Rebels with a cause: Molecular features and physiological consequences of yeast prions

FEMS Yeast Research

Volumn 14, Issue 1, 2014, Pages 136-147

  Garcia, David M ^a   Jarosz, Daniel F ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid; Chaperones; Epigenetics; Prions; Protein aggregation

Indexed keywords

CHAPERONE; FUNGAL PROTEIN; PRION PROTEIN; PRION;

AMINO ACID SEQUENCE; ARTICLE; CELL FUNCTION; ENVIRONMENTAL STRESS; EPIGENETICS; GENE EXPRESSION; GENETIC VARIABILITY; INHERITANCE; MOLECULAR BIOLOGY; NONHUMAN; PODOSPORA ANSERINA; PRION DISEASE; PROTEIN HOMEOSTASIS; PROTEIN STRUCTURE; RIBOSOME; STOP CODON; YEAST; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY; PRION; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

MAMMALIA;

EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, FUNGAL; PRIONS; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EID: 84893742865     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/1567-1364.12116     Document Type: Article

References (103)

1. 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.
2. Balch WE, Morimoto RI, Dillin A & Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319: 916-919.
3. Ball AJ, Wong DK & Elliott JJ (1976) Glucosamine resistance in yeast. I. A preliminary genetic analysis. Genetics 84: 311-317.
4. Barnhart MM & Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60: 131-147.
5. +] Prion transmission barriers protect Saccharomyces cerevisiae from infection: intraspecies 'species barriers'. Genetics 190: 569-579.
6. +] prions. Mol Microbiol 51: 1649-1659.
7. Brown JC & Lindquist S (2009) A heritable switch in carbon source utilization driven by an unusual yeast prion. Genes Dev 23: 2320-2332.
8. Bruce M, Chree A, McConnell I, Foster J, Pearson G & Fraser H (1994) Transmission of bovine spongiform encephalopathy and scrapie to mice: strain variation and the species barrier. Philos Trans R Soc Lond B Biol Sci 343: 405-411.
9. +]. Science 268: 880-884.
10. Chiti F & Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
11. Clavaguera F, Bolmont T, Crowther RA et al. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11: 909-913.
12. Collins SR, Douglass A, Vale RD & Weissman JS (2004) Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol 2: e321.
13. 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.
14. Cox B (1965) [Psi], A cytoplasmic suppressor of super-suppressor in yeast. Heredity 20: 505-521.
15. 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.
16. 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.
17. +] prion in Saccharomyces cerevisiae. Genetics 147: 507-519.
18. +]. Cell 106: 171-182.
19. Dobson CM (1999) Protein misfolding, evolution and disease. Trends Biochem Sci 24: 329-332.
20. Doyle SM & Wickner S (2009) Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 34: 40-48.
21. 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.
22. Dueholm MS, Petersen SV, Sønderkær M et al. (2010) Functional amyloid in Pseudomonas. Mol Microbiol 77: 1009-1020.
23. 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.
24. Espinosa Angarica V, Ventura S & Sancho J (2013) Discovering putative prion sequences in complete proteomes using probabilistic representations of Q/N-rich domains. BMC Genomics 1: 4.
25. Fiumara F, Fioriti L, Kandel ER & Hendrickson WA (2010) Essential role of coiled coils for aggregation and activity of Q/N-rich prions and PolyQ proteins. Cell 143: 1121-1135.
26. 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.
27. Gebbink MF, Claessen D, Bouma B, Dijkhuizen L & Wosten HA (2005) Amyloids - a functional coat for microorganisms. Nat Rev Microbiol 3: 333-341.
28. +], a heritable prion-like factor of S. cerevisiae. Cell 89: 811-819.
29. Greenwald J & Riek R (2010) Biology of amyloid: structure, function, and regulation. Structure 18: 1244-1260.
30. Griffith JS (1967) Self-replication and scrapie. Nature 215: 1043-1044.
31. +], even with realistic rates of yeast sex. PLoS Genet 5: e1000517.
32. Guo JL, Covell DJ, Daniels JP et al. (2013) Distinct alpha-synuclein strains differentially promote tau inclusions in neurons. Cell 154: 103-117.
33. Halfmann R., Lindquist S (2008) Screening for amyloid aggregation by semi-denaturing detergent-agarose gel electrophoresis. J Vis Exp doi:10.3791/838.
34. Halfmann R & Lindquist S (2010) Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330: 629-632.
35. Halfmann R, Alberti S & Lindquist S (2010) Prions, protein homeostasis, and phenotypic diversity. Trends Cell Biol 20: 125-133.
36. Halfmann R, Alberti S, Krishnan R et al. (2011) Opposing effects of glutamine and asparagine govern prion formation by intrinsically disordered proteins. Mol Cell 43: 72-84.
37. Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK & Lindquist S (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482: 363-368.
38. Hardy J & Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356.
39. Holmes DL, Lancaster AK, Lindquist S & Halfmann R (2013) Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153: 153-165.
40. Hou F, Sun L, Zheng H, Skaug B, Jiang QX & Chen ZJ (2011) MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146: 448-461.
41. Jarosz DF & Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330: 1820-1824.
42. Jucker M & Walker LC (2013) Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501: 45-51.
43. Kato M, Han TW, Xie S et al. (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149: 753-767.
44. Keleman K, Kruttner S, Alenius M & Dickson BJ (2007) Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 10: 1587-1593.
45. Kelly AC, Shewmaker FP, Kryndushkin D & Wickner RB (2012) Sex, prions, and plasmids in yeast. P Natl Acad Sci USA 109: E2683-E2690.
46. +] variants. J Mol Biol 307: 1247-1260.
47. King CY & Diaz-Avalos R (2004) Protein-only transmission of three yeast prion strains. Nature 428: 319-323.
48. King CY, Tittmann P, Gross H, Gebert R, Aebi M & Wuthrich K (1997) Prion-inducing domain 2-114 of yeast Sup35 protein transforms in vitro into amyloid-like filaments. P Natl Acad Sci USA 94: 6618-6622.
49. Krishnan R & Lindquist SL (2005) Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435: 765-772.
50. Krishnan R, Goodman JL, Mukhopadhyay S, Pacheco CD, Lemke EA, Deniz AA & Lindquist S (2012) Conserved features of intermediates in amyloid assembly determine their benign or toxic states. P Natl Acad Sci USA 109: 11172-11177.
51. Lacroute F (1971) Non-Mendelian mutation allowing ureidosuccinic acid uptake in yeast. J Bacteriol 106: 519-522.
52. +] system. Genetics 184: 393-400.
53. Lang GI & Murray AW (2008) Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae. Genetics 178: 67-82.
54. Li JY, Englund E, Holton JL et al. (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14: 501-503.
55. 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.
56. Liu B, Larsson L, Franssens V et al. (2011) Segregation of protein aggregates involves actin and the polarity machinery. Cell 147: 959-961.
57. Lopez-Otin C, Blasco MA, Partridge L, Serrano M & Kroemer G (2013) The hallmarks of aging. Cell 153: 1194-1217.
58. 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.
59. +] Prion. Mol Cell 50: 675-685.
60. Mayer MP & Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62: 670-684.
61. +] is a lethal yeast prion. P Natl Acad Sci USA 108: 5337-5341.
62. +] are diseases. P Natl Acad Sci USA 102: 10575-10580.
63. +] prion. Cell 106: 183-194.
64. 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.
65. +] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J 15: 3127-3134.
66. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP & Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307: 262-265.
67. Prusiner SB (1982) Novel proteinaceous infectious particles cause scrapie. Science 216: 136-144.
68. Prusiner SB (2012) Cell biology. A unifying role for prions in neurodegenerative diseases. Science 336: 1511-1513.
69. Ridley RM, Baker HF, Windle CP & Cummings RM (2006) Very long term studies of the seeding of beta-amyloidosis in primates. J Neural Transm 113: 1243-1251.
70. +] in yeast is a nuclear-residing prion form of the global transcriptional regulator Sfp1. P Natl Acad Sci USA 107: 10573-10577.
71. Rujano MA, Bosveld F, Salomons FA et al. (2006) Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol 4: e417.
72. +]: a novel non-Mendelian nonsense suppressor determinant in Saccharomyces cerevisiae. Curr Genet 56: 467-478.
73. Sanchez Y, Taulien J, Borkovich KA & Lindquist S (1992) Hsp104 is required for tolerance to many forms of stress. EMBO J 11: 2357-2364.
74. Santoso A, Chien P, Osherovich LZ & Weissman JS (2000) Molecular basis of a yeast prion species barrier. Cell 100: 277-288.
75. Scott M, Foster D, Mirenda C et al. (1989) Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59: 847-857.
76. Serio TR, Cashikar AG, Kowal AS et al. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289: 1317-1321.
77. Sharma D & Masison DC (2009) Hsp70 structure, function, regulation and influence on yeast prions. Protein Pept Lett 16: 571-581.
78. Shorter J & Lindquist S (2004) Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers. Science 304: 1793-1797.
79. Shorter J & Lindquist S (2005) Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 6: 435-450.
80. Shorter J & Lindquist S (2006) Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities. Mol Cell 23: 425-438.
81. Shorter J & Lindquist S (2008) Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J 27: 2712-2724.
82. Si K, Lindquist S & Kandel ER (2003) A neuronal isoform of the Aplysia CPEB has prion-like properties. Cell 115: 879-891.
83. 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.
84. Sondheimer N & Lindquist S (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5: 163-172.
85. 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.
86. Taipale M, Jarosz DF & Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515-528.
87. 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.
88. Tanaka M, Chien P, Yonekura K & Weissman JS (2005) Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins. Cell 121: 49-62.
89. 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.
90. + chaperone Hsp104 is part of a network that links the actin cytoskeleton with the inheritance of damaged proteins. Mol Cell Biol 29: 3738-3745.
91. Tessier PM & Lindquist S (2007) Prion recognition elements govern nucleation, strain specificity and species barriers. Nature 447: 556-561.
92. Toyama BH, Kelly MJ, Gross JD & Weissman JS (2007) The structural basis of yeast prion strain variants. Nature 449: 233-237.
93. True HL & Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477-483.
94. True HL, Berlin I & Lindquist SL (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431: 184-187.
95. Tuite MF & Cox BS (2003) Propagation of yeast prions. Nat Rev Mol Cell Biol 4: 878-890.
96. Tyedmers J, Madariaga ML & Lindquist S (2008) Prion switching in response to environmental stress. PLoS Biol 6: e294.
97. Volkov KV, Aksenova AY, Soom MJ et al. (2002) Novel non-Mendelian determinant involved in the control of translation accuracy in Saccharomyces cerevisiae. Genetics 160: 25-36.
98. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R & Meier BH (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319: 1523-1526.
99. Wickner RB (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569.
100. Wickner RB, Edskes HK, Shewmaker F & Nakayashiki T (2007) Prions of fungi: inherited structures and biological roles. Nat Rev Microbiol 5: 611-618.
101. +] and [URE3] are molecular degenerative diseases. Prion 5: 258-262.
102. +] prion of Saccharomyces cerevisiae can be propagated by an Hsp104 orthologue from Candida albicans. Eukaryot Cell 5: 217-225.
103. 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.