Dual role of ribosome-associated chaperones in prion formation and propagation

Current Genetics

Volumn 62, Issue 4, 2016, Pages 677-685

  Chernoff, Yury O ^a,b   Kiktev, Denis A ^a,b,c  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid aggregation; Hsp70; Protein folding; Saccharomyces cerevisiae; Translation

Indexed keywords

CHAPERONE; PRION PROTEIN; TRANSLATION TERMINATION FACTOR; MACROMOLECULE; PRION; PROTEIN AGGREGATE; PROTEIN BINDING;

CYTOSOL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STABILITY; REVIEW; RIBOSOME; YEAST; CHEMISTRY; GENETICS; MACROMOLECULE; METABOLISM; PRION; PROTEIN DOMAIN; PROTEINOSIS;

MACROMOLECULAR SUBSTANCES; MOLECULAR CHAPERONES; PRIONS; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RIBOSOMES;

EID: 84960353541     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-016-0586-2     Document Type: Review

References (61)

1. Abrams JL, Verghese J, Gibney PA, Morano KA (2014) Hierarchical functional specificity of cytosolic heat shock protein 70 (Hsp70) nucleotide exchange factors in yeast. J Biol Chem 289:13155–13167. doi:10.1074/jbc.M113.530014
2. Aguilar-Calvo P, Garcia C, Espinosa JC, Andreoletti O, Torres JM (2015) Prion and prion-like diseases in animals. Virus Res 207:82–93. doi:10.1016/j.virusres.2014.11.026
3. Albanese V, Reissmann S, Frydman J (2010) A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J Cell Biol 189:69–81. doi:10.1083/jcb.201001054
4. Ali M, Chernova TA, Newnam GP, Yin L, Shanks J, Karpova TS, Lee A, Laur O, Subramanian S, Kim D, McNally JG, Seyfried NT, Chernoff YO, Wilkinson KD (2014) Stress-dependent proteolytic processing of the actin assembly protein Lsb1 modulates a yeast prion. J Biol Chem 289:27625–27639. doi:10.1074/jbc.M114.582429
5. +]. Genetics 169:1227–1242. doi:10.1534/genetics.104.037168
6. Amor AJ, Castanzo DT, Delany SP, Selechnik DM, van Ooy A, Cameron DM (2015) The ribosome-associated complex antagonizes prion formation in yeast. Prion 9:144–164. doi:10.1080/19336896.2015.1022022
7. +] aggregates with heterogeneous protein composition. Mol Biol Cell 19:2433–2443. doi:10.1091/mbc.E08-01-0078
8. Blanco LP, Evans ML, Smith DR, Badtke MP, Chapman MR (2012) Diversity, biogenesis and function of microbial amyloids. Trends Microbiol 20:66–73. doi:10.1016/j.tim.2011.11.005
9. Buxbaum JN, Linke RP (2012) A molecular history of the amyloidoses. J Mol Biol 421:142–159. doi:10.1016/j.jmb.2012.01.024
10. +] prion-curing factor. Curr Genet 39:62–67
11. Chernoff YO, Newnam GP, Kumar J, Allen K, Zink AD (1999) 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 19:8103–8112
12. Chernova TA et al (2011) Prion induction by the short-lived, stress-induced protein Lsb2 is regulated by ubiquitination and association with the actin cytoskeleton. Mol Cell 43:242–252. doi:10.1016/j.molcel.2011.07.001
13. Chernova TA, Wilkinson KD, Chernoff YO (2014) Physiological and environmental control of yeast prions. FEMS Microbiol Rev 38:326–344. doi:10.1111/1574-6976.12053
14. Chiabudini M, Conz C, Reckmann F, Rospert S (2012) Ribosome-associated complex and Ssb are required for translational repression induced by polylysine segments within nascent chains. Mol Cell Biol 32:4769–4779. doi:10.1128/MCB.00809-12
15. Chiabudini M, Tais A, Zhang Y, Hayashi S, Wolfle T, Fitzke E, Rospert S (2014) Release factor eRF3 mediates premature translation termination on polylysine-stalled ribosomes in Saccharomyces cerevisiae. Mol Cell Biol 34:4062–4076. doi:10.1128/MCB.00799-14
16. +] prion in Saccharomyces cerevisiae. Genetics 147:507–519
17. +]. Cell 106:171–182
18. Dragovic Z, Shomura Y, Tzvetkov N, Hartl FU, Bracher A (2006) Fes1p acts as a nucleotide exchange factor for the ribosome-associated molecular chaperone Ssb1p. Biol Chem 387:1593–1600. doi:10.1515/BC.2006.198
19. Fiaux J, Horst J, Scior A, Preissler S, Koplin A, Bukau B, Deuerling E (2010) Structural analysis of the ribosome-associated complex (RAC) reveals an unusual Hsp70/Hsp40 interaction. J Biol Chem 285:3227–3234. doi:10.1074/jbc.M109.075804
20. Flynn GC, Chappell TG, Rothman JE (1989) Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245:385–390
21. Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid—from bacteria to humans. Trends Biochem Sci 32:217–224. doi:10.1016/j.tibs.2007.03.003
22. Gautschi M et al (2001) RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin. Proc Natl Acad Sci USA 98:3762–3767. doi:10.1073/pnas.071057198
23. Ho YH, Gasch AP (2015) Exploiting the yeast stress-activated signaling network to inform on stress biology and disease signaling. Curr Genet 61:503–511. doi:10.1007/s00294-015-0491-0
24. Holmes DL, Lancaster AK, Lindquist S, Halfmann R (2013) Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153:153–165. doi:10.1016/j.cell.2013.02.026
25. Huang P, Gautschi M, Walter W, Rospert S, Craig EA (2005) The Hsp70 Ssz1 modulates the function of the ribosome-associated J-protein Zuo1. Nat Struct Mol Biol 12:497–504. doi:10.1038/nsmb942
26. Jaiswal H, Conz C, Otto H, Wolfle T, Fitzke E, Mayer MP, Rospert S (2011) The chaperone network connected to human ribosome-associated complex. Mol Cell Biol 31:1160–1173. doi:10.1128/MCB.00986-10
27. James P, Pfund C, Craig EA (1997) Functional specificity among Hsp70 molecular chaperones. Science 275:387–389
28. Kabani M, Melki R (2015a) Sup35p in its soluble and prion states is packaged inside extracellular vesicles. MBio. doi:10.1128/mBio.01017-15
29. Kabani M, Melki R (2015b) More than just trash bins? Potential roles for extracellular vesicles in the vertical and horizontal transmission of yeast prions. Curr Genet. doi:10.1007/s00294-015-0534-6
30. Kiktev DA, Melomed MM, Lu CD, Newnam GP, Chernoff YO (2015) Feedback control of prion formation and propagation by the ribosome-associated chaperone complex. Mol Microbiol 96:621–632. doi:10.1111/mmi.12960
31. Klaips CL, Hochstrasser ML, Langlois CR, Serio TR (2015) Correction: spatial quality control bypasses cell-based limitations on proteostasis to promote prion curing. Elife 4:e06494. doi:10.7554/eLife.06494
32. Kominek J, Marszalek J, Neuveglise C, Craig EA, Williams BL (2013) The complex evolutionary dynamics of Hsp70s: a genomic and functional perspective. Genome Biol Evol 5:2460–2477. doi:10.1093/gbe/evt192
33. Koplin A, Preissler S, Ilina Y, Koch M, Scior A, Erhardt M, Deuerling E (2010) A dual function for chaperones SSB-RAC and the NAC nascent polypeptide-associated complex on ribosomes. J Cell Biol 189:57–68. doi:10.1083/jcb.200910074
34. +] and their prion-specific effects. Curr Biol 10:1443–1446
35. Li J, Wu Y, Qian X, Sha B (2006) Crystal structure of yeast Sis1 peptide-binding fragment and Hsp70 Ssa1 C-terminal complex. Biochem J 398:353–360. doi:10.1042/BJ20060618
36. Liebman SW, Chernoff YO (2012) Prions in yeast. Genetics 191:1041–1072. doi:10.1534/genetics.111.137760
37. Lopez N, Halladay J, Walter W, Craig EA (1999) SSB, encoding a ribosome-associated chaperone, is coordinately regulated with ribosomal protein genes. J Bacteriol 181:3136–3143
38. Malinverni D, Marsili S, Barducci A, De Los Rios P (2015) Large-scale conformational transitions and dimerization are encoded in the amino-acid sequences of Hsp70 haperones. PLoS Comput Biol 11:e1004262. doi:10.1371/journal.pcbi.1004262
39. Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA (1992) The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71:97–105
40. Newnam GP, Wegrzyn RD, Lindquist SL, Chernoff YO (1999) Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol Cell Biol 19:1325–1333
41. Newnam GP, Birchmore JL, Chernoff YO (2011) Destabilization and recovery of a yeast prion after mild heat shock. J Mol Biol 408:432–448. doi:10.1016/j.jmb.2011.02.034
42. Nizhnikov AA, Antonets KS, Inge-Vechtomov SG, Derkatch IL (2014) Modulation of efficiency of translation termination in Saccharomyces cerevisiae. Prion 8:247–260. doi:10.4161/pri.29851
43. +] prion. Cell 106:183–194
44. Palleros DR, Welch WJ, Fink AL (1991) Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding. Proc Natl Acad Sci USA 88:5719–5723
45. Protacio RU, Storey AJ, Davidson MK, Wahls WP (2015) Nonsense codon suppression in fission yeast due to mutations of tRNA(Ser. 11) and translation release factor Sup35 (eRF3). Curr Genet 61:165–173. doi:10.1007/s00294-014-0465-7
46. Prunuske AJ, Waltner JK, Kuhn P, Gu B, Craig EA (2012) Role for the molecular chaperones Zuo1 and Ssz1 in quorum sensing via activation of the transcription factor Pdr1. Proc Natl Acad Sci USA 109:472–477. doi:10.1073/pnas.1119184109
47. Qian X, Hou W, Zhengang L, Sha B (2002) Direct interactions between molecular chaperones heat-shock protein (Hsp) 70 and Hsp40: yeast Hsp70 Ssa1 binds the extreme C-terminal region of yeast Hsp40 Sis1. Biochem J 361:27–34
48. Reidy M, Masison DC (2011) Modulation and elimination of yeast prions by protein chaperones and co-chaperones. Prion 5:245–249. doi:10.4161/pri.17749
49. Rikhvanov EG, Romanova NV, Chernoff YO (2007) Chaperone effects on prion and nonprion aggregates. Prion 1:217–222
50. Sarbeng EB et al (2015) A functional DnaK dimer is essential for the efficient interaction with Hsp40 heat shock protein. J Biol Chem 290:8849–8862. doi:10.1074/jbc.M114.596288
51. Shaner L, Sousa R, Morano KA (2006) Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. Biochemistry 45:15075–15084. doi:10.1021/bi061279k
52. Sharma D, Masison DC (2009) Hsp70 structure, function, regulation and influence on yeast prions. Protein Pept Lett 16:571–581
53. Shorter J, Lindquist S (2008) Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J 27:2712–2724. doi:10.1038/emboj.2008.194
54. Tyedmers J, Madariaga ML, Lindquist S (2008) Prion switching in response to environmental stress. PLoS Biol 6:e294. doi:10.1371/journal.pbio.0060294
55. Wallace EW et al (2015) Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress. Cell 162:1286–1298. doi:10.1016/j.cell.2015.08.041
56. Werner-Washburne M, Craig EA (1989) Expression of members of the Saccharomyces cerevisiae hsp70 multigene family. Genome 31:684–689
57. Werner-Washburne M, Stone DE, Craig EA (1987) Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol Cell Biol 7:2568–2577
58. Wickner RB, Shewmaker FP, Bateman DA, Edskes HK, Gorkovskiy A, Dayani Y, Bezsonov EE (2015) Yeast prions: structure, biology, and prion-handling systems. Microbiol Mol Biol Rev 79:1–17. doi:10.1128/MMBR.00041-14
59. Willmund F et al (2013) The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152:196–209. doi:10.1016/j.cell.2012.12.001
60. 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. doi:10.1083/jcb.201201074
61. Zhang Y et al (2014) Structural basis for interaction of a cotranslational chaperone with the eukaryotic ribosome. Nat Struct Mol Biol 21:1042–1046. doi:10.1038/nsmb.2908