Skip to main content
Log in

Investigation of the Relationship Between Oxidative Stress and Glucose Signaling in Schizosaccharomyces pombe

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

The invertase mutant defective in the glucose signaling pathway of Schizosaccharomyces pombe (ird11) is resistant to glucose repression. This mutant is able to consume sucrose alongside glucose and grows in glucose-containing media with a generation time close to that of the wild type. Intracellular oxidation, protein carbonyl, and reduced glutathione levels and catalase, superoxide dismutase, and glutathione peroxidase activity were investigated in ird11, to determine the relationship between oxidative stress response and glucose signaling. The expression profiles of some genes involved in regulation of glucose repression (fbp1, fructose-1,6-bis-phosphatase; hxk2, hexokinase) and stress response (atf1 and pap1 transcription factors; ctt1, catalase; sod1, Cu,Zn superoxide dismutase) were analyzed using the quantitative real-time PCR technique. Oxidative stress response in ird11 seems to be affected by glucose signaling in a manner different from that caused by glucose deprivation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen DA, Yaqoob MM, Harwood SM (2005) Mechanisms of high glucose-induced apoptosis and its relationship to diabetic complications. J Nutr Biochem 16(12):705–713

    Article  PubMed  CAS  Google Scholar 

  • Beutler E (1975) Red cell metabolism. In: A manual of biochemical methods. 2d ed. Grune and Stratton, New York

  • Carlson M (1999) Glucose repression in yeast. Curr Opin Microbiol 2(2):202–207

    Article  PubMed  CAS  Google Scholar 

  • Ceriello A, Russo P, Amstad P, Cerutti P (1996) High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 45(4):471–477

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Vaghchhipawala Z, Li W, Asard H, Dickman MB (2004) Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 135:1630–1641

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Wilkinson CRM, Watt S, Penkett CJ, Toone WM, Jones N, Bahler J (2008) Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol Biol Cell 19:308–317

    Article  PubMed  CAS  Google Scholar 

  • Cho WY, Park HE, Lim JC (2000) Catalase, glutathione S-transferase and thioltransferase respond differently to oxidative stress in Schizosaccharomyces pombe. J Biochem Mol Biol 33(4):344–348

    CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta 329:23–38

    Article  CAS  Google Scholar 

  • Fagan JM, Sleczka BG, Sohar I (1999) Quantification of oxidative damage to tissue proteins. Int J Biochem Cell Biol 31:751–757

    Article  PubMed  CAS  Google Scholar 

  • Flores CL, Rodriguez C, Petit T, Gancedo C (2000) Carbohydrate and energy-yielding metabolism in non-conventional yeast. FEMS Microbiol 24:507–529

    CAS  Google Scholar 

  • Forsburg S, Rhind N (2006) Basic methods for fission yeast. Yeast 23(3):173

    Article  PubMed  CAS  Google Scholar 

  • Giannopolitis N, Ries SK (1977) Super oxide dismutase, I: occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Gutz H, Heslot H, Leupold U, Loprieno N (1974) Schizosaccharomyces pombe. In: King RC (ed) Handbook of genetics. Plenum Press, New York, pp 395–446

    Google Scholar 

  • Hoffman CS (2005) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Transac 33:257–260

    Article  CAS  Google Scholar 

  • Hoffman CS, Winston F (1989) A transcriptionally regulated expression vector for the fission yeast, Schizosaccharomyces pombe. Gene 84:473–479

    Article  PubMed  CAS  Google Scholar 

  • Hoffman CS, Winston F (1990) Isolation and characterization of mutants constitutive for expression of the fbp1 gene of Schizosaccharomyces pombe. Genetics 124:807–816

    PubMed  CAS  Google Scholar 

  • Hoffman CS, Winston F (1991) Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. Genes Dev 5:561–571

    Article  PubMed  CAS  Google Scholar 

  • Ikner A, Shiozaki K (2005) Yeast signaling pathways in the oxidative stress response. Mutat Res 6(569):13–27

    Google Scholar 

  • Inai Y, Nishikimi M (2002) Increased degradation of oxidized proteins in yeast defective in 26S proteasome assembly. Arch Biochem Biophys 404:279–284

    Article  PubMed  CAS  Google Scholar 

  • Jamieson DJ (1992) Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione. J Bacteriol 174:6678–6681

    PubMed  CAS  Google Scholar 

  • Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511–1527

    Article  PubMed  CAS  Google Scholar 

  • Janoo RTK, Neely LA, Braun BR, Whitehall SK, Hoffman CS (2001) Transcriptional regulators of the Schizosaccharomyces pombe fbp1 gene include two redundant Tup1p-like corepressors and the CCAAT binding factor activation complex. Genetics 157:1205–1215

    PubMed  CAS  Google Scholar 

  • Johnston M (1999) Feasting, fasting and fermenting glucose sensing in yeast and other cell. Trends Genet 15(1):29–33

    Article  PubMed  CAS  Google Scholar 

  • Kanoh J, Watanabe Y, Ohsugi M, Iino Y, Yamamoto M (1996) Schizosaccharomyces pombe gad7+ encodes a phosphoprotein with a bZIP domain, which is required for proper G1 arrest and gene expression under nitrogen starvation. Genes to Cells 1:391–408

    Article  PubMed  CAS  Google Scholar 

  • Karaer S, Tarhan C, Pekmez M, Hamad I, Arda N, Topal Sarıkaya A (2010) Expression of human A4V mutant Cu,Zn superoxide dismutase in Schizosaccharomyces pombe: investigations of its toxic properties. Biochem Genet 48:113–124

    Article  PubMed  CAS  Google Scholar 

  • Kig C, Turkel S, Temizkan G (2005) Isolation and characterization of glucose derepressed invertase mutants from Schizosaccharomyces pombe. Biosci Biotechnol Biochem 69(12):2475–2478

    Article  PubMed  CAS  Google Scholar 

  • Kim SJ, Cho NC, Ryu IW, Kim K, Park EH, Lim CJ (2006) Carbone source-dependent regulation of the Schizosaccharomyces pombe pbh1 gene. J Microbiol 44(6):689–693

    PubMed  CAS  Google Scholar 

  • Lin SJ, Defossez PA, Guarente L (2000) Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289(5487):2126–2128

    Article  PubMed  CAS  Google Scholar 

  • Lin S-J, Kaeberlein M, Andalis AA, Sturtz LA, Defossez P-A, Culotta VC, Fink GR, Guarente L (2002) Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418:344–348

    Article  PubMed  CAS  Google Scholar 

  • Madrid M, Soto T, Franco A, Paredes V, Vicente J, Hidalgo E, Gacto M, Cansado J (2004) A cooperative role for Atf1 and Pap1 in the detoxification of the oxidative stress induced by glucose deprivation in Schizosaccharomyces pombe. J Biol Chem 279(40):41594–41602

    Article  PubMed  CAS  Google Scholar 

  • Mutoh N, Nakagawa CW, Yamada K (2002) Characterization of Cu, Zn-superoxide dismutase-deficient mutant of fission yeast Schizosaccharomyces pombe. Curr Genet 41:82–88

    Article  PubMed  CAS  Google Scholar 

  • Neely L, Hoffman CS (2000) Protein kinase A and mitogen-activated protein kinase pathways antagonistically regulate fission yeast fbp1 transcription by employing different modes of action at two upstream activation sites. Mol Cell Biol 20(17):6426–6434

    Article  PubMed  CAS  Google Scholar 

  • Okai Y, Okai HK, Machida K, Nakamura H, Nakayama K, Fujita K, Tanaka T, Otani S, Taniguchi M (2000) Protective effect of antioxidants against para-nonylphenol-induced inhibition of cell growth in Saccharomyces cerevisiae. FEMS Microbiol Lett 185:65–70

    Article  PubMed  CAS  Google Scholar 

  • Petit T, Blázquez MA, Gancedo C (1996) Schizosaccharomyces pombe possesses an unusual and a conventional hexokinase: biochemical and molecular characterization of both hexokinases. FEBS Lett 378(2):185–189

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45

    Article  PubMed  CAS  Google Scholar 

  • Picke E, Keisari Y (1980) A simple colorimetric method for the measurement of hydrogen peroxide produced by cells in culture. J Immunol Methods 38:161

    Article  Google Scholar 

  • Quinn J, Findlay VJ, Dawson K, Millar JBA, Jones N, Morgan BA, Toone M (2002) Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 3:805–816

    Article  Google Scholar 

  • Reinheckel T, Grune T, Davies KJ (2000) Stress response: methods and protocols. Ch 5 in: methods in molecular biology: the measurement of protein degradation in response to oxidative stress. Humana Press, Totowa, NJ

    Google Scholar 

  • Rincon AM, Codon AC, Castrejon F, Benitez T (2001) Improved properties of baker’s yeast mutants resistant to 2-deoxy-d-glucose. Appl Environ Microbiol 67(9):4279–4285

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Winderick J, Thevelein JM (2001) Glucose-sensing mechanisms in eukaryotic cells. Trends Biochem Sci 26(5):310–317

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Winderick J, Thevelein JM (2002) Glucose-sensing and signaling mechanisms in yeast. FEMS Yeast Res 2:183–201

    PubMed  CAS  Google Scholar 

  • Roux AE, Leroux A, Alaamery MA, Hoffman CS, Chartrand P, Ferbeyre G, Rokeach LA (2009) Pro-aging effects of glucose signalling through a G protein-coupled glucose receptor in fission yeast. PLoS Genetics 5(3):e1000408

    Article  PubMed  Google Scholar 

  • Roux AE, Arseneault G, Chartrand P, Ferbeyre G, Rokeach L (2010) A screen for genes involved in respiration control and longevity in Schizosaccharomyces pombe. Ann N Y Acad Sci 1197:19–27

    Article  PubMed  CAS  Google Scholar 

  • Schmidt MW, Houseman A, Ivanov AR, Wolf DA (2007) Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe. Mol Sys Biol 3(79):1–12

    Google Scholar 

  • Stettler S, Warbrick E, Prochnik S, Mackie S, Fantes P (1996) The wis1 signal transduction pathway is required for expression of cAMP-repressed genes in fission yeast. J Cell Science 109:1927–1935

    PubMed  CAS  Google Scholar 

  • Stiefel J, Wang L, Kelly DA, Janoo RTK, Seitz J, Whitehall SK, Hoffman CS (2004) Suppressors of an adenylate cyclase deletion in the fission yeast Schizosaccharomyces pombe. Eukaryotic Cell 3(3):610–619

    Article  PubMed  CAS  Google Scholar 

  • Toone WM, Kuge S, Samuels M, Morgan BA, Toda T, Jones N (1998) Regulation of the fission yeast transcription factor Pap1 by oxidative stress: requirement for the nuclear export factor Crm1 (exportin) and the stress-activated MAP kinaseSty1/Spc1. Genes Dev 12(10):1453–1463

    Article  PubMed  CAS  Google Scholar 

  • Toone WM, Morgan BA, Jones N (2001) Redox control of AP-1-like factors in yeast and beyond. Oncogene 20:2336–2346

    Article  PubMed  CAS  Google Scholar 

  • Vassarotti A, Friesen JD (1985) Isolation of the fructose-1, 6-bisphosphatase gene of the yeast Schizosaccharomyces pombe: evidence for transcriptional regulation. J Biol Chem 260:6348–6353

    PubMed  CAS  Google Scholar 

  • Waterborg JH (2002) The Lowry method for proteins quantitation. In: Walker JM (ed) The protein protocols handbook. Humana Press, Totowa, NJ, pp 7–9

    Chapter  Google Scholar 

Download references

Acknowledgments

This research was supported by Istanbul University Research Fund, Projects BAP1477 and UDP-4218.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bedia Palabiyik.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Palabiyik, B., Kig, C., Pekmez, M. et al. Investigation of the Relationship Between Oxidative Stress and Glucose Signaling in Schizosaccharomyces pombe . Biochem Genet 50, 336–349 (2012). https://doi.org/10.1007/s10528-011-9477-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-011-9477-x

Keywords

Navigation