Molecular Biology

, Volume 48, Issue 5, pp 688–693 | Cite as

Prion-like determinant [NSI +] decreases the expression of the SUP45 gene in Saccharomyces cerevisiae

  • A. M. Kondrashkina
  • K. S. Antonets
  • A. P. Galkin
  • A. A. Nizhnikov
Cell Molecular Biology

Abstract

Previously, we described and characterized the yeast nonchromosomal determinant [NSI +], which possesses prion properties. This determinant causes a decrease in fidelity of translation termination, which is phenotypically detectable as the nonsense suppression in the strains with decreased functional activity of eRF3 release factor. As a result of the genetic screen, we demonstrated that an increase in the expression of SUP45 that encodes the eRF1 release factor (Sup45), masks, but does not eliminate nonsense suppression in the [NSI +] strains. In the present study, we first demonstrated the direct cause for the nonsense suppression in [NSI +] strains. We demonstrated that [NSI +] decreases the relative amounts of SUP45 mRNA, which causes a decrease in the amounts of Sup45 protein that can be detected in the stationary growth phase. The data obtained suggest the structural protein of [NSI +] seems to be either a transcription factor or participates in the regulation of cellular mRNA stability.

Keywords

yeast translation termination prion nonsense suppression SUP45 [NSI+

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Wickner R.B. 1994. [URE3] as an altered URE2 protein: Evidence for a prion analog in Saccharomyces cerevisiae. Science. 264, 566–569.CrossRefPubMedGoogle Scholar
  2. 2.
    Derkatch I.L., Bradley M.E., Hong J.Y., Liebman S.W. 2001. Prions affect the appearance of other prions: The story of [PIN]. Cell. 106, 171–182.CrossRefPubMedGoogle Scholar
  3. 3.
    Derkatch I.L., Bradley M.E., Zhou P., Chernoff Y.O., Liebman S.W. 1997. Genetic and environmental factors affecting the de novo appearance of the [PSI +] prion in Saccharomyces cerevisiae. Genetics. 147, 507–519.PubMedCentralPubMedGoogle Scholar
  4. 4.
    Du Z., Park K.W., Yu H., Fan Q., Li L. 2008. Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nature Genet. 40, 460–465.CrossRefPubMedCentralPubMedGoogle Scholar
  5. 5.
    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.CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    Patel B.K., Liebman S.W. 2007. “Prion-proof” for [PIN +]: Infection with in vitro-made amyloid aggregates of Rnq1p-(132–405) induces [PIN+]. J. Mol. Biol. 365, 773–782.CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Rogoza T., Goginashvili A., Rodionova S., Ivanov M., Viktorovskaya O., Rubel A., Volkov K., Mironova L. 2010. Non-Mendelian determinant [ISP +] in yeast is a nuclear-residing prion form of the global transcriptional regulator Sfp1. Proc. Natl. Acad. Sci. U. S. A. 107, 10573–10577.CrossRefPubMedCentralPubMedGoogle Scholar
  8. 8.
    Halfmann R., Wright J.R., Alberti S., Lindquist S., Rexach M. 2012. Prion formation by a yeast GLFG nucleoporin. Prion. 6, 391–399.CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    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.CrossRefPubMedGoogle Scholar
  10. 10.
    Osherovich L.Z., Weissman J.S. 2001. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI +] prion. Cell. 106, 183–194.CrossRefPubMedGoogle Scholar
  11. 11.
    Roberts B.T., Wickner R.B. 2003. Heritable activity: A prion that propagates by covalent autoactivation. Genes Dev. 17, 2083–2087.CrossRefPubMedCentralPubMedGoogle Scholar
  12. 12.
    Brown J.C., Lindquist S. 2009. A heritable switch in carbon source utilization driven by an unusual yeast prion. Genes Dev. 23, 2320–2332.CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Yang W., Yang H., Tien P. 2006. In vitro self-propagation of recombinant PrPSc-like conformation generated in the yeast cytoplasm. FEBS Lett. 580, 4231–4235.CrossRefPubMedGoogle Scholar
  14. 14.
    Serio T.R., Cashikar A.G., Kowal A., Sawicki G.J., Moslehi J.J., Serpell L., Arnsdorf M.F., Lindquist S.L. 2000. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science. 289, 1317–1321.CrossRefPubMedGoogle Scholar
  15. 15.
    Saifitdinova A.F., Nizhnikov A.A., Lada A.G., Rubel A.A., Magomedova Z.M., Ignatova V.V., Inge-Vechtomov S.G., Galkin A.P. 2010. [NSI +]: A novel non-Mendelian suppressor determinant in Saccharomyces cerevisiae. Curr. Genet. 56, 467–478.CrossRefPubMedGoogle Scholar
  16. 16.
    Nizhnikov A.A., Magomedova Z.M., Rubel A.A., Kondrashkina A.M., Inge-Vechtomov S.G., Galkin A.P. 2012. [NSI +] determinant has a pleiotropic phenotypic manifestation that is modulated by SUP35, SUP45, and VTS1 genes. Curr. Genet. 58, 35–47.CrossRefPubMedGoogle Scholar
  17. 17.
    Zhouravleva G., Frolova L., Le Goff X., Le Guellec R., Inge-Vechtomov S., Kisselev L., Philippe M.1995. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 14, 4065–4072.PubMedCentralPubMedGoogle Scholar
  18. 18.
    Kaiser C., Michaelis S., Mitchell A. 1994. Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press.Google Scholar
  19. 19.
    Hanahan D. 1985. DNA Cloning: A Practical Approach. IRL Press.Google Scholar
  20. 20.
    Sambrook J., Fritsch E.F., Maniatis T. 1989. Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press.Google Scholar
  21. 21.
    Zakharov I.A., Kozhin S.A., Kozhina T.N., Fedorova I.V. 1984. Sbornik metodik po genetike drozhzhei-sakharomitsetov (Methods in Saccharomyces Yeast Genetics), Leningrad: Nauka.Google Scholar
  22. 22.
    Sherman F., Fink G.R., Hancks J.B. 1986. Methods in Yeast Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press.Google Scholar
  23. 23.
    Livak K., Schmittgen T. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods. 25, 402–408.CrossRefPubMedGoogle Scholar
  24. 24.
    Newnam G.P., Wegrzyn R.D., Lindquist S.L., Chernoff Y.O. 1999. Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol. Cell. Biol. 19, 1325–1333.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Bradford M.M. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.CrossRefPubMedGoogle Scholar
  26. 26.
    Kiktev D., Moskalenko S., Murina O., Baudin-Baillieu A., Rousset J.P., Zhouravleva G. 2009. The paradox of viable sup45 STOP mutations: A necessary equilibrium between translational readthrough, activity and stability of the protein. Mol. Genet. Genom. 282, 83–96.CrossRefGoogle Scholar
  27. 27.
    Inge-Vechtomov S.G. 1964. Back mutations to prototrophism in adenine-dependent yeasts. Vestn. Leningr. Gos. Univ. 9, 112–117.Google Scholar
  28. 28.
    Ivanov M.S., Radchenko E.A., Mironova L.N. 2010. The protein complex Ppz1p/Hal3p and nonsense suppression efficiency in the yeast Saccharomyces cerevisiae. Mol. Biol. (Moscow). 44, 907–914.CrossRefGoogle Scholar
  29. 29.
    Nizhnikov A.A., Kondrashkina A.M., Antonets K.S., Galkin A.P. 2014. Overexpression of genes encoding asparagine-glutamine-rich transcriptional factors causes nonsense suppression in Saccharomyces cerevisiae. Russian Journal of Genetics: Applied Research. 4, 122–130.CrossRefGoogle Scholar
  30. 30.
    Nizhnikov A.A., Magomedova Z.M., Saifitdinova A.F., Inge-Vechtomov S.G., Galkin A.P. 2012. Identification of genes encoding potentially amyloidogenic proteins that take part in the regulation of nonsense suppression in yeast Saccharomyces cerevisiae. Russ. J. Genet.: Applied Res. 2, 399–405.Google Scholar
  31. 31.
    Nizhnikov A.A., Magomedova Z.M., Saifitdinova A.F., Inge-Vechtomov S.G., Galkin A.P. 2011. Identification of genes encoding potentially amyloidogenic proteins involved in regulation of nonsense suppression in yeast Saccharomyces cerevisiae. Ekol. Genet. 9, 79–86.Google Scholar
  32. 32.
    Cox B.S. 1965. Psi, a cytoplasmic supperssor of supersuppressors in yeast. Heredity. 20, 505–521.CrossRefGoogle Scholar
  33. 33.
    Radchenko E., Rogoza T., Khokhrina M., Drozdova P., Mironova L. 2011. SUP35 expression is enhanced in yeast containing [ISP +], a prion form of the transcriptional regulator Sfp1. Prion. 5, 317–322.CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    Nizhnikov A.A., Kondrashkina A.M., Galkin A.P. 2013. Interactions of [NSI +] prion-like determinant with SUP35 and VTS1 genes in Saccharomyces cerevisiae. Russ. J. Genet. 49, 1004–1012.CrossRefGoogle Scholar
  35. 35.
    Ono B., Yoshida R., Kamiya K., Sugimoto T. 2005. Suppression of termination mutations caused by defects of the NMD machinery in Saccharomyces cerevisiae. Genes Genet. Syst. 80, 311–316.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2014

Authors and Affiliations

  • A. M. Kondrashkina
    • 1
  • K. S. Antonets
    • 1
  • A. P. Galkin
    • 1
    • 2
  • A. A. Nizhnikov
    • 1
    • 2
  1. 1.Department of Genetics and BiotechnologySt. Petersburg State UniversitySt. PetersburgRussia
  2. 2.St. Petersburg Branch Vavilov Institute of General GeneticsRussian Academy of ScienceSt. PetersburgRussia

Personalised recommendations