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Recent advances of research on the [PSI+] prion in Saccharomyces cerevisiae

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Mycoscience

Abstract

Prion diseases such as bovine spongiform encephalopathy or Creutzfeldt-Jakob disease have been extensively studied in recent years. Research in this field is being done in highly secured laboratories because of potential transmission of prions to humans. Emerging similarities between mammalian and yeast prions allow using yeast-based assays to examine the activity of anti-prion drugs. Besides the intensively studied clinical aspects of prion diseases, the evolutionary aspects of prion proteins present in the yeast Saccharomyces cerevisiae are also extensively investigated. One of the key feature of prions, the ability to be stable in two alternative conformations, seems to play an important role in the evolution of this fungi, although some authors point out the negative influence of these particles upon yeast physiology. In this review, the most intensively studied fields of the research carried out on [PSI+] prion in yeast are summarized.

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References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bach S, Talarek N, Andrieu T, Vierfond JM, Mettey Y, Galons H, Dormont D, Meijer L, Cullin C, Blondel M (2003) Isolation of drugs active against mammalian prions using a yeast-based screening assay. Nat Biotechnol 21:1075–1081

    Article  PubMed  CAS  Google Scholar 

  • Bailey CH, Kandel ER, Si K (2004) The persistence of long-term memory; a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 44:49–57

    Article  PubMed  CAS  Google Scholar 

  • Benkemoun L, Saupe SJ (2006) Prion proteins as genetic material in fungi. Fungal Genet Biol 43:789–803

    Article  PubMed  CAS  Google Scholar 

  • Bösl B, Grimminger V, Walter S (2006) The molecular chaperone Hsp104: a molecular machine for protein disaggregation. J Struct Biol 156:139–148

    PubMed  Google Scholar 

  • Callahan MA, Xiong L, Caughey B (2001) Reversibility of scrapie-associated prion protein aggregation. J Biol Chem 276:28022–28028

    Article  PubMed  CAS  Google Scholar 

  • Chen B, Newnam GP, Chernoff YO (2007) Prion species barrier between the closely related yeast proteins is detected despite coaggregation. Proc Natl Acad Sci U S A 104:2791–2796

    Article  PubMed  CAS  Google Scholar 

  • Chernoff YO (2007) Stress and prions: lessons from the yeast model. FEBS Lett 581:3695–3701

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cox B (1965) [PSI], a cytoplasmic suppressor of super-suppression in yeast. Heredity 20:505–521

    Article  Google Scholar 

  • Cox B, Tuite MF, McLaughlin CS (1988) The psi factor of yeast: a problem in inheritance. Yeast 4:159–178

    Article  PubMed  CAS  Google Scholar 

  • Crist CG, Nakamura Y (2006) Cross-talk between RNA and prions. J Biochem (Tokyo) 140:167–173

    CAS  Google Scholar 

  • DePace AH, Santoso A, Hillner P, Weissman JS (1998) A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93:1241–1252

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Derkatch IL, Bradley ME, Zhou P, Chernoff YO, Liebman SW (1997) Genetic and environmental factors affecting the de novo appearance f the [PSI+] prion in Saccharomyces cerevisiae. Genetics 147: 507–519

    PubMed  CAS  Google Scholar 

  • Doel SM, McCready SJ, Nierras CR, Cox BS (1994) The dominant PNM2 − mutation which eliminates the Φ factor of Saccharomyces cerevisiae is the result of a missense mutation in the SUP35 gene. Genetics 137:659–670

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hara H, Nakayashiki T, Crist CG, Nakamura Y (2003) Prion domain interaction responsible for species discrimination in yeast [PSI+] transmission. Genes Cells 8:925–939

    Article  PubMed  CAS  Google Scholar 

  • Harrison LB, Yu Z, Stajich JE, Dietrich FS, Harrison PM (2007) Evolution of budding yeast prion-determinant sequences across diverse fungi. J Mol Biol 368:273–282

    Article  PubMed  CAS  Google Scholar 

  • Kochneva-Pervukhova NV, Paushkin SV, Kushnirov VV, Cox BS, Tuite MF, Ter-Avanesyan MD (1998) Mechanism of inhibition of Psi+ prion determinant propagation by a mutation of the N-terminus of the yeast Sup35 protein. EMBO J 17:5805–5810

    Article  PubMed  CAS  Google Scholar 

  • Korth C, May B, Cohen FE, Prusiner SB (2001) Acridine and phenothiazine deriverates as pharmacotherapeutics for prion disease. Proc Natl Acad Sci U S A 98:9836–9841

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kushnirov VV, Ter-Avanesyan MD, Surguchov AP, Smirnov VN, Inge-Vechtomov SG (1987) Localization of possible functional domains in sup2 gene product of the yeast Saccharomyces cerevisiae. FEBS Lett 215:257–260

    Article  PubMed  CAS  Google Scholar 

  • Kushnirov VV, Ter-Avanesyan MD, Telckov MV, Surguchov AP, Smirnov VN, Inge-Vechtomov SG (1988) Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae. Gene (Amst) 66:45–54

    CAS  Google Scholar 

  • Kushnirov VV, Kochneva-Pervukhova NV, Chechenova MB, Frolova NS, Ter-Avanesian MD (2000) Prion properties of the Sup35 protein of yeast Pichia methanolica. EMBO J 19:324–331

    Article  PubMed  CAS  Google Scholar 

  • Li L, Lindquist S (2000) Creating a protein-based element of inheritance. Science 287:661–664

    Article  PubMed  CAS  Google Scholar 

  • Liu JJ, Lindquist S (1999) Oligopeptide-repeat expansions modulate “protein-only” inheritance in yeast. Nature (Lond) 400:573–576

    Article  CAS  Google Scholar 

  • Moriyama H, Edskes HK, Wickner RB (2000) [URE3] prion propagation in Saccharomyces cerevisiae: requirement for chaperone Hsp104 and curing by overexpressed chaperone Ydj1p. Mol Cell Biol 20:8916–8922

    Article  PubMed  CAS  Google Scholar 

  • Nakayashiki T, Ebihara K, Bannai H, Nakamura Y (2001) Yeast [PSI+] “prions” that are crosstransmissible and susceptible beyond a species barrier through a quasi-prion state. Mol Cell 7:1121–1130

    Article  PubMed  CAS  Google Scholar 

  • Nakayashiki T, Kurtzman CP, Edskes HK, Wickner RB (2005) Yeast prions [URE3] and [PSI+] are diseases. Proc Natl Acad Sci U S A 102:10575–10580

    Article  PubMed  CAS  Google Scholar 

  • Nishida N, Harris DA, Vilette D, Laude H, Frobert Y, Grassi J, Casanova D, Milhavet O, Lehmann S (2000) Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein. J Virol 74: 320–325

    Article  PubMed  CAS  Google Scholar 

  • Osherovich LZ, Cox BS, Tuite MF, Weissman JS (2004) Dissection and design of yeast prions. PLoS Biol 2:442–451

    Article  Google Scholar 

  • Papassotiropoulos A, Wollmer MA, Aguzzi A, Hock C, Nitsch RM, de Quervain DJ (2005) The prion gene is associated with human long-term memory. Hum Mol Genet 14:2241–2246

    Article  PubMed  CAS  Google Scholar 

  • Parsell DA, Kowal AS, Singer MA, Lindquist S (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature (Lond) 372:475–478

    Article  CAS  Google Scholar 

  • Patino MM, Liu JJ, Glover JR, Lindquist S (1996) Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273:622–626

    Article  PubMed  CAS  Google Scholar 

  • Prusiner SB (1982) Novel proteinaceous infectious particles cause scrapie. Science 216:136–144

    Article  PubMed  CAS  Google Scholar 

  • Prusiner SB (1994) Biology and genetics of prion diseases. Annu Rev Microbiol 48:655–686

    Article  PubMed  CAS  Google Scholar 

  • Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95: 13363–13383

    Article  PubMed  CAS  Google Scholar 

  • Resende CG, Outeiro TF, Sands L, Lindquist S, Tuite MF (2003) Prion protein gene polymorphisms in Saccharomyces cerevisiae. Mol Microbiol 49:1005–1017

    Article  PubMed  CAS  Google Scholar 

  • Santoso A, Chien P, Osherovich LZ, Weissman JS (2000) Molecular basis of a yeast prion species barrier. Cell 100:277–288

    Article  PubMed  CAS  Google Scholar 

  • Serio TR, Lindquist SL (1999) [PSI+]: an epigenetic modulator of translation termination efficiency. Annu Rev Cell Dev Biol 15:661–703

    Article  PubMed  CAS  Google Scholar 

  • Serio TR, Lindquist SL (2000) Protein-only inheritance in yeast: something to get [PSI+]-ched about. Trends Cell Biol 10:98–105

    Article  PubMed  CAS  Google Scholar 

  • Shewmaker F, Wickner RB (2006) Ageing in yeast does not enhance prion generation. Yeast 23:1123–1128

    Article  PubMed  CAS  Google Scholar 

  • Shkundina IS, Kushnirov VV, Tuite MF, Ter-Avanesyan MD (2006) The role of the N-terminal oligopeptide repeats of the yeast Sup35 prion protein in propagation and transmission of prion variants. Genetics 172:827–835

    Article  PubMed  CAS  Google Scholar 

  • Sondheimer N, Lindquist S (2000) Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 5:163–172

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ter-Avanesyan MD, Kushnirov VV, Dagkesamanskaya AR, Didichenko SA, Chernoff YO, Inge-Vechtomov SG, Smirnov VN (1993) Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol Microbiol 7:683–692

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Tessier PM, Lindquist S (2007) Prion recognition elements govern nucleation, strain specificity and species barriers. Nature (Lond) 447:556–561

    Article  CAS  Google Scholar 

  • Tribouillard D, Bach S, Gug F, Desban N, Beringue V, Andrieu T, Dormont D, Galons H, Laude H, Vilette D, Blondel M (2006) Using budding yeast to screen for anti-prion drugs. Biotechnol J 1:58–67

    Article  PubMed  CAS  Google Scholar 

  • True HL (2006) The battle of the fold: chaperones take on prions. Trends Genet 22:110–117

    Article  PubMed  CAS  Google Scholar 

  • True HL, Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature (Lond) 407:477–483

    Article  CAS  Google Scholar 

  • True HL, Berlin I, Lindquist SL (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature (Lond) 431:184–187

    Article  CAS  Google Scholar 

  • Tuite MF, Mundy CR, Cox BS (1981) Agents that cause a high frequency of genetic change from [psi+] to [psi−] in Saccharomyces cerevisiae. Genetics 98:691–711

    PubMed  CAS  Google Scholar 

  • Tuite MF, Lund PM, Futcher AB, Dobson MJ, Cox BS, McLaughlin CS (1982) Relationship of the [psi] factor with other plasmids of Saccharomyces cerevisiae. Plasmid 8:103–111

    Article  PubMed  CAS  Google Scholar 

  • Uptain SM, Lindquist S (2002) Prions as protein-based genetic elements. Annu Rev Microbiol 56:703–741

    Article  PubMed  CAS  Google Scholar 

  • Vilette D, Andreoletti O, Archer F, Madelaine MF, Vilotte JL, Lehmann S, Laude H (2001) Ex vivo propagation of infectious sheep scrapie agent in heterologous epithelial cells expressing ovine prion protein. Proc Natl Acad Sci U S A 98:4055–4059

    Article  PubMed  CAS  Google Scholar 

  • von der Haar T, Jossé L, Wright P, Zenthon J, Tuite MF (2007) Development of a novel yeast cell-based system for studying the aggregation of Alzheimer’s disease-associated A beta peptides in vivo. Neurodegener Dis 4:136–147

    Article  PubMed  CAS  Google Scholar 

  • von der Haar T, Tuite MF (2007) Regulated translational bypass of stop codons in yeast. Trends Microbiol 15:78–86

    Article  PubMed  CAS  Google Scholar 

  • Wechselberger C, Wurm S, Pfarr W, Höglinger O (2002) The physiological functions of prion protein. Exp Cell Res 281:1–8

    Article  PubMed  CAS  Google Scholar 

  • Wickner RB (1994) [URE3] as an altered Ure2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264:566–569

    Article  PubMed  CAS  Google Scholar 

  • Young CS, Cox BS (1971) Extrachromosomal elements in a super-suppression system of yeast. I. A nuclear gene controlling the inheritance of the extrachromosomal elements. Heredity 26:413–522

    Article  Google Scholar 

  • Young CS, Cox BS (1972) Extrachromosomal elements in a supersuppression system of yeast. II. Relations with other extrachromosomal elements. Heredity 28:189–199

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Molecular Biology, Institute of Biochemistry, Faculty of Biology, University of Warsaw, 1 Miecznikowa St., PL-02-096, Warsaw, Poland

    Takao Ishikawa

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  1. Takao Ishikawa
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Correspondence to Takao Ishikawa.

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Ishikawa, T. Recent advances of research on the [PSI+] prion in Saccharomyces cerevisiae . Mycoscience 49, 221–228 (2008). https://doi.org/10.1007/s10267-008-0413-9

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  • DOI: https://doi.org/10.1007/s10267-008-0413-9

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