Advertisement

Biochemistry (Moscow)

, Volume 82, Issue 10, pp 1147–1157 | Cite as

Distinct mechanisms of phenotypic effects of inactivation and prionization of Swi1 protein in Saccharomyces cerevisiae

  • K. S. Antonets
  • S. F. Kliver
  • D. E. Polev
  • A. R. Shuvalova
  • E. A. Andreeva
  • S. G. Inge-Vechtomov
  • A. A. Nizhnikov
Article

Abstract

Prions are proteins that under the same conditions can exist in two or more conformations, and at least one of the conformations has infectious properties. The prionization of a protein is typically accompanied by its functional inactivation due to sequestration of monomers by the prion aggregates. The most of prions has been identified in the yeast Saccharomyces cerevisiae. One of them is [SWI +], a prion isoform of the Swi1 protein, which is a component of the evolutionarily conserved chromatin remodeling complex SWI/SNF. Earlier, it was shown that the prionization of [SWI +] induces a nonsense suppression, which leads to weak growth of the [SWI +] strains containing mutant variants of the SUP35 gene and the nonsense allele ade1-14 UGA on selective medium without adenine. This effect occurs because of [SWI +] induction that causes a decrease in the amount of the SUP45 mRNA. Strains carrying the SWI1 deletion exhibit significantly higher suppression of the ade1-14 UGA nonsense mutation than the [SWI +] strains. In the present study, we identified genes whose expression is altered in the background of the SWI1 deletion using RNA sequencing. We found that the ade1-14 UGA suppression in the swi1Δ strains is caused by an increase in the expression of this mutant allele of the ADE1 gene. At the same time, the SUP45 expression level in the swi1Δ strains does not significantly differ from the expression level of this gene in the [swi ] strains. Thus, we have shown that the phenotypic effects of Swi1 prionization and deletion are mediated by different molecular mechanisms. Based on these data, we have concluded that the prionization of proteins is not only unequal to their inactivation, but also can lead to the acquisition of novel phenotypic effects and functions.

Keywords

amyloid prion Swi1 Ade1 Sup45 yeast Saccharomyces cerevisiae 

Abbreviations

eRF

eukaryotic release factor

qPCR

real-time quantitative polymerase chain reaction

RNA-Seq

RNA sequencing

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Tang, L., Nogales, E., and Ciferri, C. (2010) Structure and function of SWI/SNF chromatin remodeling complexes and mechanistic implications for transcription, Prog. Biophys. Mol. Biol., 102, 122–128.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Dechassa, M. L., Zhang, B., Horowitz-Scherer, R., Persinger, J., Woodcock, C. L., Peterson, C. L., and Bartholomew, B. (2008) Architecture of the SWI/SNF–nucleosome complex, Mol. Cell Biol., 28, 6010–6021.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Neigeborn, L., and Carlson, M. (1984) Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae, Genetics, 108, 845–858.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Peterson, C. L., and Herskowitz, I. (1992) Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encodea global activator of transcription, Cell, 68, 573–583.CrossRefPubMedGoogle Scholar
  5. 5.
    Laurent, B. C., Yang, X., and Carlson, M. (1992) An essential Saccharomyces cerevisiae gene homologous to SNF2 encodes a helicase-related protein in a new family, Mol. Cell Biol., 12, 1893–1902.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Eisen, J. A., Sweder, K. S., and Hanawalt, P. C. (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions, Nucleic Acids Res., 23, 2715–2723.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Hargreaves, D. C., and Crabtree, G. R. (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms, Cell Res., 21, 396–420.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Prochasson, P., Neely, K. E., Hassan, A. H., Li, B., and Workman, J. L. (2003) Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains, Mol. Cell, 12, 983–990.CrossRefPubMedGoogle Scholar
  9. 9.
    Perez-Martin, J., and Johnson, A. D. (1998) The C-terminal domain of Sin1 interacts with the SWI–SNF complex in yeast, Mol. Cell Biol., 18, 4157–4164.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Breeden, L., and Nasmyth, K. (1987) Cell cycle control of the yeast HOgene: cis- and trans-acting regulators, Cell, 48, 389–397.CrossRefPubMedGoogle Scholar
  11. 11.
    Hirschhorn, J. N., Brown, S. A., Clark, C. D., and Winston, F. (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure, Genes Dev., 6, 2288–2298.CrossRefPubMedGoogle Scholar
  12. 12.
    Haber, J. E., and Garvik, B. (1977) A new gene affecting the efficiency of mating-type interconversions in homothallic strains of Saccharomyces cerevisiae, Genetics, 87, 33–50.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Taguchi, A. K., and Young, E. T. (1987) The cloning and mapping of ADR6, a gene required for sporulation and for expression of the alcohol dehydrogenase II isozyme from Saccharomyces cerevisiae, Genetics, 116, 531–540.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Du, Z., Park, K. K.-W., Yu, H., Fan, Q., and Li, L. (2008) Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae, Nat. Genet., 40, 460–465.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Alberti, S., Halfmann, R., King, O., Kapila, A., and Lindquist, S. (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins, Cell, 137, 146–158.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Nizhnikov, A. A., Antonets, K. S., Bondarev, S. A., Inge-Vechtomov, S. G., and Derkatch, I. L. (2016) Prions, amyloids, and RNA: pieces of a puzzle, Prion, 10, 182–206.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Wickner, R. B., Edskes, H. K., Shewmaker, F., Nakayashiki, T., Engel, A., McCann, L., and Kryndushkin, D. (2007) Yeast prions: evolution of the prion concept, Prion, 1, 94–100.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kondrashkina, A. M., Antonets, K. S., Galkin, A. P., and Nizhnikov, A. A. (2014) Prion-like determinant [NSI+] decreases expression of the SUP45 gene in Saccharomyces cerevisiae, Mol. Biol., 48, 688–693.CrossRefGoogle Scholar
  19. 19.
    Nizhnikov, A. A., Ryzhova, T. A., Volkov, K. V., Zadorsky, S. P., Sopova, J. V., Inge-Vechtomov, S. G., and Galkin, A. P. (2016) Interaction of prions causes heritable traits in Saccharomyces cerevisiae, PLoS Genet., 12, e1006504.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zhouravleva, G., Frolova, L., Le Goff, X., Le Guellec, R., Inge-Vechtomov, S., Kisselev, L., and 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.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Stansfield, I., Jones, K. M., Ter-Avanesyan, M. D., and Tuite, M. F. (1995) The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae, EMBO J., 14, 4365–4373.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Saifitdinova, A. F., Nizhnikov, A. A., Lada, A. G., Rubel, A. A., Magomedova, Z. M., Ignatova, V. V., Inge-Vechtomov, S. G., and Galkin, A. P. (2010) [NSI+]: a novel non-Mendelian nonsense suppressor determinant in Saccharomyces cerevisiae, Curr. Genet., 56, 467–478.CrossRefPubMedGoogle Scholar
  23. 23.
    Nizhnikov, A. A., Magomedova, Z. M., Rubel, A. A., Kondrashkina, A. M., Inge-Vechtomov, S. G., and 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
  24. 24.
    Nizhnikov, A. A., Antonets, K. S., Inge-Vechtomov, S. G., and Derkatch, I. L. (2014) Modulation of efficiency of translation termination in Saccharomyces cerevisiae, Prion, 8, 247–260.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Kaiser, C., Michaelis, S., and Mitchell, A. (1994) Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual, Cold Spring Harbor Laboratory Press.Google Scholar
  26. 26.
    Zakharov, I. A., Kozhin, S. A., Kozhina, T. N., and Fedorova, I. V. (1984) Collected Methods in Genetics of the Yeast Saccharomyces [in Russian], Nauka, Leningrad.Google Scholar
  27. 27.
    Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method, Methods, 25, 402–408.CrossRefPubMedGoogle Scholar
  28. 28.
    Starostina, E., Tamazian, G., Dobrynin, P., O’Brien, S., and Komissarov, A. (2015) Cookiecutter: a tool for kmer-based read filtering and extraction, BioRxiv, 024679.Google Scholar
  29. 29.
    Bolger, A. M., Lohse, M., and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114–2120.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., and Gingeras, T. R. (2013) STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15–21.CrossRefPubMedGoogle Scholar
  31. 31.
    Anders, S., Pyl, P. T., and Huber, W. (2015) HTSeq-A Python framework to work with high-throughput sequencing data, Bioinformatics, 31, 166–169.CrossRefPubMedGoogle Scholar
  32. 32.
    Love, M. I., Huber, W., and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Kolde, R. (2012) Package “pheatmap”, Bioconductor, 1–6.Google Scholar
  34. 34.
    Stern, M., Jensen, R., and Herskowitz, I. (1984) Five SWI genes are required for expression of the HO gene in yeast, J. Mol. Biol., 178, 853–868.CrossRefPubMedGoogle Scholar
  35. 35.
    Krings, G., and Bastia, D. (2004) swi1- and swi3-dependent and independent replication fork arrest at the ribosomal DNA of Schizosaccharomyces pombe, Proc. Natl. Acad. Sci. USA, 101, 14085–14090.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Sanz, A. B., Garcia, R., Rodriguez-Pena, J. M., Diez-Muniz, S., Nombela, C., Peterson, C. L., and Arroyo, J. (2012) Chromatin remodeling by the SWI/SNF complex is essential for transcription mediated by the yeast cell wall integrity MAPK pathway, Mol. Biol. Cell, 23, 2805–2817.CrossRefPubMedGoogle Scholar
  37. 37.
    Adkins, M. W., Williams, S. K., Linger, J., and Tyler, J. K. (2007) Chromatin disassembly from the PHO5 promoter is essential for the recruitment of the general transcription machinery and coactivators, Mol. Cell Biol., 27, 6372–6382.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Erkina, T. Y., Tschetter, P. A., and Erkine, A. M. (2008) Different requirements of the SWI/SNF complex for robust nucleosome displacement at promoters of heat shock factor and Msn2- and Msn4-regulated heat shock genes, Mol. Cell Biol., 28, 1207–1217.CrossRefPubMedGoogle Scholar
  39. 39.
    Shivaswamy, S., and Iyer, V. R. (2008) Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWI/SNF in the heat shock stress response, Mol. Cell. Biol., 28, 2221–2234.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Tkach, J. M., Yimit, A., Lee, A. Y., Riffle, M., Costanzo, M., Jaschob, D., Hendry, J. A., Ou, J., Moffat, J., Boone, C., Davis, T. N., Nislow, C., and Brown, G. W. (2012) Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress, Nat. Cell Biol., 14, 966–976.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Wickner, R. B., Masison, D. C., and Edskes, H. K. (1995) [PSI] and [URE3] as yeast prions, Yeast, 11, 1671–1685.CrossRefPubMedGoogle Scholar
  42. 42.
    Nizhnikov, A. A., Kondrashkina, A. M., and Galkin, A. P. (2013) Interactions of [NSI+] determinant with SUP35 and VTS1 genes in Saccharomyces cerevisiae, Rus. J. Genet., 49, 1004–1012.CrossRefGoogle Scholar
  43. 43.
    Derkatch, I. L., Bradley, M. E., Hong, J. Y., and Liebman, S. W. (2001) Prions affect the appearance of other prions: the story of [PIN+], Cell, 106, 171–182.CrossRefPubMedGoogle Scholar
  44. 44.
    Orlowska-Matuszewska, G., and Wawrzycka, D. (2006) A novel phenotype of eight spores asci in deletants of the prion-like Rnq1p in Saccharomyces cerevisiae, Biochem. Biophys. Res. Commun., 340, 190–193.CrossRefPubMedGoogle Scholar
  45. 45.
    Strawn, L. A., and True, H. L. (2006) Deletion of RNQ1 gene reveals novel functional relationship between divergently transcribed Bik1p/CLIP-170 and Sfi1p in spindle pole body separation, Curr. Genet., 50, 347–366.CrossRefPubMedGoogle Scholar
  46. 46.
    Arslan, F., Hong, J. Y., Kanneganti, V., Park, S. K., and Liebman, S. W. (2015) Heterologous aggregates promote de novo prion appearance via more than one mechanism, PLoS Genet., 11, e1004814.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Du, Z., Zhang, Y., and Li, L. (2015) The yeast prion [SWI +] abolishes multicellular growth by triggering conformational changes of multiple regulators required for flocculin gene expression, Cell Rep., 13, 2865–2878.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • K. S. Antonets
    • 1
    • 2
    • 3
  • S. F. Kliver
    • 1
    • 3
  • D. E. Polev
    • 1
  • A. R. Shuvalova
    • 1
  • E. A. Andreeva
    • 1
    • 2
  • S. G. Inge-Vechtomov
    • 1
    • 2
  • A. A. Nizhnikov
    • 1
    • 2
    • 3
  1. 1.St. Petersburg State UniversitySt. PetersburgRussia
  2. 2.St. Petersburg Branch of Vavilov Institute of General GeneticsRussian Academy of SciencesSt. PetersburgRussia
  3. 3.All-Russian Research Institute for Agricultural MicrobiologyPushkin, St. PetersburgRussia

Personalised recommendations