Skip to main content
Log in

Adaptive stress response to menadione-induced oxidative stress in Saccharomyces cerevisiae KNU5377

  • Articles
  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

The molecular mechanisms involved in the ability of yeast cells to adapt and respond to oxidative stress are of great interest to the pharmaceutical, medical, food, and fermentation industries. In this study, we investigated the time-dependent, cellular redox homeostasis ability to adapt to menadione-induced oxidative stress, using biochemical and proteomic approaches in Saccharomyces cerevisiae KNU5377. Time-dependent cell viability was inversely proportional to endogenous amounts of ROS measured by a fluorescence assay with 2′,7′-dichlorofluorescin diacetate (DCFHDA), and was hypersensitive when cells were exposed to the compound for 60 min. Morphological changes, protein oxidation and lipid peroxidation were also observed. To overcome the unfavorable conditions due to the presence of menadione, yeast cells activated a variety of cell rescue proteins including antioxidant enzymes, molecular chaperones, energy-generating metabolic enzymes, and antioxidant molecules such as trehalose. Thus, these results show that menadione causes ROS generation and high accumulation of cellular ROS levels, which affects cell viability and cell morphology and there is a correlation between resistance to menadione and the high induction of cell rescue proteins after cells enter into this physiological state, which provides a clue about the complex and dynamic stress response in yeast cells.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alic, N., T. Felder, M.D. Temple, C. Gloeckner, V.J. Higgins, P. Briza, and I.W. Dawes. 2004. Genome-wide transcriptional responses to a lipid hydroperoxide: adaptation occurs without induction of oxidant defenses. Free Radic. Biol. Med. 37, 23–35.

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Peral, F.J., O. Zaragoza, Y. Pedreno, and J.C. Arguelles. 2002. Protective role of trehalose during severe oxidative stress caused by hydrogen peroxide and the adaptive oxidative stress response in Candida albicans. Microbiology 148, 2599–2606.

    PubMed  CAS  Google Scholar 

  • Aranda, A., A. Querol, and M. del Olmo. 2002. Correlation between acetaldehyde and ethanol resistance and expression of HSP genes in yeast strains isolated during the biological aging of sherry wines. Arch. Microbiol. 177, 304–312.

    Article  PubMed  CAS  Google Scholar 

  • Benaroudj, N., D.H. Lee, and A.L. Goldberg. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276, 24261–24267.

    Article  PubMed  CAS  Google Scholar 

  • Beriault, R., D. Chenier, R. Singh, J. Middaugh, R. Mailloux, and V. Appanna. 2005. Detection and purification of glucose 6-phos phate dehydrogenase, malic enzyme, and NADP-dependent isocitrate dehydrogenase by blue native polyacrylamide gel electrophoresis. Electrophoresis 26, 2892–2897.

    Article  PubMed  CAS  Google Scholar 

  • Brosnan, M.P., D. Donnelly, T.C. James, and U. Bond. 2000. The stress response is repressed during fermentation in brewery strains of yeast. J. Appl. Microbiol. 88, 746–755.

    Article  PubMed  CAS  Google Scholar 

  • Cabiscol, E., G. Belli, J. Tamarit, P. Echave, E. Herrero, and J. Ros. 2002. Mitochondrial Hsp60, resistance to oxidative stress, and the labile iron pool are closely connected in Saccharomyces cerevisiae. J. Biol. Chem. 277, 44531–44538.

    Article  PubMed  CAS  Google Scholar 

  • Carrasco, P., A. Querol, and M. del Olmo. 2001. Analysis of the stress resistance of commercial wine yeast strains. Arch. Microbiol. 175, 450–457.

    Article  PubMed  CAS  Google Scholar 

  • Cashikar, A.G., M. Duennwald, and S.L. Lindquist. 2005. A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J. Biol. Chem. 280, 23869–23875.

    Article  PubMed  CAS  Google Scholar 

  • Castro, F.A., R.S. Herdeiro, A.D. Panek, E.C. Eleutherio, and M.D. Pereira. 2007. Menadione stress in Saccharomyces cerevisiae strains deficient in the glutathione transferases. Biochim. Biophys. Acta. 1770, 213–220.

    PubMed  CAS  Google Scholar 

  • Costa, V. and P. Moradas-Ferreira. 2001. Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol. Aspects Med. 22, 217–246.

    Article  PubMed  CAS  Google Scholar 

  • Echave, P., J. Tamarit, E. Cabiscol, and J. Ros. 2003. Novel antioxidant role of alcohol dehydrogenase E from Escherichia coli. J. Biol. Chem. 278, 30193–30198.

    Article  PubMed  CAS  Google Scholar 

  • Estruch, F. 2000. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol. Rev. 24, 469–486.

    Article  PubMed  CAS  Google Scholar 

  • Fernandes, P.N., S.C. Mannarino, C.G. Silva, M.D. Pereira, A.D. Panek, and E.C. Eleutherio. 2007. Oxidative stress response in eukaryotes: effect of glutathione, superoxide dismutase and catalase on adaptation to peroxide and menadione stresses in Saccharomyces cerevisiae. Redox Rep. 12, 236–244.

    Article  PubMed  CAS  Google Scholar 

  • Francois, J. and J.L. Parrou. 2001. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25, 125–145.

    Article  PubMed  CAS  Google Scholar 

  • Fujita, K., R. Kawai, H. Iwahashi, and Y. Komatsu. 1998. Hsp104 responds to heat and oxidative stress with different intracellular localization in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 248, 542–547.

    Article  PubMed  CAS  Google Scholar 

  • Gasch, A.P., P.T. Spellman, C.M. Kao, O. Carmel-Harel, M.B. Eisen, G. Storz, D. Botstein, and P.O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241–4257.

    PubMed  CAS  Google Scholar 

  • Gibson, B.R., S.J. Lawrence, J.P. Leclaire, C.D. Powell, and K.A. Smart. 2007. Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol. Rev. 31, 535–569.

    Article  PubMed  CAS  Google Scholar 

  • Grabowska, D. and A. Chelstowska. 2003. The ALD6 gene product is indispensable for providing NADPH in yeast cells lacking glucose-6-phosphate dehydrogenase activity. J. Biol. Chem. 278, 13984–13988.

    Article  PubMed  CAS  Google Scholar 

  • Haslbeck, M., N. Braun, T. Stromer, B. Richter, N. Model, S. Weinkauf, and J. Buchner. 2004. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 23, 638–649.

    Article  PubMed  CAS  Google Scholar 

  • Herdeiro, R.S., M.D. Pereira, A.D. Panek, and E.C. Eleutherio. 2006. Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochim. Biophys. Acta 1760, 340–346.

    PubMed  CAS  Google Scholar 

  • Herrero, E., J. Ros, G. Belli, and E. Cabiscol. 2008. Redox control and oxidative stress in yeast cells. Biochim. Biophys. Acta. 1780, 1217–1235.

    PubMed  CAS  Google Scholar 

  • Horak, C.E. and M. Snyder. 2002. Global analysis of gene expression in yeast. Funct. Integr. Genomics 2, 171–180.

    Article  PubMed  CAS  Google Scholar 

  • Jamieson, D.J. 1998. Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14, 1511–1527.

    Article  PubMed  CAS  Google Scholar 

  • Jelinsky, S.A. and L.D. Samson. 1999. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Natl. Acad. Sci. USA 96, 1486–1491.

    Article  PubMed  CAS  Google Scholar 

  • Kim, I., H. Yun, and I. Jin. 2007a. Comparative proteomic analyses of the yeast Saccharomyces cerevisiae KNU5377 strain against menadione-induced oxidative stress. J. Microbiol. Biotechnol. 17, 207–217.

    PubMed  CAS  Google Scholar 

  • Kim, I.S., H.S. Yun, S.H. Kwak, and I.N. Jin. 2007b. The physiological role of CPR1 in Saccharomyces cerevisiae KNU5377 against menadione stress by proteomics. J. Microbiol. 45, 326–332.

    PubMed  CAS  Google Scholar 

  • Kim, I.S., H.S. Yun, I.S. Park, H.Y. Sohn, H. Iwahashi, and I.N. Jin. 2006. A knockout strain of CPR1 induced during fermentation of Saccharomyces cerevisiae KNU5377 is susceptible to various types of stress. J. Biosci. Bioeng. 102, 288–296.

    Article  PubMed  CAS  Google Scholar 

  • Le Moan, N., G. Clement, S. Le Maout, F. Tacnet, and M.B. Toledano. 2006. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J. Biol. Chem. 281, 10420–10430.

    Article  PubMed  Google Scholar 

  • Lopez-Mirabal, H.R. and J.R. Winther. 2008. Redox characteristics of the eukaryotic cytosol. Biochim. Biophys. Acta 1783, 629–640.

    Article  PubMed  CAS  Google Scholar 

  • Lushchak, V.I. and D.V. Gospodaryov. 2005. Catalases protect cellular proteins from oxidative modification in Saccharomyces cerevisiae. Cell Biol. Int. 29, 187–192.

    Article  PubMed  CAS  Google Scholar 

  • Machida, K., T. Tanaka, and M. Taniguchi. 1999. Depletion of glutathione as a cause of the promotive effects of polygodial, a sesquiterpene on the production of reactive oxygen species in Saccharomyces cerevisiae. J. Biosci. Bioeng. 88, 526–530.

    Article  PubMed  CAS  Google Scholar 

  • Moradas-Ferreira, P. and V. Costa. 2000. Adaptive response of the yeast Saccharomyces cerevisiae to reactive oxygen species: defences, damage and death. Redox Rep. 5, 277–285.

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Avino, J.P., R. Prasad, V.J. Miralles, R.M. Benito, and R. Serrano. 1999. A proposal for nomenclature of aldehyde dehydrogenases in Saccharomyces cerevisiae and characterization of the stress-inducible ALD2 and ALD3 genes. Yeast 15, 829–842.

    Article  PubMed  CAS  Google Scholar 

  • Parrou, J.L. and J. Francois. 1997. A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal. Biochem. 248, 186–188.

    Article  PubMed  CAS  Google Scholar 

  • Querol, A., M.T. Fernandez-Espinar, M. del Olmo, and E. Barrio. 2003. Adaptive evolution of wine yeast. Int. J. Food Microbiol. 86, 3–10.

    Article  PubMed  CAS  Google Scholar 

  • Reverter-Branchat, G., E. Cabiscol, J. Tamarit, and J. Ros. 2004. Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae: common targets and prevention by calorie restriction. J. Biol. Chem. 279, 31983–31989.

    Article  PubMed  CAS  Google Scholar 

  • San Miguel, P.F. and J.C. Arguelles. 1994. Differential changes in the activity of cytosolic and vacuolar trehalases along the growth cycle of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1200, 155–160.

    PubMed  CAS  Google Scholar 

  • Sirisattha, S., Y. Momose, E. Kitagawa, and H. Iwahashi. 2004. Toxicity of anionic detergents determined by Saccharomyces cerevisiae microarray analysis. Water Res. 38, 61–70.

    Article  PubMed  CAS  Google Scholar 

  • Thorpe, G.W., C.S. Fong, N. Alic, V.J. Higgins, and I.W. Dawes. 2004. Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc. Natl. Acad. Sci. USA 101, 6564–6569.

    Article  PubMed  CAS  Google Scholar 

  • Tucker, C.L. and S. Fields. 2004. Quantitative genome-wide analysis of yeast deletion strain sensitivities to oxidative and chemical stress. Comp. Funct. Genomics 5, 216–224.

    Article  PubMed  CAS  Google Scholar 

  • Voit, E.O. 2003. Biochemical and genomic regulation of the trehalose cycle in yeast: review of observations and canonical model analysis. J. Theor. Biol. 223, 55–78.

    Article  PubMed  CAS  Google Scholar 

  • Zadzinski, R., A. Fortuniak, T. Bilinski, M. Grey, and G. Bartosz. 1998. Menadione toxicity in Saccharomyces cerevisiae cells: activation by conjugation with glutathione. Biochem. Mol. Biol. Int. 44, 747–759.

    PubMed  CAS  Google Scholar 

  • Zuzuarregui, A. and M.L. del Olmo. 2004. Expression of stress response genes in wine strains with different fermentative behavior. FEMS Yeast Res. 4, 699–710.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Il-Sup Kim or Ingnyol Jin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, IS., Sohn, HY. & Jin, I. Adaptive stress response to menadione-induced oxidative stress in Saccharomyces cerevisiae KNU5377. J Microbiol. 49, 816–823 (2011). https://doi.org/10.1007/s12275-011-1154-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-011-1154-6

Keywords

Navigation