout MS, Morgan BJ, Tuite MF. The number and transmission of [PSI] prion seeds (Propagons) in the yeast Saccharomyces cerevisiae. PLoS ONE 2009; 4:4670.
19. +]. Science 1995; 268:880-884
20. Hung GC, Masison DC. N-terminal domain of yeast Hsp104 chaperone is dispensable for thermotolerance and prion propagation but necessary for curing prions by Hsp104 overexpression. Genetics 2006; 173:611-620 (Pubitemid 43945883)
21. Tessarz P, Mogk A, Bukau B. Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol Microbiol 2008; 68:87-97.
22. Shorter J, Lindquist S. Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities. Mol Cell 2006; 23:425-438 (Pubitemid 44128844)
23. +] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 2003; 278:49636-49643
24. Tuite MF, Cox BS. Propagation of yeast prions. Nat Rev Mol Cell Biol 2003; 4:878-890 (Pubitemid 37411726)
25. Bailleul PA, Newnam GP, Steenbergen JN, Chernoff YO. Genetic study of interactions between the cytoskeletal assembly protein sla1 and prion-forming domain of the release factor Sup35 (eRF3) in Saccharomyces cerevisiae. Genetics 1999; 153:81-94. (Pubitemid 29434770)
26. Bailleul-Winslett PA, Newnam GP, Wegrzyn RD, Chernoff YO. An antiprion effect of the anticytoskeletal drug latrunculin A in yeast. Gene Expr 2000; 9:145-156 (Pubitemid 32180168)
27. Ganusova EE, Ozolins LN, Bhagat S, Newnam GP, Wegrzyn RD, Sherman MY, et al. Modulation of prion formation, aggregation and toxicity by the actin cytoskeleton in yeast. Mol Cell Biol 2006; 26:617-629 (Pubitemid 43089773)
28. Erjavec N, Larsson L, Grantham J, Nystrom T. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev 2007; 21:2410-2421 (Pubitemid 47529371)
29. + chaperone Hsp104 is part of a network that links the actin cytoskeleton with the inheritance of damaged proteins. Mol Cell Biol 2009.
30. Glover JR, Lindquist S. Hsp104, Hsp70 and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 1998; 94:73-82.
31. Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA 1999; 96:13732-13737
32. Doyle SM, Wickner S. Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 2009; 34:40-48
33. Nishikawa S, Brodsky JL, Nakatsukasa K. Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD). J Biochem 2005; 137:551-555 (Pubitemid 40874532)
34. Picard D. Chaperoning steroid hormone action. Trends Endocrinol Metab 2006; 17:229-235 (Pubitemid 44164280)
35. Baker MJ, Frazier AE, Gulbis JM, Ryan MT. Mitochondrial protein-import machinery: correlating structure with function. Trends Cell Biol 2007; 17:456-464 (Pubitemid 47499044)
36. Bukau B, Horwich AL. The Hsp70 and Hsp60 chaperone machines. Cell 1998; 92:351-366 (Pubitemid 28093013)
37. Young JC, Agashe VR, Siegers K, Hartl FU. Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 2004; 5:781-791 (Pubitemid 39336272)
38. Meimaridou E, Gooljar SB, Chapple JP. From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery. J Mol Endocrinol 2009; 42:1-9.
39. Werner-Washburne M, Stone DE, Craig EA. Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol Cell Biol 1987; 7:2568-2577
40. Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 1992; 71:97-105.
41. Boorstein WR, Ziegelhoffer T, Craig EA. Molecular evolution of the HSP70 multigene family. J Mol Evol 1994; 38:1-17. (Pubitemid 24018361)
42. Greene MK, Maskos K, Landry SJ. Role of the J-domain in the cooperation of Hsp40 with Hsp70. Proc Natl Acad Sci USA 1998; 95:6108-6113 (Pubitemid 28248972)
43. Wittung-Stafshede P, Guidry J, Horne BE, Landry SJ. The J-domain of Hsp40 couples ATP hydrolysis to substrate capture in Hsp70. Biochemistry 2003; 42:4937-4944 (Pubitemid 36532046)
44. Kryndushkin DS, Smirnov VN, Ter-Avanesyan MD, Kushnirov VV. Increased expression of Hsp40 chaperones, transcriptional factors and ribosomal protein Rpp0 can cure yeast prions. J Biol Chem 2002; 277:23702-23708 (Pubitemid 34952210)
45. Kabani M, Beckerich JM, Brodsky JL. Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 2002; 22:4677-4689 (Pubitemid 34620404)
46. Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J 2006; 25:2510-2518 (Pubitemid 44012233)
47. Dragovic Z, Broadley SA, Shomura Y, Bracher A, Hartl FU. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J 2006; 25:2519-2528 (Pubitemid 44012234)
48. Wegele H, Haslbeck M, Reinstein J, Buchner J. Sti1 is a novel activator of the Ssa proteins. J Biol Chem 2003; 278:25970-25976 (Pubitemid 36835362)
49. Hainzl O, Wegele H, Richter K, Buchner J. Cns1 is an activator of the Ssa1 ATPase activity. J Biol Chem 2004; 279:23267-23273 (Pubitemid 38685635)
50. +] is prion impaired by factors that regulate Hsp70 substrate binding. Mol Cell Biol 2004; 24:3928-3937
51. +] prion. EMBO J 2001; 20:2435-2442
52. +]. Genetics 2005; 169:1227-1242
53. +] aggregates with heterogeneous protein composition. Mol Biol Cell 2008; 19:2433-2443
54. Inoue Y, Taguchi H, Kishimoto A, Yoshida M. Hsp104 binds to yeast Sup35 prion fiber but needs other factor(s) to sever it. J Biol Chem 2004; 279:52319-52323 (Pubitemid 39656606)
55. Krzewska J, Melki R. Molecular chaperones and the assembly of the prion Sup35p, an in vitro study. EMBO J 2006; 25:822-833 (Pubitemid 43292443)
56. Shorter J, Lindquist S. Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J 2008; 27:2712-2724
57. Savistchenko J, Krzewska J, Fay N, Melki R. Molecular chaperones and the assembly of the prion Ure2p in vitro. J Biol Chem 2008; 283:15732-15739
58. +] as a cellular stress. Genetics 2000; 156:559-570
59. +]. Genetics 2003; 163:495-506.
60. Loovers HM, Guinan E, Jones GW. Importance of the Hsp70 ATPase domain in yeast prion propagation. Genetics 2007; 175:621-630 (Pubitemid 46798263)
61. Song Y, Wu YX, Jung G, Tutar Y, Eisenberg E, Greene LE, et al. Role for Hsp70 chaperone in Saccharomyces cerevisiae prion seed replication. Eukaryot Cell 2005; 4:289-297
62. Needham PG, Masison DC. Prion-impairing mutations in Hsp70 chaperone Ssa1: Effects on ATPase and chaperone activities. Arch Biochem Biophys 2008; 478:167-174
63. Moriyama H, Edskes HK, Wickner RB. [URE3] Prion propagation in Saccharomyces cerevisiae: requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p. Mol Cell Biol 2000; 20:8916-8922
64. Higurashi T, Hines JK, Sahi C, Aron R, Craig EA. Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc Natl Acad Sci USA 2008; 105:16596-16601
65. Sharma D, Stanley RF, Masison DC. Curing of Yeast [URE3] Prion by the Hsp40 Cochaperone Ydj1p Is Mediated by Hsp70. Genetics 2009; 181:129-137
66. Lian HY, Zhang H, Zhang ZR, Loovers HM, Jones GW, Rowling PJ, et al. Hsp40 interacts directly with the native state of the yeast prion protein Ure2 and inhibits formation of amyloid-like fibrils. J Biol Chem 2007; 282:11931-11940 (Pubitemid 47100673)
67. Kryndushkin D, Wickner RB. Nucleotide exchange factors for Hsp70s are required for [URE3] prion propagation in Saccharomyces cerevisiae. Mol Biol Cell 2007; 18:2149-2154
68. Becker J, Walter W, Yan W, Craig EA. Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol Cell Biol 1996; 16:4378-4386 (Pubitemid 26251239)
69. Hon T, Lee HC, Hach A, Johnson JL, Craig EA, Erdjument-Bromage H, et al. The Hsp70-Ydj1 molecular chaperone represses the activity of the heme activator protein Hap1 in the absence of heme. Mol Cell Biol 2001; 21:7923-7932 (Pubitemid 33051785)
70. Sahi C, Craig EA. Network of general and specialty J protein chaperones of the yeast cytosol. Proc Natl Acad Sci USA 2007; 104:7163-7168
71. Bradley ME, Edskes HK, Hong JY, Wickner RB, Liebman SW. Interactions among prions and prion "strains" in yeast. Proc Natl Acad Sci USA 2002; 99:16392-16399
72. +]. Mol Biol Cell 2003; 14:1172-1181
73. Summers DW, Douglas PM, Ren HY, Cyr DM. The type I Hsp40 Ydj1 utilizes a farnesyl moiety and zinc finger-like region to suppress prion toxicity. J Biol Chem 2009; 284:3628-3639
74. Flom GA, Lemieszek M, Fortunato EA, Johnson JL. Farnesylation of Ydj1 is required for in vivo interaction with Hsp90 client proteins. Mol Biol Cell 2008; 19:5249-5258
75. +] and [URE3] prions and curing of [URE3] by Hsp70 protein chaperone Ssa1p but not by Ssa2p. Mol Cell Biol 2002; 22:3590-3598
76. +] seeds necessary for prion propagation. EMBO J 2007; 26:3794-3803
77. Yan W, Craig EA. The glycine-phenylalanine-rich region determines the specificity of the yeast Hsp40 Sis1. Mol Cell Biol 1999; 19:7751-7758 (Pubitemid 29493439)
78. Douglas PM, Treusch S, Ren HY, Halfmann R, Duennwald ML, Lindquist S, et al. Chaperone-dependent amyloid assembly protects cells from prion toxicity. Proc Natl Acad Sci USA 2008; 105:7206-7211 (Pubitemid 351754456)
79. Tipton KA, Verges KJ, Weissman JS. In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Mol Cell 2008; 32:584-591
80. Gokhale KC, Newnam GP, Sherman MY, Chernoff YO. Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J Biol Chem 2005; 280:22809-22818 (Pubitemid 40853187)
81. Lu Z, Cyr DM. Protein folding activity of Hsp70 is modified differentially by the hsp40 co-chaperones Sis1 and Ydj1. J Biol Chem 1998; 273:27824-27830 (Pubitemid 28496069)
82. Fan CY, Lee S, Ren HY, Cyr DM. Exchangeable chaperone modules contribute to specification of type I and type II Hsp40 cellular function. Mol Biol Cell 2004; 15:761-773 (Pubitemid 38146491)
83. Roberts BT, Moriyama H, Wickner RB. [URE3] prion propagation is abolished by a mutation of the primary cytosolic Hsp70 of budding yeast. Yeast 2004; 21:107-117 (Pubitemid 38219964)
84. Sharma D, Masison DC. Functionally redundant isoforms of a yeast hsp70 chaperone subfamily have different antiprion effects. Genetics 2008; 179:1301-1311
85. Newnam GP, Wegrzyn RD, Lindquist SL, Chernoff YO. Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol Cell Biol 1999; 19:1325-1333 (Pubitemid 29046874)
86. Borchsenius AS, Wegrzyn RD, Newnam GP, Inge-Vechtomov SG, Chernoff YO. Yeast prion protein derivative defective in aggregate shearing and production of new 'seeds'. EMBO J 2001; 20:6683-6691
87. Borchsenius AS, Muller S, Newnam GP, Inge-Vechtomov SG, Chernoff YO. Prion variant maintained only at high levels of the Hsp104 disaggregase. Curr Genet 2006; 49:21-29 (Pubitemid 43118774)
88. Mathur V, Hong JY, Liebman SW. Ssa1 overexpression and [PIN(+)] variants cure [PSI(+)] by dilution of aggregates. J Mol Biol 2009.
89. Chernoff YO, Newnam GP, Kumar J, Allen K, Zink AD. Evidence for a protein mutator in yeast: role of the Hsp70-related chaperone ssb in formation, stability and toxicity of the [PSI] prion. Mol Cell Biol 1999; 19:8103-8112
90. +] prion-curing factor. Curr Genet 2001; 39:62-67
91. Tutar Y, Song Y, Masison DC. Primate chaperones Hsc70 (constitutive) and Hsp70 (induced) differ functionally in supporting growth and prion propagation in Saccharomyces cerevisiae. Genetics 2006; 172:851-861 (Pubitemid 43345423)
92. Hall D, Edskes H. Silent prions lying in wait: a two-hit model of prion/amyloid formation and infection. J Mol Biol 2004; 336:775-786 (Pubitemid 38183028)
93. Tanaka M, Collins SR, Toyama BH, Weissman JS. The physical basis of how prion conformations determine strain phenotypes. Nature 2006; 442:585-589 (Pubitemid 44167919)
94. +] prion. Genetics 2007; 177:1583-1593
95. Shewmaker F, Wickner RB, Tycko R. Amyloid of the prion domain of Sup35p has an in-register parallel beta-sheet structure. Proc Natl Acad Sci USA 2006; 103:19754-19759 (Pubitemid 46037503)
96. Baxa U, Wickner RB, Steven AC, Anderson DE, Marekov LN, Yau WM, et al. Characterization of beta-sheet structure in Ure2p1-89 yeast prion fibrils by solid-state nuclear magnetic resonance. Biochemistry 2007; 46:13149-13162 (Pubitemid 350086233)
97. Shewmaker F, Ross ED, Tycko R, Wickner RB. Amyloids of shuffled prion domains that form prions have a parallel in-register beta-sheet structure. Biochemistry 2008; 47:4000-4007
98. +] prion, has a parallel in-register beta-sheet structure. Proc Natl Acad Sci USA 2008; 105:2403-2408
99. Wickner RB, Shewmaker F, Kryndushkin D, Edskes HK. Protein inheritance (prions) based on parallel in-register beta-sheet amyloid structures. Bioessays 2008; 30:955-964
100. Ness F, Ferreira P, Cox BS, Tuite MF. Guanidine hydrochloride inhibits the generation of prion "seeds" but not prion protein aggregation in yeast. Mol Cell Biol 2002; 22:5593-5605
101. Du Z, Park KW, Yu H, Fan Q, Li L. Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat Genet 2008; 40:460-465
102. Patel BK, Gavin-Smyth J, Liebman SW. The yeast global transcriptional co repressor protein Cyc8 can propagate as a prion. Nat Cell Biol 2009; 11:344-349