1887

Abstract

The Wis1p-Sty1p mitogen-activated protein kinase cascade is a major signalling system in the fission yeast for a wide range of stress responses. It is known that trehalose functions as a protective metabolite to counteract deleterious effects of environmental stresses. Herein it is reported that the expression of genes related to trehalose metabolism in , (neutral trehalase) and [trehalose-6-phosphate (T6P) synthase], is partially regulated by the Sty1p kinase under salt-induced osmotic stress and conditions of slight oxidative stress and is fully dependent on this kinase under severe oxidative stress. This control is carried out through transcription factors Atf1p/Pcr1p during osmotic stress and through Pap1p during exposure to low levels of oxidative stress. However, all three transcription factors are needed for gene expression under conditions of extreme oxidative stress. In addition, a role for Sty1p in the modulation of post-transcriptional activation of trehalase mediated by Pka1p/Sck1p kinases, as well as in the activity of T6P synthase under such stressful conditions has been demonstrated. These results reveal a novel dual action of the Wis1p-Sty1p pathway in the regulation of trehalose metabolism in fission yeast.

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2003-07-01
2024-11-12
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References

  1. Blázquez M. A., Stucka R., Feldmann H., Gancedo C. 1994; Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe . J Bacteriol 176:3895–3902
    [Google Scholar]
  2. Boeke J. D., La Croute F., Fink G. R. 1984; A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197:345–346
    [Google Scholar]
  3. Cansado J., Soto T., Fernández J., Vicente-Soler J., Gacto M. 1998; Characterization of mutants devoid of neutral trehalase activity in the fission yeast Schizosaccharomyces pombe : partial protection from heat shock and high-salt stress. J Bacteriol 180:1342–1345
    [Google Scholar]
  4. Carrillo D., Vicente-Soler J., Gacto M. 1994; Cyclic AMP signaling pathway and trehalase activation in the fission yeast Schizosaccharomyces pombe . Microbiology 140:1467–1472
    [Google Scholar]
  5. Caspari T. 1997; Onset of gluconate-H+ symport in Schizosaccharomyces pombe is regulated by the kinases Wis1 and Pka1, and requires the git1 + gene product. J Cell Sci 110:2599–2608
    [Google Scholar]
  6. Chen D., Toone W. M., Mata J., Lyne R., Burns G., Kirinen K., Brazma A., Jones N., Bähler J. 2003; Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–219
    [Google Scholar]
  7. Crowe J. H., Crowe L. M., Chapman D. 1984; Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703
    [Google Scholar]
  8. Degols G., Shiozaki K., Russell P. 1996; Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe . Mol Cell Biol 16:2870–2877
    [Google Scholar]
  9. Fernández J., Soto T., Vicente-Soler J., Cansado J., Gacto M. 1997a; Heat-shock response in Schizosaccharomyces pombe cells lacking cyclic AMP-dependent phosphorylation. Curr Genet 31:112–118
    [Google Scholar]
  10. Fernández J., Soto T., Vicente-Soler J., Cansado J., Gacto M. 1997b; Osmo-stress-induced changes in neutral trehalase activity of the fission yeast Schizosaccharomyces pombe . Biochim Biophys Acta 135741–48
    [Google Scholar]
  11. Fernández J., Soto T., Franco A., Vicente-Soler J., Cansado J., Gacto M. 1998; Enhancement of neutral trehalase activity by oxidative stress in the fission yeast Schizosaccharomyces pombe . Fungal Genet Biol 25:79–86
    [Google Scholar]
  12. Franco A., Soto T., Vicente-Soler J., Valero Guillén P., Cansado J., Gacto M. 2000; Characterization of tpp1 + as encoding a main trehalose-6P phosphatase in the fission yeast Schizosaccharomyces pombe. J Bacteriol 182:5880–5884
    [Google Scholar]
  13. Higuchi R., Krummel B., Saiki R. K. 1988; A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16:7351–7367
    [Google Scholar]
  14. Hottiger T., De Virgilio C., Hall M. N., Boller T., Wiemken A. 1994; The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro . Eur J Biochem 219:187–193
    [Google Scholar]
  15. Kato T., Okazaki K., Murakami H., Stettler S., Fantes P., Okayama H. 1996; Stress signal, mediated by a Hog1-like MAP kinase, controls sexual development in fission yeast. FEBS Lett 378:207–212
    [Google Scholar]
  16. Maeda T., Watanabe Y., Kunimoto H., Yamamoto M. 1994; Cloning of the pka1 gene encoding the catalytic subunit of the cAMP dependent protein kinase in Schizosaccharomyces pombe . J Biol Chem 269:9632–9637
    [Google Scholar]
  17. Millar J. B. A., Buck V., Wilkinson M. G. 1995; Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev 9:2117–2130
    [Google Scholar]
  18. Moreno S., Klar A., Nurse P. 1991; Molecular genetic analysis of the fission yeast Schizosaccharomyces pombe . Methods Enzymol 194:795–823
    [Google Scholar]
  19. Neely L. A., Hoffman C. S. 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 20:6426–6434
    [Google Scholar]
  20. Quinn J., Findlay V. J., Dawson K., Millar J. B. A., Jones N., Morgan B. A., Toone W. M. 2002; Distinct regulatory proteins control the graded transcriptional response to increasing H2O2 levels in fission yeast Schizosaccharomyces pombe . Mol Biol Cell 13:805–816
    [Google Scholar]
  21. Shiozaki K., Russell P. 1995; Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast. Nature 378:739–743
    [Google Scholar]
  22. Shiozaki K., Russell P. 1996; Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev 10:2276–2288
    [Google Scholar]
  23. Singer M. A., Lindquist S. 1998; Multiple effects of trehalose on protein folding in vitro and in vivo . Mol Cell 1:639–648
    [Google Scholar]
  24. Soto T., Fernández J., Domínguez A., Vicente-Soler J., Cansado J., Gacto M. 1998 Analysis of the ntp1 + gene, encoding neutral trehalase in the fission yeast Schizosaccharomyces pombe Biochim Biophys Acta; 1443225–229
    [Google Scholar]
  25. Soto T., Fernández J., Vicente-Soler J., Cansado J., Gacto M. 1999; Accumulation of trehalose by overexpression of tps1 , coding for trehalose-6-phosphate synthase, causes increased resistance to multiple stresses in the fission yeast Schizosaccharomyces pombe . Appl Environ Microbiol 65:2020–2024
    [Google Scholar]
  26. Takeda T., Toda T., Kominami K., Kohnosu A., Yanagida M., Jones N. 1995; Schizosaccharomyces pombe atf1 + encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J 14:6193–6208
    [Google Scholar]
  27. Toone W. M., Jones N. 1999; AP-1 transcription factors in yeast. Curr Opin Genet Dev 9:55–61
    [Google Scholar]
  28. Toone W. M., Kuge S., Samuels S., Morgan B. A., 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 kinase Sty1/Spc1. Genes Dev 12:1453–1463
    [Google Scholar]
  29. Wahls W. P., Smith G. R. 1994; A heteromeric protein that binds to a meiotic homologous recombination hot spot: correlation of binding and hot spot activity. Genes Dev 8:1693–1702
    [Google Scholar]
  30. Warbrick E., Fantes P. 1991; The wis1 protein kinase is a dosage-dependent regulator of mitosis in Schizosaccharomyces pombe . EMBO J 10:4291–4299
    [Google Scholar]
  31. Watanabe Y., Yamamoto M. 1996; Schizosaccharomyces pombe pcr1 + encodes a CREB/ATF protein involved in regulation of gene expression for sexual development. Mol Cell Biol 16:704–711
    [Google Scholar]
  32. Wilkinson M. G., Millar J. B. A. 1998; SAPKs and transcription factors do the nucleocytoplasmic tango. Genes Dev 12:1391–1397
    [Google Scholar]
  33. Wilkinson M. G., Samuels M., Takeda T., Toone M. W., Shieh J., Toda T., Millar J. B. A., Jones N. 1996; The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev 10:2289–2301
    [Google Scholar]
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