1887

Microbiology Society logo

Volume 142, Issue 8

Ribosomal protein gene transcription in shows a biphasic response to nutritional changes Free

Abstract

Nutrients are major determinants of ribosomal protein (rp-) gene transcription in . In order to investigate the molecular mechanisms underlying this nutritional control, yeast mutants that display defects in the glucose upshift response of rp-gene transcription were isolated. Interestingly, although growth of these mutants on glucose-containing medium was severely affected an initial increase in rp-gene transcription by nutritional upshift was still observed. However, at later time points, rp-mRNA levels decreased strongly. Various other types of severe growth limitation also did not prevent the initial upshift in transcription. The results suggest that the glucose upshift response of rp-gene transcription comprises two phases: an initial, transient response independent of the actual growth potential, and a sustained response which is dependent on growth and requires both glucose and adequate nitrogen sources. Previously, it was found that protein kinase A (Pka) mediates the initial upshift response, without the need for regulation of Pka activity by cAMP. The present data substantiate that, besides the RAS/adenylate cyclase pathway, an alternative pathway through Pka regulates rp-gene transcription. In addition, evidence is presented that the sustained response does not require Pka activity. Based on these results, taken together, a model is proposed in which rp-gene transcription is dynamically regulated by multiple signal transduction pathways.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): nutritional signalling , ribosomal protein gene and Saccharomyces cerevisiae
© Society for General Microbiology 1996
Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-142-8-2279
1996-08-01
2024-05-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/142/8/mic-142-8-2279.html?itemId=/content/journal/micro/10.1099/13500872-142-8-2279&mimeType=html&fmt=ahah

References

  1. Arguelles J.C., Mbonyi K., Van Aelst L., Vanhalewyn M., Jans A.W., Thevelein J.M. 1990; Absence of glucose-induced cAMP signaling in the Saccharomyces cerevisiae mutants cat1 and cat3 which are deficient in derepression of glucose-repressible proteins. Arch Microbiol 154:199–205
     [Google Scholar]
  2. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. 1994 Current Protocols in Molecular Biology 1 New York: John Wiley;
     [Google Scholar]
  3. Belazzi T., Wagner A., Wieser R., Schanz M., Adam G., Hartig A., Ruis H. 1991; Negative regulation of transcription of the Saccharomyces cerevisiae catalase T ( CTT1 ) gene by cAMP is mediated by a positive control element. EMBO J 10:585–592
     [Google Scholar]
  4. 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
     [Google Scholar]
  5. Broach J.R. 1991; RAS genes in Saccharomyces cerevisiae : signal transduction in search of a pathway. Trends Genet 7:28–33
     [Google Scholar]
  6. Broek D., Toda T., Michaeli T., Levin L., Birchmeier C., Zoller M., Powers S., Wigler M. 1987; The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell 48:789–799
     [Google Scholar]
  7. Bromley S., Hereford L., Rosbash M. 1982; Further evidence that the rna2 mutation of Saccharomyces cerevisiae affects mRNA processing. Mol Cell Biol 2:1205–1211
     [Google Scholar]
  8. 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
     [Google Scholar]
  9. Donovan D.M., Pearson N.J. 1986; Transcriptional regulation of ribosomal proteins during a nutritional upshift in Saccharomyces cerevisiae . Mol Cell Biol 6:2429–2435
     [Google Scholar]
  10. Durfee T., Becherer K., Chen P.L., Yeh S.H., Yang Y., Kilburn A.E., Lee W.H., Elledge S.J. 1993; The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev 7:555–569
     [Google Scholar]
  11. Durnez P., Pernambuco M.B., Oris E., Arguelles J.C., Mergels-berg H., Thevelein J.M. 1994; Activation of trehalase during growth induction by nitrogen sources in the yeast Saccharomyces cerevisiae depends on the free catalytic subunits of cAMP-dependent protein kinase, but not on functional Ras proteins. Yeast 10:1049–1064
     [Google Scholar]
  12. Fleig U.N., Pridmore R.D., Philippsen P. 1986; Construction of LYS2 cartridges for use in genetic manipulations of Saccharomyces cerevisiae . Gene 46:237–245
     [Google Scholar]
  13. Gancedo J.M. 1992; Carbon catabolite repression in yeast. Eur J Biochem 206:297–313
     [Google Scholar]
  14. Garrett S., Broach J. 1989; Loss of Ras activity in Saccharomyces cerevisiae is suppressed by disruptions of a new kinase gene, YAK1 whose product may act downstream of the cAMP-dependent protein kinase. Genes Dev 3:1336–1348
     [Google Scholar]
  15. Goncalves P.M., Griffioen G., Minnee R., Bosma M., Kraakman L.S., Mager W.H., Planta R.J. 1995; Transcription activation of yeast ribosomal protein genes requires additional elements apart from binding sites for Abflp or Raplp. Nucleic Acids Res 23:1475–1480
     [Google Scholar]
  16. Griffioen G., Mager W.H., Planta R.J. 1994; Nutritional upshift response of ribosomal protein gene transcription in Saccharomyces cerevisiae . FEMS Microbiol Eett 123:137–144
     [Google Scholar]
  17. Herruer M.H., Mager W.H., Woudt L.P., Nieuwint R.T., Wassenaar G.M., Groeneveld P., Planta R.J. 1987; Transcriptional control of yeast ribosomal protein synthesis during carbon-source upshift. Nucleic Acids Res 15:10133–10144
     [Google Scholar]
  18. Hinnebusch A.G. 1988; Mechanisms of gene regulation in the general control of amino acid biosynthesis in Saccharomyces cerevisiae . Microbiol Rev 52:248–273
     [Google Scholar]
  19. Hinnebusch A.G. 1994; Translational control of GCN4: an in vivo barometer of initiation-factor activity. Trends Biochem Sci 19:409–414
     [Google Scholar]
  20. Hirimburegama K., Durnez P., Keleman J., Oris E., Vergauwen R., Mergelsberg H., Thevelein J.M. 1992; Nutrient-induced activation of trehalase in nutrient-starved cells of the yeast Saccharomyces cerevisiae : cAMP is not involved as second messenger. J Gen Microbiol 138:2035–2043
     [Google Scholar]
  21. Kataoka T., Powers S., McGill C., Fasano O., Strathern J., Broach J., Wigler M. 1984; Genetic analysis of yeast RAS1 and RAS2 genes. Cell 37:437–445
     [Google Scholar]
  22. Kief D.R., Warner J.R. 1981; Coordinate control of syntheses of ribosomal ribonucleic acid and ribosomal proteins during nutritional shift-up in Saccharomyces cerevisiae . Mol Cell Biol 1:1007–1015
     [Google Scholar]
  23. Klein C., Struhl K. 1994; Protein kinase A mediates growth- regulated expression of yeast ribosomal protein genes by modulating Rapl transcriptional activity. Mol Cell Biol 14:1920–1928
     [Google Scholar]
  24. Kraakman L.S., Griffioen G., Zerp S., Groeneveld P., Thevelein J.M., Mager W.H., Planta R.J. 1993; Growth-related expression of ribosomal protein genes in Saccharomyces cerevisiae . Mol Gen Genet 239:196–204
     [Google Scholar]
  25. Kuenzler M., Balmelli T., Egli C. M., Paravicini G., Braus G.H. 1993; Cloning, primary structure, and regulation of the HIS7 gene encoding a bifunctional glutamine amidotransferase: cyclase from Saccharomyces cerevisiae . J Bacteriol 175:5548–5558
     [Google Scholar]
  26. Leer R.J., van Raamsdonk-Duin M.M., Hagendoorn M.J., Mager W.H., Planta R.J. 1984; Structural comparison of yeast ribosomal protein genes. Nucleic Acids Res 12:6685–6700
     [Google Scholar]
  27. 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]
  28. Marchler G., Schuller C., Adam G., Ruis H. 1993; A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 12:1997–2003
     [Google Scholar]
  29. Matsumoto K., Uno I., Ishikawa T. 1983a; Control of cell division in Saccharomyces cerevisiae mutants defective in adenylate cyclase and cAMP-dependent protein kinase. Exp Cell Res 146:151–161
     [Google Scholar]
  30. Matsumoto K., Uno I., Ishikawa T. 1983b; Initiation of meiosis in yeast mutants defective in adenylate cyclase and cyclic AMP-dependent protein kinase. Cell 32:417–423
     [Google Scholar]
  31. Neuman-Silberberg F.S., Bhattacharya S., Broach J.R. 1995; Nutrient availability and the RAS/cyclic AMP pathway both induce expression of ribosomal protein genes in Saccharomyces cerevisiae but by different mechanisms. Mol Cell Biol 15:3187–3196
     [Google Scholar]
  32. Nikawa J., Cameron S., Toda T., Ferguson K.M., Wigler M. 1987; Rigorous feedback control of cAMP levels in Saccharomyces cerevisiae . Genes Dev 1:931–937
     [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
     [Google Scholar]
  34. Rose M.D., Fink G.R. 1987; KAR1 a gene required for function of both intranuclear and extranuclear microtubules in yeast. Cell 48:1047–1060
     [Google Scholar]
  35. Tanaka K., Matsumoto K., Toh-e A. 1988; Dual regulation of the expression of the polyubiquitin gene by cyclic AMP and heat shock in yeast. EMBO J 7:495–502
     [Google Scholar]
  36. 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
     [Google Scholar]
  37. Thevelein J.M. 1992; The RAS-adenylate cyclase pathway and cell cycle control in Saccharomyces cerevisiae . Antonie Eeeuwenhoek 62:109–130
     [Google Scholar]
  38. Thevelein J.M. 1994; Signal transduction in yeast. Yeast 10:1753–1790
     [Google Scholar]
  39. Toda T., Cameron S., Sass P., Zoller M., Scott J. D., McMullen B., Hurwitz M., Krebs E.G., Wigler M. 1987a; Cloning and characterization of BCY /, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae . Mol Cell Biol 7:1371–1377
     [Google Scholar]
  40. Toda T., Cameron S., Sass P., Zoller M., Wigler M. 1987b; Three different genes in S.cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 50:277–287
     [Google Scholar]
  41. Toda T., Uno I., Ishikawa T., Powers S., Kataoka T., Broek D., Cameron S., Broach J., Matsumoto K., Wigler M. 1985; In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 40:27–36
     [Google Scholar]
  42. Trumbly R.J. 1992; Glucose repression in the yeast Saccbaromyces cerevisiae . Mol Microbiol 6:15–21
     [Google Scholar]
  43. Werner-Washburne M., Braun E., Johnston G.C., Singer R.A. 1993; Stationary phase in the yeast Saccbaromyces cerevisiae . Microbiol Rev 57:383–401
     [Google Scholar]
  44. Winston M.K., Bhattacharjee J.K. 1982; Growth inhibition by α-aminoadipate and reversal of the effect by specific amino acid supplements in Saccbaromyces cerevisiae . J Bacteriol 152:874–879
     [Google Scholar]
  45. Zaret K.S., Sherman F. 1985; α-Aminoadipate as a primary nitrogen source for Saccbaromyces cerevisiae mutants. J Bacteriol 162:579–583
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/13500872-142-8-2279
Loading
Ribosomal protein gene transcription in Saccharomyces cerevisiae shows a biphasic response to nutritional changes
Microbiology 142, 2279 (1996); https://doi.org/10.1099/13500872-142-8-2279
/content/journal/micro/10.1099/13500872-142-8-2279
/content/journal/micro/10.1099/13500872-142-8-2279
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error