• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of embojLink to Publisher's site
EMBO J. Apr 1, 1999; 18(7): 1974–1981.
PMCID: PMC1171282

Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism.

Abstract

[PSI+] is a protein-based heritable phenotype of the yeast Saccharomyces cerevisiae which reflects the prion-like behaviour of the endogenous Sup35p protein release factor. [PSI+] strains exhibit a marked decrease in translation termination efficiency, which permits decoding of translation termination signals and, presumably, the production of abnormally extended polypeptides. We have examined whether the [PSI+]-induced expression of such an altered proteome might confer some selective growth advantage over [psi-] strains. Although otherwise isogenic [PSI+] and [psi-] strains show no difference in growth rates under normal laboratory conditions, we demonstrate that [PSI+] strains do exhibit enhanced tolerance to heat and chemical stress, compared with [psi-] strains. Moreover, we also show that the prion-like determinant [PSI+] is able to regulate translation termination efficiency in response to environmental stress, since growth in the presence of ethanol results in a transient increase in the efficiency of translation termination and a loss of the [PSI+] phenotype. We present a model to describe the prion-mediated regulation of translation termination efficiency and discuss its implications in relation to the potential physiological role of prions in S.cerevisiae and other fungi.

Full Text

The Full Text of this article is available as a PDF (266K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Basu J, Williams BC, Li Z, Williams EV, Goldberg ML. Depletion of a Drosophila homolog of yeast Sup35p disrupts spindle assembly, chromosome segregation, and cytokinesis during male meiosis. Cell Motil Cytoskeleton. 1998;39(4):286–302. [PubMed]
  • Bonetti B, Fu L, Moon J, Bedwell DM. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol. 1995 Aug 18;251(3):334–345. [PubMed]
  • Chernoff YO, Derkach IL, Inge-Vechtomov SG. Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr Genet. 1993 Sep;24(3):268–270. [PubMed]
  • Chernoff YO, Lindquist SL, Ono B, Inge-Vechtomov SG, Liebman SW. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science. 1995 May 12;268(5212):880–884. [PubMed]
  • Coustou V, Deleu C, Saupe S, Begueret J. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9773–9778. [PMC free article] [PubMed]
  • Cox B. Cytoplasmic inheritance. Prion-like factors in yeast. Curr Biol. 1994 Aug 1;4(8):744–748. [PubMed]
  • Cox BS, Tuite MF, McLaughlin CS. The psi factor of yeast: a problem in inheritance. Yeast. 1988 Sep;4(3):159–178. [PubMed]
  • Bearn AG. Archibald Edward Garrod, the reluctant geneticist. Genetics. 1994 May;137(1):1–4. [PMC free article] [PubMed]
  • Fearon K, McClendon V, Bonetti B, Bedwell DM. Premature translation termination mutations are efficiently suppressed in a highly conserved region of yeast Ste6p, a member of the ATP-binding cassette (ABC) transporter family. J Biol Chem. 1994 Jul 8;269(27):17802–17808. [PubMed]
  • Firoozan M, Grant CM, Duarte JA, Tuite MF. Quantitation of readthrough of termination codons in yeast using a novel gene fusion assay. Yeast. 1991 Feb;7(2):173–183. [PubMed]
  • Fischer M, Rülicke T, Raeber A, Sailer A, Moser M, Oesch B, Brandner S, Aguzzi A, Weissmann C. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 1996 Mar 15;15(6):1255–1264. [PMC free article] [PubMed]
  • Grant CM, Firoozan M, Tuite MF. Mistranslation induces the heat-shock response in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1989 Feb;3(2):215–220. [PubMed]
  • Griffith JS. Self-replication and scrapie. Nature. 1967 Sep 2;215(5105):1043–1044. [PubMed]
  • Horwich AL, Weissman JS. Deadly conformations--protein misfolding in prion disease. Cell. 1997 May 16;89(4):499–510. [PubMed]
  • Kikuchi Y, Shimatake H, Kikuchi A. A yeast gene required for the G1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. EMBO J. 1988 Apr;7(4):1175–1182. [PMC free article] [PubMed]
  • Kushnirov VV, Ter-Avanesyan MD, Telckov MV, Surguchov AP, Smirnov VN, Inge-Vechtomov SG. Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae. Gene. 1988 Jun 15;66(1):45–54. [PubMed]
  • Lindquist S. Mad cows meet psi-chotic yeast: the expansion of the prion hypothesis. Cell. 1997 May 16;89(4):495–498. [PubMed]
  • Lindquist S, Kim G. Heat-shock protein 104 expression is sufficient for thermotolerance in yeast. Proc Natl Acad Sci U S A. 1996 May 28;93(11):5301–5306. [PMC free article] [PubMed]
  • Liu H, Styles CA, Fink GR. Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics. 1996 Nov;144(3):967–978. [PMC free article] [PubMed]
  • Mager WH, Ferreira PM. Stress response of yeast. Biochem J. 1993 Feb 15;290(Pt 1):1–13. [PMC free article] [PubMed]
  • Oesch B, Westaway D, Wälchli M, McKinley MP, Kent SB, Aebersold R, Barry RA, Tempst P, Teplow DB, Hood LE, et al. A cellular gene encodes scrapie PrP 27-30 protein. Cell. 1985 Apr;40(4):735–746. [PubMed]
  • Patino MM, Liu JJ, Glover JR, Lindquist S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science. 1996 Aug 2;273(5275):622–626. [PubMed]
  • Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 1996 Jun 17;15(12):3127–3134. [PMC free article] [PubMed]
  • Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: implications for prion-dependent regulation. Mol Cell Biol. 1997 May;17(5):2798–2805. [PMC free article] [PubMed]
  • Piper PW. The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol Lett. 1995 Dec 15;134(2-3):121–127. [PubMed]
  • Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science. 1982 Apr 9;216(4542):136–144. [PubMed]
  • Sanchez Y, Lindquist SL. HSP104 required for induced thermotolerance. Science. 1990 Jun 1;248(4959):1112–1115. [PubMed]
  • Sanchez Y, Taulien J, Borkovich KA, Lindquist S. Hsp104 is required for tolerance to many forms of stress. EMBO J. 1992 Jun;11(6):2357–2364. [PMC free article] [PubMed]
  • Santos MA, Perreau VM, Tuite MF. Transfer RNA structural change is a key element in the reassignment of the CUG codon in Candida albicans. EMBO J. 1996 Sep 16;15(18):5060–5068. [PMC free article] [PubMed]
  • Stansfield I, Jones KM, Kushnirov VV, Dagkesamanskaya AR, Poznyakovski AI, Paushkin SV, Nierras CR, Cox BS, Ter-Avanesyan MD, Tuite MF. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 1995 Sep 1;14(17):4365–4373. [PMC free article] [PubMed]
  • Stansfield I, Akhmaloka, Tuite MF. A mutant allele of the SUP45 (SAL4) gene of Saccharomyces cerevisiae shows temperature-dependent allosuppressor and omnipotent suppressor phenotypes. Curr Genet. 1995 Apr;27(5):417–426. [PubMed]
  • Ter-Avanesyan MD, Kushnirov VV, Dagkesamanskaya AR, Didichenko SA, Chernoff YO, Inge-Vechtomov SG, Smirnov VN. Deletion analysis of the SUP35 gene of the yeast Saccharomyces cerevisiae reveals two non-overlapping functional regions in the encoded protein. Mol Microbiol. 1993 Mar;7(5):683–692. [PubMed]
  • Ter-Avanesyan MD, Dagkesamanskaya AR, Kushnirov VV, Smirnov VN. The SUP35 omnipotent suppressor gene is involved in the maintenance of the non-Mendelian determinant [psi+] in the yeast Saccharomyces cerevisiae. Genetics. 1994 Jul;137(3):671–676. [PMC free article] [PubMed]
  • Tuite MF, Lindquist SL. Maintenance and inheritance of yeast prions. Trends Genet. 1996 Nov;12(11):467–471. [PubMed]
  • Tuite MF, Mundy CR, Cox BS. Agents that cause a high frequency of genetic change from [psi+] to [psi-] in Saccharomyces cerevisiae. Genetics. 1981 Aug;98(4):691–711. [PMC free article] [PubMed]
  • Tuite MF, Bentley NJ, Bossier P, Fitch IT. The structure and function of small heat shock proteins: analysis of the Saccharomyces cerevisiae Hsp26 protein. Antonie Van Leeuwenhoek. 1990 Oct;58(3):147–154. [PubMed]
  • Weissmann C. The Ninth Datta Lecture. Molecular biology of transmissible spongiform encephalopathies. FEBS Lett. 1996 Jun 24;389(1):3–11. [PubMed]
  • Wickner RB, Masison DC. Evidence for two prions in yeast: [URE3] and [PSI]. Curr Top Microbiol Immunol. 1996;207:147–160. [PubMed]
  • Zhouravleva G, Frolova L, Le Goff X, Le Guellec R, Inge-Vechtomov S, Kisselev L, Philippe M. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 1995 Aug 15;14(16):4065–4072. [PMC free article] [PubMed]

Articles from The EMBO Journal are provided here courtesy of The European Molecular Biology Organization

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...