Regulation of the Hsp104 middle domain activity is critical for yeast prion propagation

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Dulle, Jennifer E ^a,b   Stein, Kevin C ^a   True, Heather L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 104;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; HEAT TOLERANCE; PRION; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; SACCHAROMYCES CEREVISIAE; TEMPERATURE DEPENDENCE;

ELECTROPHORESIS, AGAR GEL; HEAT-SHOCK PROTEINS; LUCIFERASES; MICROSCOPY, FLUORESCENCE; MOLECULAR CHAPERONES; MUTAGENESIS; OLIGONUCLEOTIDES; PRIONS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84899885443     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087521     Document Type: Article

References (75)

1. Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82. (Pubitemid 28347471)
2. Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 96: 13732-13737.
3. Parsell DA, Kowal AS, Lindquist S (1994) Saccharomyces cerevisiae Hsp104 protein. Purification and characterization of ATP-induced structural changes. J Biol Chem 269: 4480-4487.
4. Parsell DA, Kowal AS, Singer MA, Lindquist S (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475-478.
5. Tessarz P, Mogk A, Bukau B (2008) Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol Microbiol 68: 87-97. (Pubitemid 351372041)
6. Weibezahn J, Tessarz P, Schlieker C, Zahn R, Maglica Z, et al. (2004) Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119: 653-665. (Pubitemid 39535753)
7. Sanchez Y, Lindquist SL (1990) HSP104 required for induced thermotolerance. Science 248: 1112-1115. (Pubitemid 120031537)
8. Chernoff YO, Lindquist SL, Ono B, Inge-Vechtomov SG, Liebman SW (1995) Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi +]. Science 268: 880-884.
9. True HL (2006) The battle of the fold: chaperones take on prions. Trends Genet 22: 110-117.
10. Cox B, Ness F, Tuite M (2003) Analysis of the generation and segregation of propagons: entities that propagate the [PSI+] prion in yeast. Genetics 165: 23-33. (Pubitemid 37204053)
11. True HL, Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477-483.
12. Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK, et al. (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482: 363-368.
13. Du Z, Park KW, Yu H, Fan Q, Li L (2008) Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat Genet 40: 460-465. (Pubitemid 351450881)
14. Li L, Lindquist S (2000) Creating a protein-based element of inheritance. Science 287: 661-664. (Pubitemid 30070915)
15. Harris DA, True HL (2006) New insights into prion structure and toxicity. Neuron 50: 353-357.
16. Satpute-Krishnan P, Langseth SX, Serio TR (2007) Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol 5: e24.
17. Satpute-Krishnan P, Serio TR (2005) Prion protein remodelling confers an immediate phenotypic switch. Nature 437: 262-265. (Pubitemid 41294489)
18. Shorter J, Lindquist S (2004) Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304: 1793-1797. (Pubitemid 38787894)
19. Kryndushkin DS, Alexandrov IM, Ter-Avanesyan MD, Kushnirov VV (2003) Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 278: 49636-49643.
20. DeSantis ME, Shorter J (2012) Hsp104 drives "protein-only" positive selection of Sup35 prion strains encoding strong [PSI(+)]. Chem Biol 19: 1400-1410.
21. DeSantis ME, Leung EH, Sweeny EA, Jackrel ME, Cushman-Nick M, et al. (2012) Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151: 778-793.
22. Dulle J, True HL (2013) Low activity of select Hsp104 mutants is sufficient to propagate unstable prion variants. Prion 7.
23. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD (1996) Propagation of the yeast prion-like [psi +] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J 15: 3127-3134. (Pubitemid 26187760)
24. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD (1997) In vitro propagation of the prion-like state of yeast Sup35 protein. Science 277: 381-383. (Pubitemid 27450712)
25. Ter-Avanesyan MD, Dagkesamanskaya AR, Kushnirov VV, Smirnov VN (1994) The SUP35 omnipotent suppressor gene is involved in the maintenance of the non-Mendelian determinant [psi+] in the yeast Saccharomyces cerevisiae. Genetics 137: 671-676. (Pubitemid 24196460)
26. True HL, Berlin I, Lindquist SL (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431: 184-187. (Pubitemid 39243470)
27. Derkatch IL, Bradley ME, Hong JY, Liebman SW (2001) Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106: 171-182. (Pubitemid 32772628)
28. Derkatch IL, Bradley ME, Masse SV, Zadorsky SP, Polozkov GV, et al. (2000) Dependence and independence of [PSI(+)] and [PIN(+)]: a two-prion system in yeast? Embo J 19: 1942-1952. (Pubitemid 30237570)
29. Derkatch IL, Bradley ME, Zhou P, Chernoff YO, Liebman SW (1997) Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 147: 507-519. (Pubitemid 27418562)
30. Sondheimer N, Lindquist S (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5: 163-172. (Pubitemid 30105445)
31. Osherovich LZ, Weissman JS (2001) Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 106: 183-194. (Pubitemid 32772629)
32. Tyedmers J, Madariaga ML, Lindquist S (2008) Prion switching in response to environmental stress. PLoS Biol 6: e294.
33. Vishveshwara N, Bradley ME, Liebman SW (2009) Sequestration of essential proteins causes prion associated toxicity in yeast. Mol Microbiol 73: 1101-1114.
34. Eaglestone SS, Cox BS, Tuite MF (1999) Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism. EMBO J 18: 1974-1981. (Pubitemid 29158540)
35. McGlinchey RP, Kryndushkin D, Wickner RB (2011) Suicidal [PSI+] is a lethal yeast prion. Proc Natl Acad Sci U S A 108: 5337-5341.
36. Tipton KA, Verges KJ, Weissman JS (2008) In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Mol Cell 32: 584-591.
37. Hung GC, Masison DC (2006) N-terminal domain of yeast Hsp104 chaperone is dispensable for thermotolerance and prion propagation but necessary for curing prions by Hsp104 overexpression. Genetics 173: 611-620.
38. Schirmer EC, Queitsch C, Kowal AS, Parsell DA, Lindquist S (1998) The ATPase activity of Hsp104, effects of environmental conditions and mutations. J Biol Chem 273: 15546-15552. (Pubitemid 28298166)
39. Grimminger-Marquardt V, Lashuel HA (2010) Structure and function of the molecular chaperone Hsp104 from yeast. Biopolymers 93: 252-276.
40. Tkach JM, Glover JR (2004) Amino acid substitutions in the C-terminal AAA+ module of Hsp104 prevent substrate recognition by disrupting oligomerization and cause high temperature inactivation. J Biol Chem 279: 35692-35701. (Pubitemid 39100573)
41. Dulle JE, Bouttenot RE, Underwood LA, True HL (2013) Soluble oligomers are sufficient for transmission of a yeast prion but do not confer phenotype. J Cell Biol 203: 197-204.
42. Schirmer EC, Homann OR, Kowal AS, Lindquist S (2004) Dominant gain-offunction mutations in Hsp104p reveal crucial roles for the middle region. Mol Biol Cell 15: 2061-2072. (Pubitemid 38580628)
43. Lipinska N, Zietkiewicz S, Sobczak A, Jurczyk A, Potocki W, et al. (2013) Disruption of ionic interactions between the nucleotide binding domain 1 (NBD1) and middle (M) domain in Hsp100 disaggregase unleashes toxic hyperactivity and partial independence from Hsp70. J Biol Chem 288: 2857-2869.
44. Zolkiewski M (2006) A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61: 1094-1100.
45. Desantis ME, Shorter J (2012) The elusive middle domain of Hsp104 and ClpB: location and function. Biochim Biophys Acta 1823: 29-39.
46. Biter AB, Lee J, Sung N, Tsai FT, Lee S (2012) Functional analysis of conserved cis- and trans-elements in the Hsp104 protein disaggregating machine. J Struct Biol 179: 172-180.
47. Haslberger T, Weibezahn J, Zahn R, Lee S, Tsai FT, et al. (2007) M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol Cell 25: 247-260. (Pubitemid 46109605)
48. Oguchi Y, Kummer E, Seyffer F, Berynskyy M, Anstett B, et al. (2012) A tightly regulated molecular toggle controls AAA+ disaggregase. Nat Struct Mol Biol 19: 1338-1346.
49. Sielaff B, Tsai FT (2010) The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner. J Mol Biol 402: 30-37.
50. Mogk A, Schlieker C, Strub C, Rist W, Weibezahn J, et al. (2003) Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J Biol Chem 278: 17615-17624. (Pubitemid 36799363)
51. Kedzierska S, Akoev V, Barnett ME, Zolkiewski M (2003) Structure and function of the middle domain of ClpB from Escherichia coli. Biochemistry 42: 14242-14248. (Pubitemid 37499421)
52. Lee J, Kim JH, Biter AB, Sielaff B, Lee S, et al. (2013) Heat shock protein (Hsp) 70 is an activator of the Hsp104 motor. Proc Natl Acad Sci U S A 110: 8513-8518.
53. Miot M, Reidy M, Doyle SM, Hoskins JR, Johnston DM, et al. (2011) Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc Natl Acad Sci U S A 108: 6915-6920.
54. Seyffer F, Kummer E, Oguchi Y, Winkler J, Kumar M, et al. (2012) Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces. Nat Struct Mol Biol 19: 1347-1355.
55. Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, et al. (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115: 229-240. (Pubitemid 37329586)
56. Lee S, Sielaff B, Lee J, Tsai FT (2010) CryoEM structure of Hsp104 and its mechanistic implication for protein disaggregation. Proc Natl Acad Sci U S A 107: 8135-8140.
57. Derkatch IL, Chernoff YO, Kushnirov VV, Inge-Vechtomov SG, Liebman SW (1996) Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144: 1375-1386. (Pubitemid 26427888)
58. Bradley ME, Edskes HK, Hong JY, Wickner RB, Liebman SW (2002) Interactions among prions and prion "strains" in yeast. Proc Natl Acad Sci U S A 99 Suppl 4: 16392-16399. (Pubitemid 35470984)
59. Bardill JP, Dulle JE, Fisher JR, True HL (2009) Requirements of Hsp104p activity and Sis1p binding for propagation of the [RNQ (+)] prion. Prion 3: 151-160.
60. Derkatch IL, Bradley ME, Zhou P, Liebman SW (1999) The PNM2 mutation in the prion protein domain of SUP35 has distinct effects on different variants of the [PSI+] prion in yeast. Curr Genet 35: 59-67. (Pubitemid 29141247)
61. Lum R, Tkach JM, Vierling E, Glover JR (2004) Evidence for an unfolding/ threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J Biol Chem 279: 29139-29146. (Pubitemid 38915786)
62. Cashikar AG, Schirmer EC, Hattendorf DA, Glover JR, Ramakrishnan MS, et al. (2002) Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein. Mol Cell 9: 751-760. (Pubitemid 34454887)
63. Reidy M, Miot M, Masison DC (2012) Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions. Genetics 192: 185-193.
64. Gokhale KC, Newnam GP, Sherman MY, Chernoff YO (2005) Modulation of prion-dependent polyglutamine aggregation and toxicity by chaperone proteins in the yeast model. J Biol Chem 280: 22809-22818. (Pubitemid 40853187)
65. Kurahashi H, Nakamura Y (2007) Channel mutations in Hsp104 hexamer distinctively affect thermotolerance and prion-specific propagation. Mol Microbiol 63: 1669-1683. (Pubitemid 46426708)
66. Bradley ME, Liebman SW (2003) Destabilizing interactions among [PSI(+)] and [PIN (+)] yeast prion variants. Genetics 165: 1675-1685. (Pubitemid 38040262)
67. Huang VJ, Stein KC, True HL (2013) Spontaneous Variants of the [RNQ+] Prion in Yeast Demonstrate the Extensive Conformational Diversity Possible with Prion Proteins. PLoS One 8: e79582.
68. Watanabe YH, Nakazaki Y, Suno R, Yoshida M (2009) Stability of the two wings of the coiled-coil domain of ClpB chaperone is critical for its disaggregation activity. Biochem J 421: 71-77.
69. Kummer E, Oguchi Y, Seyffer F, Bukau B, Mogk A (2013) Mechanism of Hsp104/ClpB inhibition by prion curing Guanidinium hydrochloride. FEBS Lett 587: 810-817.
70. Mathur V, Hong JY, Liebman SW (2009) Ssa1 overexpression and [PIN(+)] variants cure [PSI(+)] by dilution of aggregates. J Mol Biol 390: 155-167.
71. Kryndushkin DS, Smirnov VN, Ter-Avanesyan MD, Kushnirov VV (2002) Increased expression of Hsp40 chaperones, transcriptional factors, and ribosomal protein Rpp0 can cure yeast prions. J Biol Chem 277: 23702-23708. (Pubitemid 34952210)
72. Sweeny EA, Shorter J (2008) Prion proteostasis: Hsp104 meets its supporting cast. Prion 2: 135-140.
73. Newnam GP, Birchmore JL, Chernoff YO (2011) Destabilization and recovery of a yeast prion after mild heat shock. J Mol Biol 408: 432-448.
74. Bagriantsev S, Liebman SW (2004) Specificity of prion assembly in vivo. [PSI+] and [PIN +] form separate structures in yeast. J Biol Chem 279: 51042-51048. (Pubitemid 40017845)
75. Wendler P, Shorter J, Plisson C, Cashikar AG, Lindquist S, et al. (2007) Atypical AAA+ subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104. Cell 131: 1366-1377.