Physiological and environmental control of yeast prions

FEMS Microbiology Reviews

Volumn 38, Issue 2, 2014, Pages 326-344

  Chernova, Tatiana A ^a   Wilkinson, Keith D ^a   Chernoff, Yury O ^b,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

Amyloid; Chaperone; Cytoskeleton; Heat shock; Quality control; Ubiquitin

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; PRION PROTEIN; PROTEASOME; UBIQUITIN;

ACTIN FILAMENT; CELL DIVISION; CYTOSKELETON; DEGRADATION; ENVIRONMENTAL STRESS; EPIGENETICS; MICROPROPAGATION; NONHUMAN; PRION; PROTEIN AGGREGATION; PROTEIN INTERACTION; PROTEIN QUALITY; REVIEW; YEAST;

EUKARYOTA; MAMMALIA; MAMMALIAN PRION;

AMYLOID; CHAPERONE; CYTOSKELETON; HEAT SHOCK; QUALITY CONTROL; UBIQUITIN;

ACTIN CYTOSKELETON; ADAPTATION, PHYSIOLOGICAL; ENVIRONMENT; HEAT-SHOCK PROTEINS; PRIONS; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE; UBIQUITIN;

EID: 84896707187     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/1574-6976.12053     Document Type: Review

References (192)

1. Aguilaniu H, Gustafsson L, Rigoulet M & Nystrom T (2003) Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299: 1751-1753.
2. Aguzzi A & O'Connor T (2010) Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nat Rev Drug Discov 9: 237-248.
3. Aguzzi A & Rajendran L (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64: 783-790.
4. Alberti S, Halfmann R, King O, Kapila A & Lindquist S (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137: 146-158.
5. Allen KD, Wegrzyn RD, Chernova TA et al. (2005) Hsp70 chaperones as modulators of prion life cycle: novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion [PSI+]. Genetics 169: 1227-1242.
6. Allen KD, Chernova TA, Tennant EP, Wilkinson KD & Chernoff YO (2007) Effects of ubiquitin system alterations on the formation and loss of a yeast prion. J Biol Chem 282: 3004-3013.
7. Andre R & Tabrizi SJ (2012) Misfolded PrP and a novel mechanism of proteasome inhibition. Prion 6: 32-36.
8. Apodaca J, Kim I & Rao H (2006) Cellular tolerance of prion protein PrP in yeast involves proteolysis and the unfolded protein response. Biochem Biophys Res Commun 347: 319-326.
9. Bailleul PA, Newnam GP, Steenbergen JN & Chernoff YO (1999) Genetic study of interactions between the cytoskeletal assembly protein sla1 and prion-forming domain of the release factor Sup35 (eRF3) in Saccharomyces cerevisiae. Genetics 153: 81-94.
10. Bailleul-Winslett PA, Newnam GP, Wegrzyn RD & Chernoff YO (2000) An antiprion effect of the anticytoskeletal drug latrunculin A in yeast. Gene Expr 9: 145-156.
11. Bennett EJ, Bence NF, Jayakumar R & Kopito RR (2005) Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol Cell 17: 351-365.
12. Bhattacharyya NP, Banerjee M & Majumder P (2008) Huntington's disease: roles of huntingtin-interacting protein 1 (HIP-1) and its molecular partner HIPPI in the regulation of apoptosis and transcription. FEBS J 275: 4271-4279.
13. Blanco LP, Evans ML, Smith DR, Badtke MP & Chapman MR (2012) Diversity, biogenesis and function of microbial amyloids. Trends Microbiol 20: 66-73.
14. Bradley ME & Liebman SW (2003) Destabilizing interactions among [PSI(+)] and [PIN(+)] yeast prion variants. Genetics 165: 1675-1685.
15. Bradley ME, Edskes HK, Hong JY, Wickner RB & Liebman SW (2002) Interactions among prions and prion "strains" in yeast. P Natl Acad Sci USA 99(suppl 4): 16392-16399.
16. Byrne LJ, Cole DJ, Cox BS, Ridout MS, Morgan BJ & Tuite MF (2009) The number and transmission of [PSI] prion seeds (Propagons) in the yeast Saccharomyces cerevisiae. PLoS One 4: e4670.
17. Chernoff YO (2001) Mutation processes at the protein level: is Lamarck back? Mutat Res 488: 39-64.
18. Chernoff YO (2007) Stress and prions: lessons from the yeast model. FEBS Lett 581: 3695-3701.
19. Chernoff YO (2008) Identity determinants of infectious proteins. P Natl Acad Sci USA 105: 13191-13192.
20. Chernoff YO, Inge-Vechtomov SG, Derkach IL, Ptyushkina MV, Tarunina OV, Dagkesamanskaya AR & Ter-Avanesyan MD (1992) Dosage-dependent translational suppression in yeast Saccharomyces cerevisiae. Yeast 8: 489-499.
21. Chernoff YO, Derkach IL & Inge-Vechtomov SG (1993) Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr Genet 24: 268-270.
22. 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.
23. 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.
24. Chernoff YO, Galkin AP, Lewitin E, Chernova TA, Newnam GP & Belenkiy SM (2000) Evolutionary conservation of prion-forming abilities of the yeast Sup35 protein. Mol Microbiol 35: 865-876.
25. Chernova TA, Allen KD, Wesoloski LM, Shanks JR, Chernoff YO & Wilkinson KD (2003) Pleiotropic effects of Ubp6 loss on drug sensitivities and yeast prion are due to depletion of the free ubiquitin pool. J Biol Chem 278: 52102-52115.
26. Chernova TA, Romanyuk AV, Karpova TS 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.
27. Chiti F & Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
28. Ciechanover A & Brundin P (2003) The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40: 427-446.
29. Clavaguera F, Bolmont T, Crowther RA et al. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11: 909-913.
30. Colby DW & Prusiner SB (2011) Prions. Cold Spring Harb Perspect Biol 3: a006833.
31. Coustou V, Deleu C, Saupe S & Begueret J (1997) The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. P Natl Acad Sci USA 94: 9773-9778.
32. Cox BS (1965) ψ, a cytoplasmic suppressor of super-suppressor in yeast. Heredity 20: 505-521.
33. 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.
34. Cox BS, Byrne LJ & Tuite MF (2007) Prion stability. Prion 1: 170-178.
35. Dennissen FJ, Kholod N & van Leeuwen FW (2012) The ubiquitin proteasome system in neurodegenerative diseases: culprit, accomplice or victim? Prog Neurobiol 96: 190-207.
36. Derdowski A, Sindi SS, Klaips CL, DiSalvo S & Serio TR (2010) A size threshold limits prion transmission and establishes phenotypic diversity. Science 330: 680-683.
37. Deriziotis P & Tabrizi SJ (2008) Prions and the proteasome. Biochim Biophys Acta 1782: 713-722.
38. Derkatch IL & Liebman SW (2007) Prion-prion interactions. Prion 1: 161-169.
39. 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.
40. 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.
41. Derkatch IL, Bradley ME, Masse SV, Zadorsky SP, Polozkov GV, Inge-Vechtomov SG & Liebman SW (2000) Dependence and independence of [PSI(+)] and [PIN(+)]: a two-prion system in yeast? EMBO J 19: 1942-1952.
42. Derkatch IL, Bradley ME, Hong JY & Liebman SW (2001) Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106: 171-182.
43. Derkatch IL, Uptain SM, Outeiro TF, Krishnan R, Lindquist SL & Liebman SW (2004) Effects of Q/N-rich, polyQ, and non-polyQ amyloids on the de novo formation of the [PSI+] prion in yeast and aggregation of Sup35 in vitro. P Natl Acad Sci USA 101: 12934-12939.
44. Douglas PM, Treusch S, Ren HY, Halfmann R, Duennwald ML, Lindquist S & Cyr DM (2008) Chaperone-dependent amyloid assembly protects cells from prion toxicity. P Natl Acad Sci USA 105: 7206-7211.
45. 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.
46. 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.
47. Erjavec N, Larsson L, Grantham J & Nystrom T (2007) Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev 21: 2410-2421.
48. Erjavec N, Cvijovic M, Klipp E & Nystrom T (2008) Selective benefits of damage partitioning in unicellular systems and its effects on aging. P Natl Acad Sci USA 105: 18764-18769.
49. 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.
50. Favaloro V, Spasic M, Schwappach B & Dobberstein B (2008) Distinct targeting pathways for the membrane insertion of tail-anchored (TA) proteins. J Cell Sci 121: 1832-1840.
51. Ferreira PC, Ness F, Edwards SR, Cox BS & Tuite MF (2001) The elimination of the yeast [PSI+] prion by guanidine hydrochloride is the result of Hsp104 inactivation. Mol Microbiol 40: 1357-1369.
52. Fowler DM & Kelly JW (2009) Aggregating knowledge about prions and amyloid. Cell 137: 20-22.
53. Frost B, Jacks RL & Diamond MI (2009) Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284: 12845-12852.
54. Ganusova EE, Ozolins LN, Bhagat S, Newnam GP, Wegrzyn RD, Sherman MY & Chernoff YO (2006) Modulation of prion formation, aggregation, and toxicity by the actin cytoskeleton in yeast. Mol Cell Biol 26: 617-629.
55. Garrity SJ, Sivanathan V, Dong J, Lindquist S & Hochschild A (2010) Conversion of a yeast prion protein to an infectious form in bacteria. P Natl Acad Sci USA 107: 10596-10601.
56. Gasch AP, Spellman PT, Kao CM et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
57. Gautschi M, Mun A, Ross S & Rospert S (2002) A functional chaperone triad on the yeast ribosome. P Natl Acad Sci USA 99: 4209-4214.
58. Gebbink MF, Claessen D, Bouma B, Dijkhuizen L & Wosten HA (2005) Amyloids-a functional coat for microorganisms. Nat Rev Microbiol 3: 333-341.
59. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM & Anderson P (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15: 5383-5398.
60. Glover JR & Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82.
61. Glover JR & Lum R (2009) Remodeling of protein aggregates by Hsp104. Protein Pept Lett 16: 587-597.
62. 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.
63. Goldberg AL (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899.
64. Gong H, Romanova NV, Allen KD et al. (2012) Polyglutamine toxicity is controlled by prion composition and gene dosage in yeast. PLoS Genet 8: e1002634.
65. Grishin AV, Rothenberg M, Downs MA & Blumer KJ (1998) Mot3, a Zn finger transcription factor that modulates gene expression and attenuates mating pheromone signaling in Saccharomyces cerevisiae. Genetics 149: 879-892.
66. Halfmann R, Wright JR, Alberti S, Lindquist S & Rexach M (2012a) Prion formation by a yeast GLFG nucleoporin. Prion 6: 391-399.
67. Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK & Lindquist S (2012b) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482: 363-368.
68. Harbison CT, Gordon DB, Lee TI et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
69. Harrison PM & Gerstein M (2003) A method to assess compositional bias in biological sequences and its application to prion-like glutamine/asparagine-rich domains in eukaryotic proteomes. Genome Biol 4: R40.
70. Heinrich SU & Lindquist S (2011) Protein-only mechanism induces self-perpetuating changes in the activity of neuronal Aplysia cytoplasmic polyadenylation element binding protein (CPEB). P Natl Acad Sci USA 108: 2999-3004.
71. Helsen CW & Glover JR (2012a) A new perspective on Hsp104-mediated propagation and curing of the yeast prion [PSI(+)]. Prion 6: 234-239.
72. Helsen CW & Glover JR (2012b) Insight into molecular basis of curing of [PSI+] prion by overexpression of 104-kDa heat shock protein (Hsp104). J Biol Chem 287: 542-556.
73. Hershko A & Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479.
74. Holmes DL, Lancaster AK, Lindquist S & Halfmann R (2013) Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153: 153-165.
75. Hundley H, Eisenman H, Walter W, Evans T, Hotokezaka Y, Wiedmann M & Craig E (2002) The in vivo function of the ribosome-associated Hsp70, Ssz1, does not require its putative peptide-binding domain. P Natl Acad Sci USA 99: 4203-4208.
76. Iconomidou VA & Hamodrakas SJ (2008) Natural protective amyloids. Curr Protein Pept Sci 9: 291-309.
77. Ikeda F & Dikic I (2008) Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: beyond the Usual Suspects' review series. EMBO Rep 9: 536-542.
78. Inaba M & Yamashita YM (2012) Asymmetric stem cell division: precision for robustness. Cell Stem Cell 11: 461-469.
79. Iwata A, Christianson JC, Bucci M, Ellerby LM, Nukina N, Forno LS & Kopito RR (2005) Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. P Natl Acad Sci USA 102: 13135-13140.
80. James P, Pfund C & Craig EA (1997) Functional specificity among Hsp70 molecular chaperones. Science 275: 387-389.
81. Johnston JA, Ward CL & Kopito RR (1998) Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143: 1883-1898.
82. Joseph SB & Kirkpatrick M (2008) Effects of the [PSI+] prion on rates of adaptation in yeast. J Evol Biol 21: 773-780.
83. Jung G, Jones G & Masison DC (2002) Amino acid residue 184 of yeast Hsp104 chaperone is critical for prion-curing by guanidine, prion propagation, and thermotolerance. P Natl Acad Sci USA 99: 9936-9941.
84. Kaganovich D, Kopito R & Frydman J (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454: 1088-1095.
85. Kerscher O, Felberbaum R & Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22: 159-180.
86. Kiktev DA, Patterson JC, Muller S, Bariar B, Pan T & Chernoff YO (2012) Regulation of chaperone effects on a yeast prion by cochaperone Sgt2. Mol Cell Biol 32: 4960-4970.
87. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M & Hartl FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82: 323-355.
88. Kirkin V, McEwan DG, Novak I & Dikic I (2009) A role for ubiquitin in selective autophagy. Mol Cell 34: 259-269.
89. Kochneva-Pervukhova NV, Poznyakovski AI, Smirnov VN & Ter-Avanesyan MD (1998) C-terminal truncation of the Sup35 protein increases the frequency of de novo generation of a prion-based [PSI+] determinant in Saccharomyces cerevisiae. Curr Genet 34: 146-151.
90. Kochneva-Pervukhova NV, Alexandrov AI & Ter-Avanesyan MD (2012) Amyloid-mediated sequestration of essential proteins contributes to mutant huntingtin toxicity in yeast. PLoS One 7: e29832.
91. Kristiansen M, Deriziotis P, Dimcheff DE et al. (2007) Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol Cell 26: 175-188.
92. Kryndushkin DS, Shewmaker F & Wickner RB (2008) Curing of the [URE3] prion by Btn2p, a Batten disease-related protein. EMBO J 27: 2725-2735.
93. Kryndushkin DS, Engel A, Edskes H & Wickner RB (2011) Molecular chaperone Hsp104 can promote yeast prion generation. Genetics 188: 339-348.
94. Kurahashi H, Ishiwata M, Shibata S & Nakamura Y (2008) A regulatory role of the Rnq1 nonprion domain for prion propagation and polyglutamine aggregates. Mol Cell Biol 28: 3313-3323.
95. Kurahashi H, Pack CG, Shibata S, Oishi K, Sako Y & Nakamura Y (2011) [PSI(+)] aggregate enlargement in rnq1 nonprion domain mutants, leading to a loss of prion in yeast. Genes Cells 16: 576-589.
96. Kushnirov VV & Ter-Avanesyan MD (1998) Structure and replication of yeast prions. Cell 94: 13-16.
97. Lacroute F (1971) Non-Mendelian mutation allowing ureidosuccinic acid uptake in yeast. J Bacteriol 106: 519-522.
98. Liebman SW & Chernoff YO (2012) Prions in yeast. Genetics 191: 1041-1072.
99. Liu B, Larsson L, Caballero A, Hao X, Oling D, Grantham J & Nystrom T (2010) The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140: 257-267.
100. Liu B, Larsson L, Franssens V et al. (2011) Segregation of protein aggregates involves actin and the polarity machinery. Cell 147: 959-961.
101. Lowe J, Blanchard A, Morrell K et al. (1988) Ubiquitin is a common factor in intermediate filament inclusion bodies of diverse type in man, including those of Parkinson's disease, Pick's disease, and Alzheimer's disease, as well as Rosenthal fibres in cerebellar astrocytomas, cytoplasmic bodies in muscle, and mallory bodies in alcoholic liver disease. J Pathol 155: 9-15.
102. Ma J & Lindquist S (2001) Wild-type PrP and a mutant associated with prion disease are subject to retrograde transport and proteasome degradation. P Natl Acad Sci USA 98: 14955-14960.
103. Madania A, Dumoulin P, Grava S et al. (1999) The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol Biol Cell 10: 3521-3538.
104. Maji SK, Perrin MH, Sawaya MR et al. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325: 328-332.
105. Majumdar A, Cesario WC, White-Grindley E et al. (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148: 515-529.
106. 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.
107. Manogaran AL, Hong JY, Hufana J, Tyedmers J, Lindquist S & Liebman SW (2011) Prion formation and polyglutamine aggregation are controlled by two classes of genes. PLoS Genet 7: e1001386.
108. Mathur V, Taneja V, Sun Y & Liebman SW (2010) Analyzing the birth and propagation of two distinct prions, [PSI+] and [Het-s](y), in yeast. Mol Biol Cell 21: 1449-1461.
109. Mattoo RU, Sharma SK, Priya S, Finka A & Goloubinoff P (2013) Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with hsp70 to solubilize protein aggregates. J Biol Chem 288: 21399-21411.
110. Mayer RJ, Lowe J, Lennox G, Doherty F & Landon M (1989) Intermediate filaments and ubiquitin: a new thread in the understanding of chronic neurodegenerative diseases. Prog Clin Biol Res 317: 809-818.
111. McGlinchey RP, Shewmaker F, McPhie P, Monterroso B, Thurber K & Wickner RB (2009) The repeat domain of the melanosome fibril protein Pmel17 forms the amyloid core promoting melanin synthesis. P Natl Acad Sci USA 106: 13731-13736.
112. Meriin AB, Zhang X, He X, Newnam GP, Chernoff YO & Sherman MY (2002) Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 157: 997-1004.
113. Meriin AB, Zhang X, Miliaras NB et al. (2003) Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol Cell Biol 23: 7554-7565.
114. Michelitsch MD & Weissman JS (2000) A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. P Natl Acad Sci USA 97: 11910-11915.
115. Mullally JE, Chernova T & Wilkinson KD (2006) Doa1 is a Cdc48 adapter that possesses a novel ubiquitin binding domain. Mol Cell Biol 26: 822-830.
116. Muralidharan V, Oksman A, Pal P, Lindquist S & Goldberg DE (2012) Plasmodium falciparum heat shock protein 110 stabilizes the asparagine repeat-rich parasite proteome during malarial fevers. Nat Commun 3: 1310.
117. Nakayashiki T, Kurtzman CP, Edskes HK & Wickner RB (2005) Yeast prions [URE3] and [PSI+] are diseases. P Natl Acad Sci USA 102: 10575-10580.
118. Namy O, Galopier A, Martini C, Matsufuji S, Fabret C & Rousset JP (2008) Epigenetic control of polyamines by the prion [PSI+]. Nat Cell Biol 10: 1069-1075.
119. 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.
120. Newby GA & Lindquist S (2013) Blessings in disguise: biological benefits of prion-like mechanisms. Trends Cell Biol 23: 251-259.
121. 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.
122. Newnam GP, Birchmore JL & Chernoff YO (2011) Destabilization and recovery of a yeast prion after mild heat shock. J Mol Biol, 408: 432-448.
123. Osherovich LZ & Weissman JS (2001) Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 106: 183-194.
124. Osherovich LZ & Weissman JS (2002) The utility of prions. Dev Cell 2: 143-151.
125. Park KW, Hahn JS, Fan Q, Thiele DJ & Li L (2006) De novo appearance and "strain" formation of yeast prion [PSI+] are regulated by the heat-shock transcription factor. Genetics 173: 35-47.
126. Park YN, Morales D, Rubinson EH, Masison D, Eisenberg E & Greene LE (2012) Differences in the curing of [PSI+] prion by various methods of Hsp104 inactivation. PLoS One 7: e37692.
127. Patel BK, Gavin-Smyth J & Liebman SW (2009) The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat Cell Biol 11: 344-349.
128. Peng J, Schwartz D, Elias JE et al. (2003) A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21: 921-926.
129. Pickart CM & Fushman D (2004) Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 8: 610-616.
130. Prusiner SB (1998) Prions. P Natl Acad Sci USA 95: 13363-13383.
131. Prusiner SB (2012) Cell biology. A unifying role for prions in neurodegenerative diseases. Science 336: 1511-1513.
132. Reidy M & Masison DC (2011) Modulation and elimination of yeast prions by protein chaperones and co-chaperones. Prion 5: 245-249.
133. Reidy M, Miot M & Masison DC (2012) Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions. Genetics 192: 185-193.
134. Resende CG, Outeiro TF, Sands L, Lindquist S & Tuite MF (2003) Prion protein gene polymorphisms in Saccharomyces cerevisiae. Mol Microbiol 49: 1005-1017.
135. Rikhvanov EG, Romanova NV & Chernoff YO (2007) Chaperone effects on prion and nonprion aggregates. Prion 1: 217-222.
136. Roberts BT, Moriyama H & Wickner RB (2004) [URE3] prion propagation is abolished by a mutation of the primary cytosolic Hsp70 of budding yeast. Yeast 21: 107-117.
137. Rogoza T, Goginashvili A, Rodionova S et al. (2010) Non-Mendelian determinant [ISP+] in yeast is a nuclear-residing prion form of the global transcriptional regulator Sfp1. P Natl Acad Sci USA 107: 10573-10577.
138. Romer L & Scheibel T (2008) The elaborate structure of spider silk: structure and function of a natural high performance fiber. Prion 2: 154-161.
139. Ross CD, McCarty BR, Hamilton M, Ben-Hur A & Ross ED (2009) A promiscuous prion: efficient induction of [URE3] prion formation by heterologous prion domains. Genetics 183: 929-940.
140. Saupe SJ (2007) A short history of small s: a prion of the fungus Podospora anserina. Prion 1: 110-115.
141. Saupe SJ (2011) The [Het-s] prion of Podospora anserina and its role in heterokaryon incompatibility. Semin Cell Dev Biol 22: 460-468.
142. Schuldiner M, Metz J, Schmid V et al. (2008) The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134: 634-645.
143. Schwimmer C & Masison DC (2002) Antagonistic interactions between yeast [PSI(+)] and [URE3] prions and curing of [URE3] by Hsp70 protein chaperone Ssa1p but not by Ssa2p. Mol Cell Biol 22: 3590-3598.
144. Sertil O, Kapoor R, Cohen BD, Abramova N & Lowry CV (2003) Synergistic repression of anaerobic genes by Mot3 and Rox1 in Saccharomyces cerevisiae. Nucleic Acids Res 31: 5831-5837.
145. Seyffer F, Kummer E, Oguchi Y et al. (2012) Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces. Nat Struct Mol Biol 19: 1347-1355.
146. Sharma D & Masison DC (2008) Functionally redundant isoforms of a yeast Hsp70 chaperone subfamily have different antiprion effects. Genetics 179: 1301-1311.
147. Sharma D & Masison DC (2011) Single methyl group determines prion propagation and protein degradation activities of yeast heat shock protein (Hsp)-70 chaperones Ssa1p and Ssa2p. P Natl Acad Sci USA 108: 13665-13670.
148. Shorter J (2011) The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One 6: e26319.
149. Si K, Lindquist S & Kandel ER (2003) A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115: 879-891.
150. Si K, Choi YB, White-Grindley E, Majumdar A & Kandel ER (2010) Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140: 421-435.
151. Sideri TC, Stojanovski K, Tuite MF & Grant CM (2010) Ribosome-associated peroxiredoxins suppress oxidative stress-induced de novo formation of the [PSI+] prion in yeast. P Natl Acad Sci USA 107: 6394-6399.
152. Sideri TC, Koloteva-Levine N, Tuite MF & Grant CM (2011) Methionine oxidation of Sup35 protein induces formation of the [PSI+] prion in a yeast peroxiredoxin mutant. J Biol Chem 286: 38924-38931.
153. Sondheimer N & Lindquist S (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5: 163-172.
154. Song C, Kanthasamy A, Jin H, Anantharam V & Kanthasamy AG (2011) Paraquat induces epigenetic changes by promoting histone acetylation in cell culture models of dopaminergic degeneration. Neurotoxicology 32: 586-595.
155. Specht S, Miller SB, Mogk A & Bukau B (2011) Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J Cell Biol 195: 617-629.
156. Spokoini R, Moldavski O, Nahmias Y, England JL, Schuldiner M & Kaganovich D (2012) Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep 2: 738-747.
157. Stefanovic S & Hegde RS (2007) Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128: 1147-1159.
158. Stein KC & True HL (2011) The [RNQ+] prion: a model of both functional and pathological amyloid. Prion 5: 291-298.
159. Suzuki G & Tanaka M (2013) Active conversion to the prion state as a molecular switch for cellular adaptation to environmental stress. BioEssays 35: 12-16.
160. Suzuki G, Shimazu N & Tanaka M (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336: 355-359.
161. Tanaka M, Collins SR, Toyama BH & Weissman JS (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442: 585-589.
162. Taneja V, Maddelein ML, Talarek N, Saupe SJ & Liebman SW (2007) A non-Q/N-rich prion domain of a foreign prion, [Het-s], can propagate as a prion in yeast. Mol Cell 27: 67-77.
163. Tessarz P, Schwarz M, Mogk A & Bukau B (2009) The yeast AAA+ chaperone Hsp104 is part of a network that links the actin cytoskeleton with the inheritance of damaged proteins. Mol Cell Biol 29: 3738-3745.
164. Toret CP & Drubin DG (2006) The budding yeast endocytic pathway. J Cell Sci 119: 4585-4587.
165. Treusch S & Lindquist S (2012) An intrinsically disordered yeast prion arrests the cell cycle by sequestering a spindle pole body component. J Cell Biol 197: 369-379.
166. True HL & Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477-483.
167. True HL, Berlin I & Lindquist SL (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431: 184-187.
168. Tyedmers J, Madariaga ML & Lindquist S (2008) Prion switching in response to environmental stress. PLoS Biol 6: e294.
169. Tyedmers J, Treusch S, Dong J, McCaffery JM, Bevis B & Lindquist S (2010) Prion induction involves an ancient system for the sequestration of aggregated proteins and heritable changes in prion fragmentation. P Natl Acad Sci USA 107: 8633-8638.
170. Venkatraman P, Wetzel R, Tanaka M, Nukina N & Goldberg AL (2004) Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol Cell 14: 95-104.
171. Verghese J, Abrams J, Wang Y & Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76: 115-158.
172. Vishveshwara N & Liebman SW (2009) Heterologous cross-seeding mimics cross-species prion conversion in a yeast model. BMC Biol 7: 26.
173. Vishveshwara N, Bradley ME & Liebman SW (2009) Sequestration of essential proteins causes prion associated toxicity in yeast. Mol Microbiol 73: 1101-1114.
174. Vitrenko YA, Gracheva EO, Richmond JE & Liebman SW (2007) Visualization of aggregation of the Rnq1 prion domain and cross-seeding interactions with Sup35NM. J Biol Chem 282: 1779-1787.
175. Walker LC & LeVine H 3rd (2012) Corruption and spread of pathogenic proteins in neurodegenerative diseases. J Biol Chem 287: 33109-33115.
176. Wang Y, Meriin AB, Zaarur N, Romanova NV, Chernoff YO, Costello CE & Sherman MY (2009) Abnormal proteins can form aggresome in yeast: aggresome-targeting signals and components of the machinery. FASEB J 23: 451-463.
177. Wegrzyn RD, Bapat K, Newnam GP, Zink AD & Chernoff YO (2001) Mechanism of prion loss after Hsp104 inactivation in yeast. Mol Cell Biol 21: 4656-4669.
178. Weimer JM, Chattopadhyay S, Custer AW & Pearce DA (2005) Elevation of Hook1 in a disease model of Batten disease does not affect a novel interaction between Ankyrin G and Hook1. Biochem Biophys Res Commun 330: 1176-1181.
179. Weisberg SJ, Lyakhovetsky R, Werdiger AC, Gitler AD, Soen Y & Kaganovich D (2012) Compartmentalization of superoxide dismutase 1 (SOD1G93A) aggregates determines their toxicity. P Natl Acad Sci USA 109: 15811-15816.
180. Welchman RL, Gordon C & Mayer RJ (2005) Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol 6: 599-609.
181. 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.
182. Wickner RB (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569.
183. Wickner RB (1997) A new prion controls fungal cell fusion incompatibility. P Natl Acad Sci USA 94: 10012-10014.
184. Wickner RB, Edskes HK, Bateman D, Kelly AC & Gorkovskiy A (2011) The yeast prions [PSI+] and [URE3] are molecular degenerative diseases. Prion 5: 258-262.
185. Willmund F, del Alamo M, Pechmann S, Chen T, Albanese V, Dammer EB, Peng J & Frydman J (2013) The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152: 196-209.
186. Winkler J, Tyedmers J, Bukau B & Mogk A (2012a) Chaperone networks in protein disaggregation and prion propagation. J Struct Biol 179: 152-160.
187. Winkler J, Tyedmers J, Bukau B & Mogk A (2012b) Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J Cell Biol 198: 387-404.
188. 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.
189. Yedidia Y, Horonchik L, Tzaban S, Yanai A & Taraboulos A (2001) Proteasomes and ubiquitin are involved in the turnover of the wild-type prion protein. EMBO J 20: 5383-5391.
190. Zhao X, Park YN, Todor H, Moomau C, Masison D, Eisenberg E & Greene LE (2012) Sequestration of Sup35 by aggregates of huntingtin fragments causes toxicity of [PSI+] yeast. J Biol Chem 287: 23346-23355.
191. Zhou P, Derkatch IL & Liebman SW (2001) The relationship between visible intracellular aggregates that appear after overexpression of Sup35 and the yeast prion-like elements [PSI(+)] and [PIN(+)]. Mol Microbiol 39: 37-46.
192. Zhou C, Slaughter BD, Unruh JR, Eldakak A, Rubinstein B & Li R (2011) Motility and segregation of Hsp104-associated protein aggregates in budding yeast. Cell 147: 1186-1196.