Functional Diversification of Hsp40: Distinct J-Protein Functional Requirements for Two Prions Allow for Chaperone-Dependent Prion Selection

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  Harris, Julia M ^a   Nguyen, Phil P ^a   Patel, Milan J ^a   Sporn, Zachary A ^a   Hines, Justin K ^a  

^a LAFAYETTE COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLYCINE; HEAT SHOCK PROTEIN 40; PHENYLALANINE; PRION PROTEIN; PROTEIN SIS1; UNCLASSIFIED DRUG; AMYLOID; DNAJB1 PROTEIN, HUMAN; PRION; SACCHAROMYCES CEREVISIAE PROTEIN; SIS1 PROTEIN, S CEREVISIAE;

ARTICLE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; FUNGAL STRAIN; GENETIC ANALYSIS; IMMUNOBLOTTING; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PRION; PROTEIN TERTIARY STRUCTURE;

AMYLOID; CELL SURVIVAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; PRIONS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84905483291     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004510     Document Type: Article

References (68)

1. Wickner RB, (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569.
2. Wickner RB, Masison DC, Edskes HK, (1995) [PSI] and [URE3] as yeast prions. Yeast 11: 1671-1685.
3. Derkatch IL, Bradley ME, Hong JY, Liebman SW, (2001) Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106: 171-182.
4. Halfmann R, Lindquist S, (2010) Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330: 629-632.
5. 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.
6. Serio TR, Cashikar AG, Moslehi JJ, Kowal AS, Lindquist SL, (1999) Yeast prion [psi +] and its determinant, Sup35p. Methods Enzymol 309: 649-673.
7. Glover JR, Kowal AS, Schirmer EC, Patino MM, Liu JJ, et al. (1997) Self-seeded fibers formed by Sup35, the protein determinant of [PSI+], a heritable prion-like factor of S. cerevisiae. Cell 89: 811-819.
8. Serio TR, Lindquist SL, (1999) [PSI+]: an epigenetic modulator of translation termination efficiency. Annu Rev Cell Dev Biol 15: 661-703.
9. Stansfield I, Jones KM, Kushnirov VV, Dagkesamanskaya AR, Poznyakovski AI, et al. (1995) The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. Embo J 14: 4365-4373.
10. Zhou P, Derkatch IL, Uptain SM, Patino MM, Lindquist S, et al. (1999) The yeast non-Mendelian factor [ETA+] is a variant of [PSI+], a prion-like form of release factor eRF3. Embo J 18: 1182-1191.
11. 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.
12. Sondheimer N, Lindquist S, (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5: 163-172.
13. Osherovich LZ, Weissman JS, (2001) Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 106: 183-194.
14. 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.
15. Serio TR, Cashikar AG, Kowal AS, Sawicki GJ, Moslehi JJ, et al. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289: 1317-1321.
16. Ness F, Ferreira P, Cox BS, Tuite MF, (2002) Guanidine hydrochloride inhibits the generation of prion "seeds" but not prion protein aggregation in yeast. Mol Cell Biol 22: 5593-5605.
17. 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.
18. Sondheimer N, Lopez N, Craig EA, Lindquist S, (2001) The role of Sis1 in the maintenance of the [RNQ+] prion. Embo J 20: 2435-2442.
19. Satpute-Krishnan P, Langseth SX, Serio TR, (2007) Hsp104-dependent remodeling of prion complexes mediates protein-only inheritance. PLoS Biol 5: e24.
20. Song Y, Wu YX, Jung G, Tutar Y, Eisenberg E, et al. (2005) Role for Hsp70 chaperone in Saccharomyces cerevisiae prion seed replication. Eukaryot Cell 4: 289-297.
21. 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.
22. Aron R, Lopez N, Walter W, Craig EA, Johnson J, (2005) In vivo bipartite interaction between the Hsp40 Sis1 and Hsp70 in Saccharomyces cerevisiae. Genetics 169: 1873-1882.
23. Aron R, Higurashi T, Sahi C, Craig EA, (2007) J-protein co-chaperone Sis1 required for generation of [RNQ+] seeds necessary for prion propagation. Embo J 26: 3794-3803.
24. Higurashi T, Hines JK, Sahi C, Aron R, Craig EA, (2008) Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc Natl Acad Sci U S A 105: 16596-16601.
25. Hines JK, Li X, Du Z, Higurashi T, Li L, et al. (2011) [SWI], the prion formed by the chromatin remodeling factor Swi1, is highly sensitive to alterations in Hsp70 chaperone system activity. PLoS Genet 7: e1001309.
26. Kampinga HH, Craig EA, (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11: 579-592.
27. Mayer MP, Schroder H, Rudiger S, Paal K, Laufen T, et al. (2000) Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat Struct Biol 7: 586-593.
28. Fan CY, Lee S, Cyr DM, (2003) Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 8: 309-316.
29. Misselwitz B, Staeck O, Rapoport TA, (1998) J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences. Mol Cell 2: 593-603.
30. Glover JR, Lindquist S, (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82.
31. Bosl B, Grimminger V, Walter S, (2006) The molecular chaperone Hsp104-a molecular machine for protein disaggregation. J Struct Biol 156: 139-148.
32. Tuite MF, Serio TR, (2010) The prion hypothesis: from biological anomaly to basic regulatory mechanism. Nat Rev Mol Cell Biol 11: 823-833.
33. Winkler J, Tyedmers J, Bukau B, Mogk A, (2012) Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J Cell Biol 198: 387-404.
34. Cheetham ME, Caplan AJ, (1998) Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3: 28-36.
35. Luke MM, Sutton A, Arndt KT, (1991) Characterization of SIS1, a Saccharomyces cerevisiae homologue of bacterial dnaJ proteins. J Cell Biol 114: 623-638.
36. Park SH, Kukushkin Y, Gupta R, Chen T, Konagai A, et al. (2013) PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell 154: 134-145.
37. Malinovska L, Kroschwald S, Munder MC, Richter D, Alberti S, (2012) Molecular chaperones and stress-inducible protein-sorting factors coordinate the spatiotemporal distribution of protein aggregates. Mol Biol Cell 23: 3041-3056.
38. Summers DW, Wolfe KJ, Ren HY, Cyr DM, (2013) The Type II Hsp40 Sis1 cooperates with Hsp70 and the E3 ligase Ubr1 to promote degradation of terminally misfolded cytosolic protein. PLoS One 8: e52099.
39. Shiber A, Breuer W, Brandeis M, Ravid T, (2013) Ubiquitin conjugation triggers misfolded protein sequestration into quality control foci when Hsp70 chaperone levels are limiting. Mol Biol Cell 24: 2076-2087.
40. Yan W, Craig EA, (1999) The glycine-phenylalanine-rich region determines the specificity of the yeast Hsp40 Sis1. Mol Cell Biol 19: 7751-7758.
41. Lopez N, Aron R, Craig EA, (2003) Specificity of class II Hsp40 Sis1 in maintenance of yeast prion [RNQ+]. Mol Biol Cell 14: 1172-1181.
42. Hines JK, Higurashi T, Srinivasan M, Craig EA, (2011) Influence of prion variant and yeast strain variation on prion-molecular chaperone requirements. Prion 5: 238-244.
43. Kirkland PA, Reidy M, Masison DC, (2011) Functions of yeast Hsp40 chaperone Sis1p dispensable for prion propagation but important for prion curing and protection from prion toxicity. Genetics 188: 565-577.
44. Hines JK, Craig EA, (2011) The sensitive [SWI (+)] prion: new perspectives on yeast prion diversity. Prion 5: 164-168.
45. King CY, (2001) Supporting the structural basis of prion strains: induction and identification of [PSI] variants. J Mol Biol 307: 1247-1260.
46. Tanaka M, Collins SR, Toyama BH, Weissman JS, (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442: 585-589.
47. 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.
48. Frederick KK, Debelouchina GT, Kayatekin C, Dorminy T, Jacavone AC, et al. (2014) Distinct prion strains are defined by amyloid core structure and chaperone binding site dynamics. Chem Biol 21: 295-305.
49. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS, (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428: 323-328.
50. Fan Q, Park KW, Du Z, Morano KA, Li L, (2007) The role of Sse1 in the de novo formation and variant determination of the [PSI+] prion. Genetics 177: 1583-1593.
51. Zhong T, Luke MM, Arndt KT, (1996) Transcriptional regulation of the yeast DnaJ homologue SIS1. J Biol Chem 271: 1349-1356.
52. 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.
53. 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.
54. Byrne LJ, Cole DJ, Cox BS, Ridout MS, Morgan BJ, et al. (2009) The number and transmission of [PSI] prion seeds (Propagons) in the yeast Saccharomyces cerevisiae. PLoS One 4: e4670.
55. Ohtsuka K, (1993) Cloning of a cDNA for heat-shock protein hsp40, a human homologue of bacterial DnaJ. Biochem Biophys Res Commun 197: 235-240.
56. Sahi C, Craig EA, (2007) Network of general and specialty J protein chaperones of the yeast cytosol. Proc Natl Acad Sci U S A 104: 7163-7168.
57. Toyama BH, Kelly MJ, Gross JD, Weissman JS, (2007) The structural basis of yeast prion strain variants. Nature 449: 233-237.
58. Verges KJ, Smith MH, Toyama BH, Weissman JS, (2011) Strain conformation, primary structure and the propagation of the yeast prion [PSI+]. Nat Struct Mol Biol 18: 493-499.
59. Stein KC, True HL, (2014) Extensive diversity of prion strains is defined by differential chaperone interactions and distinct amyloidogenic regions. PLoS Genet 10: e1004337.
60. Bagriantsev SN, Gracheva EO, Richmond JE, Liebman SW, (2008) Variant-specific [PSI+] Infection Is Transmitted by Sup35 Polymers within [PSI+] Aggregates with Heterogeneous Protein Composition. Mol Biol Cell 19: 2433-2443.
61. Yang Z, Hong JY, Derkatch IL, Liebman SW, (2013) Heterologous gln/asn-rich proteins impede the propagation of yeast prions by altering chaperone availability. PLoS Genet 9: e1003236.
62. Reidy M, Miot M, Masison DC, (2012) Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions. Genetics 192: 185-193.
63. Mumberg D, Muller R, Funk M, (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119-122.
64. Eaglestone SS, Ruddock LW, Cox BS, Tuite MF, (2000) Guanidine hydrochloride blocks a critical step in the propagation of the prion-like determinant [PSI(+)] of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97: 240-244.
65. Inge-Vechtomov SG, Tikhodeev ON, Karpova TS, (1988) [Selective systems for obtaining recessive ribosomal suppressors in saccharomycete yeasts]. Genetika 24: 1159-1165.
66. Cox BS, (1965) [PSI], a cytoplasmic suppressor of super-suppression in yeast. Heredity 20: 505-521.
67. Bousset L, Savistchenko J, Melki R, (2008) Assembly of the asparagine- and glutamine-rich yeast prions into protein fibrils. Curr Alzheimer Res 5: 251-259.
68. Bagriantsev SN, Kushnirov VV, Liebman SW, (2006) Analysis of amyloid aggregates using agarose gel electrophoresis. Methods Enzymol 412: 33-48.