1887

Abstract

Changing the growth mode of by adding fermentable amounts of glucose to cells growing on a non-fermentable carbon source leads to rapid repression of general stress-responsive genes like . Remarkably, glucose repression of appeared to occur even at very low glucose concentrations, down to 0005%. Although these low levels of glucose do not induce fermentative growth, they do act as a growth signal, since upon addition of glucose to a concentration of 002%, growth rate increased and ribosomal protein gene transcription was up-regulated. In an attempt to elucidate how this type of glucose signalling may operate, several signalling mutants were examined. Consistent with the low amounts of glucose that elicit repression, neither the main glucose-repression pathway nor cAMP-dependent activation of protein kinase A appeared to play a role in this regulation. Using mutants involved in glucose metabolism, evidence was obtained suggesting that glucose 6-phosphate serves as a signalling molecule. To identify the target for glucose repression on the promoter of the gene, a promoter deletion series was used. The major transcription factors governing (stress-induced) transcriptional activation of are Msn2p and Msn4p, binding to the general stress-responsive promoter elements (STREs). Surprisingly, glucose repression of appeared to be independent of Msn2/4p: transcription in glycerol-grown cells was unaffected in a ΔΔ strain. Nevertheless, evidence was obtained that STRE-mediated transcription is the target of repression by low amounts of glucose. These data suggest that an as yet unidentified factor is involved in STRE-mediated transcriptional regulation of .

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2000-02-01
2021-12-01
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References

  1. Beullens M., Mbonyi K., Geerts L., Gladines D., Detremerie K., Jans A. W., Thevelein J. M. 1988; Studies on the mechanism of the glucose-induced cAMP signal in glycolysis and glucose repression mutants of the yeast Saccharomyces cerevisiae. Eur J Biochem 172:227–231 [CrossRef]
    [Google Scholar]
  2. Boles E., Heinisch J., Zimmermann F. K. 1993; Different signals control the activation of glycolysis in the yeast Saccharomyces cerevisiae. Yeast 9:761–770 [CrossRef]
    [Google Scholar]
  3. Cameron S., Levin L., Zoller M., Wigler M. 1988; cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae. Cell 53:555–566 [CrossRef]
    [Google Scholar]
  4. Cereghino G. P., Scheffler I. E. 1996; Genetic analysis of glucose regulation in Saccharomyces cerevisiae: control of transcription versus mRNA turnover. EMBO J 15:363–374
    [Google Scholar]
  5. Colombo S., Ma P. S., Cauwenberg L.8 other authors 1998; Involvement of distinct G-proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAmp signalling in the yeast Saccharomyces cerevisiae. EMBO J 17:3326–3341 [CrossRef]
    [Google Scholar]
  6. Corominas J., Clotet J., Fernandez-Banares I., Boles E., Zimmermann F. K., Guinovart J. J., Arino J. 1992; Glycogen metabolism in a Saccharomyces cerevisiae phosphoglucose isomerase (pgil) disruption mutant. FEBS Lett 310:182–186 [CrossRef]
    [Google Scholar]
  7. Crauwels M., Donaton M. C. V., Pernambuco M. B., Winderickx J., De Winde J. H., Thevelein J. M. 1997; The Sch9 protein kinase in the yeast Saccharomyces cerevisiae controls cApk activity and is required for nitrogen activation of the fermentable-growth-medium-induced (FGM) pathway. Microbiology 143:2627–2637 [CrossRef]
    [Google Scholar]
  8. De Winde J. H., Crauwels M., Hohmann S., Thevelein J. M., Winderickx J. 1996; Differential requirement of the yeast sugar kinases for sugar sensing in establishing the catabolite-repressed state. Eur J Biochem 241:633–643 [CrossRef]
    [Google Scholar]
  9. Estruch F., Carlson M. 1993; Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol 13:3872–3881
    [Google Scholar]
  10. Gancedo J. M. 1998; Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361
    [Google Scholar]
  11. Gonçalves P., Planta R. J. 1998; Starting up yeast glycolysis. Trends Microbiol 6:314–319 [CrossRef]
    [Google Scholar]
  12. Gorner W., Durchschlag E., Martinez-Pastor M. T., Estruch F., Ammerer G., Hamilton B., Ruis H., Schuller C. 1998; Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 12:586–597 [CrossRef]
    [Google Scholar]
  13. Griffioen G., Mager W. H., Planta R. J. 1994; Nutritional upshift response of ribosomal protein gene transcription in Saccharomyces cerevisiae. FEMS Microbiol Lett 123:137–144 [CrossRef]
    [Google Scholar]
  14. Griffioen G., Laan R. J., Mager W. H., Planta R. J. 1996; Ribosomal protein gene transcription in Saccharomyces cerevisiae shows a biphasic response to nutritional changes. Microbiology 142:2279–2287 [CrossRef]
    [Google Scholar]
  15. Herrero P., Martinezcampa C., Moreno F. 1998; The hexokinase 2 protein participates in regulatory DNA–protein complexes necessary for glucose repression of the SUC2 gene in Saccharomyces cerevisiae. FEBS Lett 434:71–76 [CrossRef]
    [Google Scholar]
  16. Hohmann S. 1997; Shaping up: the responses of yeast to osmotic stress. In Yeast Stress Responses pp. 101–146Edited by Hohmann S., Mager W. H. Georgetown, TX: R. G. Landes;
    [Google Scholar]
  17. Hohmann S., Neves M. J., de Koning W., Alijo R., Ramos J., Thevelein J. M. 1993; The growth and signalling defects of the ggs1 (fdp1/byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII. Curr Genet 23:281–289 [CrossRef]
    [Google Scholar]
  18. Jiang Y., Davis C., Broach J. R. 1998; Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway. EMBO J 17:6942–6951 [CrossRef]
    [Google Scholar]
  19. Kraakman L., Lemaire K., Ma P. S., Teunissen A., Donaton M. C. V., Van Dijck P., Winderickx J., de Winde J. H., Thevelein J. M. 1999; A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose. Mol Microbiol 32:1002–1012 [CrossRef]
    [Google Scholar]
  20. Kubler E., Mosch H. U., Rupp S., Lisanti M. P. 1997; Gpa2p, a G-protein alpha-subunit, regulates growth and pseudohyphal development in Saccharomyces cerevisiae via a cAMP-dependent mechanism. J Biol Chem 272:20321–20323 [CrossRef]
    [Google Scholar]
  21. Lombardo A., Cereghino G. P., Scheffler I. E. 1992; Control of mRNA turnover as a mechanism of glucose repression in Saccharomyces cerevisiae. Mol Cell Biol 12:2941–2948
    [Google Scholar]
  22. Lorenz M. C., Heitman J. 1997; Yeast pseudohyphal growth is regulated by Gpa2, a G protein alpha homolog. EMBO J 16:7008–7018 [CrossRef]
    [Google Scholar]
  23. Lundin M., Nehlin J. O., Ronne H. 1994; Importance of a flanking AT-rich region in target site recognition by the GC box-binding zinc finger protein MIG1. Mol Cell Biol 14:1979–1985
    [Google Scholar]
  24. Mager W. H., Planta R. J. 1991; Coordinate expression of ribosomal protein genes in yeast as a function of cellular growth rate. Mol Cell Biochem 104:181–187
    [Google Scholar]
  25. Martinez-Pastor M. T., Marchler G., Schuller C., Marchler-Bauer A., Ruis H., Estruch F. 1996; The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15:2227–35
    [Google Scholar]
  26. Meijer M. M. C., Boonstra J., Verkleij A. J., Verrips C. T. 1998; Glucose repression in Saccharomyces cerevisiae is related to the glucose concentration rather than the glucose flux. J Biol Chem 273:24102–24107 [CrossRef]
    [Google Scholar]
  27. Moskvina E., Schuller C., Maurer C. T., Mager W. H., Ruis H. 1998; A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast 14:1041–1050 [CrossRef]
    [Google Scholar]
  28. Nehlin J. O., Carlberg M., Ronne H. 1991; Control of yeast GAL genes by MIG1 repressor: a transcriptional cascade in the glucose response. EMBO J 10:3373–3377
    [Google Scholar]
  29. Ni H. T., LaPorte D. C. 1995; Response of a yeast glycogen synthase gene to stress. Mol Microbiol 16:1197–1205 [CrossRef]
    [Google Scholar]
  30. Nonet M., Scafe C., Sexton J., Young R. 1987; Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol 7:1602–1611
    [Google Scholar]
  31. Ozcan S., Vallier L. G., Flick J. S., Carlson M., Johnston M. 1997; Expression of the SUC2 gene of Saccharomyces cerevisiae is induced by low levels of glucose. Yeast 13:127–137 [CrossRef]
    [Google Scholar]
  32. Parrou J. L., Enjalbert B., Plourde L., Bauche A., Gonzalez B., Francois J. 1999; Dynamic responses of reserve carbohydrate metabolism under carbon and nitrogen limitations in Saccharomyces cerevisiae. Yeast 15:191–203 [CrossRef]
    [Google Scholar]
  33. Pernambuco M. B., Winderickx J., Crauwels M., Griffioen G., Mager W. H., Thevelein J. M. 1996; Glucose-triggered signalling in Saccharomyces cerevisiae: different requirements for sugar phosphorylation between cells grown on glucose and those grown on non-fermentable carbon sources. Microbiology 142:1775–1782 [CrossRef]
    [Google Scholar]
  34. Praekelt U. M., Meacock P. A. 1990; HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol Gen Genet 223:97–106 [CrossRef]
    [Google Scholar]
  35. Randezgil F., Sanz P., Entian K. D., Prieto J. A. 1998; Carbon source-dependent phosphorylation of hexokinase PII and its role in the glucose-signaling response in yeast. Mol Cell Biol 18:2940–2948
    [Google Scholar]
  36. Ronne H. 1995; Glucose repression in fungi. Trends Genet 11:12–17 [CrossRef]
    [Google Scholar]
  37. Scheffler I. E., Delacruz B. J., Prieto S. 1998; Control of mRNA turnover as a mechanism of glucose repression in Saccharomyces cerevisiae. Int J Biochem Cell Biol 30:1175–1193 [CrossRef]
    [Google Scholar]
  38. Schmitt A. P., McEntee K. 1996; Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93:5777–5782 [CrossRef]
    [Google Scholar]
  39. Siderius M., Rots E., Mager W. H. 1997; High-osmolarity signalling in Saccharomyces cerevisiae is modulated in a carbon-source-dependent fashion. Microbiology 143:3241–3250 [CrossRef]
    [Google Scholar]
  40. Thevelein J. M. 1991; Fermentable sugars and intracellular acidification as specific activators of the RAS–adenylate cyclase signalling pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol 5:1301–1307 [CrossRef]
    [Google Scholar]
  41. Thevelein J. M. 1994; Signal transduction in yeast. Yeast 10:1753–1790 [CrossRef]
    [Google Scholar]
  42. Thomas B. J., Rothstein R. 1989; Elevated recombination rates in transcriptionally active DNA. Cell 56:619–630 [CrossRef]
    [Google Scholar]
  43. Toda T., Uno I., Ishikawa T.7 other authors 1985; In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40:27–36 [CrossRef]
    [Google Scholar]
  44. Treitel M. A., Carlson M. 1995; Repression by SSN6–TUP1 is directed by MIG1, a repressor/activator protein. Proc Natl Acad Sci USA 92:3132–3136 [CrossRef]
    [Google Scholar]
  45. Varela J. C., Praekelt U. M., Meacock P. A., Planta R. J., Mager W. H. 1995; The Saccharomyces cerevisiae HSP12 gene is activated by the high-osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol Cell Biol 15:6232–6245
    [Google Scholar]
  46. Yin Z. K., Smith R. J., Brown A. J. P. 1996; Multiple signalling pathways trigger the exquisite sensitivity of yeast gluconeogenic mRNAs to glucose. Mol Microbiol 20:751–764 [CrossRef]
    [Google Scholar]
  47. Yun C. W., Tamaki H., Nakayama R., Yamamoto K., Kumagai H. 1998; Gpr1p, a putative G-protein coupled receptor, regulates glucose-dependent cellular cAMP level in yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 252:29–33 [CrossRef]
    [Google Scholar]
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