Skip to main content
SpringerLink
Log in

Candida glabrata Rpn4-like Protein Complements the RPN4 Deletion in Saccharomyces cerevisiae

  • GENOMICS. TRANSCRIPTOMICS
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Expression of Saccharomyces cerevisiae proteasomal genes is regulated in a coordinated manner by a system that includes the ScRpn4 transcription factor and its binding site known as PACE. Earlier we showed that, Rpn4-like proteins from the biotechnologically important yeast species Komagataellapfaffii (Pichiapastoris), Yarrowia lipolytica, and Debaryomyces hansenii are capable of complementing the RPN4 deletion in S. cerevisiae in spite of their low structural similarity to ScRpn4. The opportunistic yeast pathogen Candida glabrata has a gene coding for a Rpn4-like protein, which has not been characterized experimentally yet. The C. glabrata ortholog ScRpn4 was expressed heterologously and found to restore the stress resistance and expression of proteasomal genes in a mutant S. cerevisiae strain with a RPN4 deletion. This complementation required the unique N-terminal region of CgRpn4. The results indicate that CgRpn4 acts as a transcriptional activator of proteasomal genes. The S. cerevisiae model can be used for further structural and functional analyses of CgRpn4.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Gabaldon T., Carrete L. 2016. The birth of a deadly yeast: tracing the evolutionary emergence of virulence traits in Candida glabrata. FEMS Yeast Res. 16, fov110.

    Article  CAS  PubMed  Google Scholar 

  2. Mannhaupt G., Feldmann H. 2007. Genomic evolution of the proteasome system among hemiascomycetous yeasts. J. Mol. Evol. 65, 529–540.

    Article  CAS  PubMed  Google Scholar 

  3. Vermitsky J.-P., Earhart K.D., Smith W.L., Homayouni R., Edlind T.D., Rogers P.D. 2006. Pdr1 regulates multidrug resistance in Candida glabrata: Gene disruption and genome-wide expression studies. Mol. Microbiol. 61, 704–722.

    Article  CAS  PubMed  Google Scholar 

  4. Owsianik G., Balzil L., Ghislain M. 2002. Control of 26S proteasome expression by transcription factors regulating multidrug resistance in Saccharomyces cerevisiae. Mol. Microbiol. 43, 1295–1308.

    Article  CAS  PubMed  Google Scholar 

  5. Kapranov A.B., Kuryatova MV., Preobrazhenskaya O.V., Tutyaeva V.V., Stucka R., Feldmann H., Karpov V.L. 2001. Isolation and identification of PACE-binding protein Rpn4, a new transcriptional activator regulating 26S-proteasomal and other genes. Mol. Biol. (Moscow). 35 (3), 356–364.

    Article  CAS  Google Scholar 

  6. Mannhaupt G., Schnall R., Karpov V., Vetter I., Feldmann H. 1999. Rpn4 acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett. 450, 27–34.

    Article  CAS  PubMed  Google Scholar 

  7. Spasskaya D.S., Karpov D.S., Mironov A.S., Karpov V.L. 2014. Transcription factor Rpn4 promotes a complex antistress response in Saccharomyces cerevisiae cells exposed to methyl methanesulfonate. Mol. Biol. (Moscow). 48 (1), 141–149.

    Article  CAS  Google Scholar 

  8. Grineva E.N., Leinsoo A.T., Spsskaya D.S., Karpov D.S., Karpov V.L. 2014. Functional analysis of Rpn4-like proteins from Komagataella (Pichia) pastoris and Yarrowia lipolytica in a heterologous Saccharomyces cerevisiae system. Biotekhnologiya. 6, 8–17.

    Google Scholar 

  9. Karpov D.S., Grineva E.N., Leinsoo A.T., Nadolinskaia N.I., Danilenko N.K., Tutyaeva V.V., Spasskaya D.S., Preobrazhenskaya O.V., Lysov Y.P., Karpov V.L. 2017. Functional analysis of Debaryomyces hansenii Rpn4 on a genetic background of Saccharomyces cerevisiae. FEMS Yeast Res. 17, fow098.

    Google Scholar 

  10. Enjalbert B., Smith D.A., Cornell M.J., Alam I., Nicholls S., Brown A.J.P., Quinn J. 2006. Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol. Biol. Cell. 17, 1018‒1032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gietz R.D., Woods R.A. 2002. Transformation of yeast by the LiAc/ss carrier DNA/PEG method. Methods Enzymol. 350, 87–96.

    Article  CAS  PubMed  Google Scholar 

  12. Schwarzmuller T., Ma B., Hiller E., Istel F., Tscherner M., Brunke S., Ames L., Firon A., Green B., Cabral V., Marcet-Houben M., Jacobsen I.D., Quintin J., Seider K., Frohner I., et al. 2014. Systematic phenotyping of a large-scale Candida glabrata deletion collection reveals novel antifungal tolerance genes. PLoS Pathog. 10, e1004211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Amberg D.C., Burke D.J., Strathern J.N. 2006. Isolation of yeast genomic DNA for southern blot analysis. CSH Protoc. 2006.

    Google Scholar 

  14. Karpov D.S., Spasskaya D.S., Tutyaeva V.V., Mironov A.S., Karpov V.L. 2013. Proteasome inhibition enhances resistance to DNA damage via upregulation of Rpn4-dependent DNA repair genes. FEBS Lett. 587, 3108–3114.

    Article  CAS  PubMed  Google Scholar 

  15. Spasskaya D.S., Karpov D.S., Karpov V.L. 2011. Escherichia coli Dam-methylase as a molecular tool for mapping binding sites of the yeast transcription factor Rpn4. Mol. Biol. (Moscow). 45 (4), 591–599.

    Article  CAS  Google Scholar 

  16. Schmitt M.E., Brown T.A., Trumpower B.L. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18, 3091–3092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406–3415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ha S.W., Ju D., Xie Y. 2012. The N-terminal domain of Rpn4 serves as a portable ubiquitin-independent degron and is recognized by specific 19S RP subunits. Biochem. Biophys. Res. Commun. 419, 226–231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Karpov D.S., Tutyaeva V.V., Karpov V.L. 2008. Mapping of yeast Rpn4p transactivation domains. FEBS Lett. 582, 3459–3464.

    Article  CAS  PubMed  Google Scholar 

  20. McWilliam H., Li W., Uludag M., Squizzato S., Park Y.M., Buso N., Cowley A.P., Lopez R. 2013. Analysis tool web services from the EMBL-EBI. Nucleic Acids Res. 41, W597–W600.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Persikov A., Singh M. 2014. De novo prediction of DNA-binding specificities for Cys2His2 zinc finger proteins. Nucleic Acids Res. 42, 97–108.

    Article  CAS  PubMed  Google Scholar 

  22. Wolfe S.A., Nekludova L., Pabo C.O. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29, 183–212.

    Article  CAS  PubMed  Google Scholar 

  23. Dreier B., Segal D.J., Barbas C.F. 2000. Insights into the molecular recognition of the 5′-GNN-3′ family of DNA sequences by zinc finger domains. J. Mol. Biol. 303, 489– 502.

    Article  CAS  PubMed  Google Scholar 

  24. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. 2004. WebLogo: A sequence logo generator. Genome Res. 14, 1188–1190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Brennan R.J., Schiestl R.H. 1996. Cadmium is an inducer of oxidative stress in yeast. Mutat. Res. 356, 171–178.

    Article  PubMed  Google Scholar 

  26. Haugen A.C., Kelley R., Collins J.B., Tucker C.J., Deng C., Afshari C.A., Brown J.M., Ideker T., Van Houten B. 2004. Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol. 5, R95.

    Article  PubMed  PubMed Central  Google Scholar 

  27. London M.K., Keck B.I., Ramos P.C., R. Dohmen R.J. 2004. Regulatory mechanisms controlling biogenesis of ubiquitin and the proteasome. FEBS Lett. 567, 259–264.

    Article  CAS  PubMed  Google Scholar 

  28. Lee J., Godon C., Lagniel G., Spector D., Garin J., Labarre J., Toledano M.B. 1999. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274, 16040–16046.

    Article  CAS  PubMed  Google Scholar 

  29. Mitchell P.J., Tjian R. 1989. Transcriptional regulation in mammalian cells by sequence specific DNA binding proteins. Science. 245, 371–378.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    D. S. Karpov, E. N. Grineva, S. V. Kiseleva, E. S. Chelarskaya, D. S. Spasskaya & V. L. Karpov

  2. Orekhovich Institute of Biomedical Chemistry, 119121, Moscow, Russia

    D. S. Karpov

Authors
  1. D. S. Karpov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. N. Grineva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. V. Kiseleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. S. Chelarskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. S. Spasskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. L. Karpov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. S. Karpov.

Additional information

Translated by T. Tkacheva

Abbreviations: PACE, proteasome-associated control element; MMS, methyl methane sulfonate; 4-NQO, 4-nitroquinoline-1-oxide; NAD, N-terminal acidic domain; CAD, C-terminal acidic domain; NTAD, N-terminal transactivation domain; N-ZnF, N-terminal zinc finger domain; C-ZnF, C-terminal zinc finger domain; QRR, glutamine-rich region.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karpov, D.S., Grineva, E.N., Kiseleva, S.V. et al. Candida glabrata Rpn4-like Protein Complements the RPN4 Deletion in Saccharomyces cerevisiae. Mol Biol 53, 242–248 (2019). https://doi.org/10.1134/S0026893319020067

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893319020067

Keywords:

Search

Navigation