Skip to main content
SpringerLink
Log in

NADH-reductive stress in Saccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1)

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

A strain of Saccharomyces cerevisiae lacking the GPD2 gene, encoding one of the glycerol-3-phosphate dehydrogenases, grows slowly under anaerobic conditions, due to reductive stress caused by the accumulation of cytoplasmic NADH. We used 2D-PAGE to study the effect on global protein expression of reductive stress in the anaerobically grown gpd2Δ strain. The most striking response was a strongly elevated expression of Tdh1p, the minor isoform of glyceraldehyde-3-phosphate dehydrogenase. This increased expression could be reversed by the addition of acetoin, a NADH-specific redox sink, which furthermore largely restored anaerobic growth of the gpd2Δ strain. Additional deletion of the TDH1 gene (but not of TDH2 or TDH3) improved anaerobic growth of the gpd2Δ strain. We therefore propose that TDH1 has properties not displayed by the other TDH isogenes and that its expression is regulated by reductive stress caused by an excess of cytoplasmic NADH.

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. 2A, B
Fig. 3

Similar content being viewed by others

References

  • Akhtar N, Blomberg A, Adler L (1997) Osmoregulation and protein expression in a pbs2delta mutant of Saccharomyces cerevisiae during adaptation to hypersaline stress. FEBS Lett 403:173–180

    Article  CAS  PubMed  Google Scholar 

  • Albers E, Liden G, Larsson C, Gustafsson L (1998) Anaerobic redox balance and nitrogen metabolism in Saccharomyces cerevisiae. Rec Dev Microbiol 2:253–279

    CAS  Google Scholar 

  • Ansell R, Granath K, Hohmann S, Thevelein JM, Adler L (1997) The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16:2179–2187

    CAS  PubMed  Google Scholar 

  • Bakker BM, Overkamp KM, Maris AJ van, Kotter P, Luttik MA, Dijken JP van, Pronk JT (2001) Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol Rev 25:15–37

    Article  PubMed  Google Scholar 

  • Bjorkqvist S, Ansell R, Adler L, Liden G (1997) Physiological response to anaerobicity of glycerol-3-phosphate dehydrogenase mutants of Saccharomyces cerevisiae. Appl Environ Microbiol 63:128–132

    PubMed  Google Scholar 

  • Blomberg A (1995) Global changes in protein synthesis during adaptation of the yeast Saccharomyces cerevisiae to 0.7 M NaCl. J Bacteriol 177:3563–3572

    CAS  PubMed  Google Scholar 

  • Boucherie H, Bataille N, Fitch IT, Perrot M, Tuite MF (1995) Differential synthesis of glyceraldehyde-3-phosphate dehydrogenase polypeptides in stressed yeast cells. FEMS Microbiol Lett 125:127–133

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Costenoble R, Valadi H, Gustafsson L, Niklasson C, Franzen CJ (2000) Microaerobic glycerol formation in Saccharomyces cerevisiae. Yeast 16:1483–1495

    Article  CAS  PubMed  Google Scholar 

  • Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257

    CAS  PubMed  Google Scholar 

  • Godon C, Lagniel G, Lee J, Buhler JM, Kieffer S, Perrot M, Boucherie H, Toledano MB, Labarre J (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273:22480–22489

    CAS  PubMed  Google Scholar 

  • Gonzalez E, Fernandez MR, Larroy C, Sola L, Pericas MA, Pares X, Biosca JA (2000) Characterization of a (2R,3R)-2,3-butanediol dehydrogenase as the Saccharomyces cerevisiae YAL060W gene product. Disruption and induction of the gene. J Biol Chem 275:35876–35885

    Article  CAS  PubMed  Google Scholar 

  • Jamsa E, Simonen M, Makarow M (1994) Selective retention of secretory proteins in the yeast endoplasmic reticulum by treatment of cells with a reducing agent. Yeast 10:355–370

    CAS  PubMed  Google Scholar 

  • Lin SJ, Guarente L (2003) Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr Opin Cell Biol 15:241–246

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Wang J, Mitsui K, Shen H, Tsurugi K (2002) Interaction of the GTS1 gene product with glyceraldehyde- 3-phosphate dehydrogenase 1 required for the maintenance of the metabolic oscillations of the yeast Saccharomyces cerevisiae. Eur J Biochem 269:3560–3569

    Article  CAS  PubMed  Google Scholar 

  • McAlister L, Holland MJ (1985a) Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15019–15027

    CAS  PubMed  Google Scholar 

  • McAlister L, Holland MJ (1985b) Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 260:15013–15018

    CAS  PubMed  Google Scholar 

  • Norbeck J, Blomberg A (1997) Two-dimensional electrophoretic separation of yeast proteins using a non-linear wide range (pH 3–10) immobilized pH gradient in the first dimension; reproducibility and evidence for isoelectric focusing of alkaline (pI>7) proteins. Yeast 13:1519–1534

    Article  CAS  PubMed  Google Scholar 

  • Norbeck J, Blomberg A (2000) The level of cAMP-dependent protein kinase A activity strongly affects osmotolerance and osmo-instigated gene expression changes in Saccharomyces cerevisiae. Yeast 16:121–137

    Article  CAS  PubMed  Google Scholar 

  • Nordström K (1968) Yeast growth and glycerol formation II. Carbon and redox balances. J Inst Brew 74:429–432

    Google Scholar 

  • Ostergaard H, Rasmussen SK, Roberts TH, Hejgaard J (2000) Inhibitory serpins from wheat grain with reactive centers resembling glutamine-rich repeats of prolamin storage proteins. Cloning and characterization of five major molecular forms. J Biol Chem 275:33272–33279

    Article  CAS  PubMed  Google Scholar 

  • Pahlman IL, Gustafsson L, Rigoulet M, Larsson C (2001) Cytosolic redox metabolism in aerobic chemostat cultures of Saccharomyces cerevisiae. Yeast 18:611–620

    Article  CAS  PubMed  Google Scholar 

  • Simons JF, Ferro-Novick S, Rose MD, Helenius A (1995) BiP/Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast. J Cell Biol 130:41–49

    CAS  PubMed  Google Scholar 

  • Sirover MA (1999) New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 1432:159–184

    CAS  PubMed  Google Scholar 

  • Thomas BJ, Rothstein R (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56:619–630

    PubMed  Google Scholar 

  • Tilton RG (2002) Diabetic vascular dysfunction: links to glucose-induced reductive stress and VEGF. Microsc Res Tech 57:390–407

    CAS  PubMed  Google Scholar 

  • Valadi H, Larsson C, Gustafsson L (1998) Improved ethanol production by glycerol-3-phosphate dehydrogenase mutants of Saccharomyces cerevisiae. Appl Microbiol Biotechnol 50:434–439

    Article  CAS  PubMed  Google Scholar 

  • Valadi H, Valadi A, Adler L, Blomberg A, Gustafsson L (2001) An improved gas distribution system for anaerobic screening of multiple microbial cultures. J Microbiol Methods 47:51–57

    Article  CAS  PubMed  Google Scholar 

  • Van Dijken JP, Scheffers WA (1986) Redox balances in the metabolism of sugars by yeasts. FEMS Microbiol Rev 32:199–225

    CAS  Google Scholar 

  • Wach A, Brachat A, Alberti-Segui C, Rebischung C, Philippsen P (1997) Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13:1065–1075

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Liu W, Mitsui K, Tsurugi K (2001) Evidence for the involvement of the GTS1 gene product in the regulation of biological rhythms in the continuous culture of the yeast Saccharomyces cerevisiae. FEBS Lett 489:81–86

    Article  CAS  PubMed  Google Scholar 

  • Warringer J, Blomberg A (2003) Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20:53–67

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The technical expertise of Ellinor Pettersson in the running of 2D-PAGE is highly acknowledged. This work was supported by grants from the Swedish Energy Council (Energimyndigheten) to L.G. and by grants from the Swedish Science Council (Vetenskapsrådet) to L.G., A.B. and L.A.

Author information

Authors and Affiliations

  1. Department of Chemistry and Bioscience/Molecular Biotechnology, Chalmers University of Technology, Box 462, 405 30, Göteborg, Sweden

    Hadi Valadi, Lena Gustafsson & Joakim Norbeck

  2. Department of Cell and Molecular Biology/Microbiology, Göteborg University, Box 462, 405 30, Göteborg, Sweden

    Åsa Valadi, Lennart Adler & Anders Blomberg

  3. National Laboratory of Forensic Science, 581 94, Linköping, Sweden

    Ricky Ansell

Authors
  1. Hadi Valadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Åsa Valadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricky Ansell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lena Gustafsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lennart Adler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joakim Norbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anders Blomberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joakim Norbeck.

Additional information

Communicated by K. Breunig

H. Valadi and Å. Valadi contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valadi, H., Valadi, Å., Ansell, R. et al. NADH-reductive stress in Saccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1). Curr Genet 45, 90–95 (2004). https://doi.org/10.1007/s00294-003-0469-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-003-0469-1

Keywords

Search

Navigation