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Volume 154, Issue 9

The pathway by which the yeast protein kinase Snf1p controls acquisition of sodium tolerance is different from that mediating glucose regulation Free

Abstract

It recently became apparent that the highly conserved Snf1p protein kinase plays roles in controlling different cellular processes in the yeast , in addition to its well-known function in glucose repression/derepression. We have previously reported that Snf1p together with Gis4p controls ion homeostasis by regulating expression of , which encodes the Ena1p Na extrusion system. In this study we found that Snf1p is rapidly phosphorylated when cells are exposed to NaCl and this phosphorylation is required for the role of Snf1p in Na tolerance. In contrast to activation by low glucose levels, the salt-induced phosphorylation of Snf1p promoted neither phosphorylation nor nuclear export of the Mig1p repressor. The mechanism that prevents Mig1p phosphorylation by active Snf1p under salt stress does not involve either hexokinase PII or the Gis4p regulator. Instead, Snf1p may mediate upregulation of expression via the repressor Nrg1p. Activation of Snf1p in response to glucose depletion requires any of the three upstream protein kinases Sak1p, Tos3p and Elm1p, with Sak1p playing the most prominent role. The same upstream kinases were required for salt-induced Snf1p phosphorylation, and also under these conditions Sak1p played the most prominent role. Unexpectedly, however, it appears that Elm1p plays a dual role in acquisition of salt tolerance by activating Snf1p and in a presently unknown parallel pathway. Together, these results indicate that under salt stress Snf1p takes part in a different pathway from that during glucose depletion and this role is performed together as well as in parallel with its upstream kinase Elm1p. Snf1p appears to be part of a wider functional network than previously anticipated and the full complexity of this network remains to be elucidated.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): HA, haemagglutinin
SGM
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2008-09-01
2024-04-19
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References

  1. Ahuatzi D., Riera A., Pelaez R., Herrero P., Moreno F. 2007; Hxk2 regulates the phosphorylation state of Mig1 and therefore its nucleocytoplasmic distribution. J Biol Chem 282:4485–4493
     [Google Scholar]
  2. Alepuz P. M., Cunningham K. W., Estruch F. 1997; Glucose repression affects ion homeostasis in yeast through the regulation of the stress-activated ENA1 gene. Mol Microbiol 26:91–98
     [Google Scholar]
  3. Amodeo G. A., Rudolph M. J., Tong L. 2007; Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1. Nature 449:492–495
     [Google Scholar]
  4. Balciunas D., Ronne H. 1999; Yeast genes GIS1–4: multicopy suppressors of the Gal- phenotype of snf1 mig1 srb8/10/11 cells. Mol Gen Genet 262:589–599
     [Google Scholar]
  5. Berkey C. D., Carlson M. 2006; A specific catalytic subunit isoform of protein kinase CK2 is required for phosphorylation of the repressor Nrg1 in Saccharomyces cerevisiae . Curr Genet 50:1–10
     [Google Scholar]
  6. Berkey C. D., Vyas V. K., Carlson M. 2004; Nrg1 and Nrg2 transcriptional repressors are differently regulated in response to carbon source. Eukaryot Cell 3:311–317
     [Google Scholar]
  7. Bouquin N., Barral Y., Courbeyrette R., Blondel M., Snyder M., Mann C. 2000; Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae . J Cell Sci 113:1435–1445
     [Google Scholar]
  8. Carling D. 2004; The AMP-activated protein kinase cascade – a unifying system for energy control. Trends Biochem Sci 29:18–24
     [Google Scholar]
  9. Carlson M. 1999; Glucose repression in yeast. Curr Opin Microbiol 2:202–207
     [Google Scholar]
  10. Causton H. C., Ren B., Koh S. S., Harbison C. T., Kanin E., Jennings E. G., Lee T. I., True H. L., Lander E. S., Young R. A. 2001; Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12:323–337
     [Google Scholar]
  11. Celenza J. L., Carlson M. 1989; Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein. Mol Cell Biol 9:5034–5044
     [Google Scholar]
  12. Celenza J. L., Eng F. J., Carlson M. 1989; Molecular analysis of the SNF4 gene of Saccharomyces cerevisiae : evidence for physical association of the SNF4 protein with the SNF1 protein kinase. Mol Cell Biol 9:5045–5054
     [Google Scholar]
  13. Crespo J. L., Daicho K., Ushimaru T., Hall M. N. 2001; The GATA transcription factors GLN3 and GAT1 link TOR to salt stress in Saccharomyces cerevisiae . J Biol Chem 276:34441–34444
     [Google Scholar]
  14. Cunningham K. W., Fink G. R. 1996; Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae . Mol Cell Biol 16:2226–2237
     [Google Scholar]
  15. De Vit M. J., Waddle J. A., Johnston M. 1997; Regulated nuclear translocation of the Mig1 glucose repressor. Mol Biol Cell 8:1603–1618
     [Google Scholar]
  16. Gari E., Piedrafita L., Aldea M., Herrero E. 1997; A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae . Yeast 13:837–848
     [Google Scholar]
  17. Garrett J. M. 1997; The control of morphogenesis in Saccharomyces cerevisiae by Elm1 kinase is responsive to RAS/cAMP pathway activity and tryptophan availability. Mol Microbiol 26:809–820
     [Google Scholar]
  18. Haro R., Garciadeblas B., Rodriguez-Navarro A. 1991; A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett 291:189–191
     [Google Scholar]
  19. Hedbacker K., Carlson M. 2008; SNF1/AMPK pathways in yeast. Front Biosci 13:2408–2420
     [Google Scholar]
  20. Hirata D., Harada S., Namba H., Miyakawa T. 1995; Adaptation to high-salt stress in Saccharomyces cerevisiae is regulated by Ca2+/calmodulin-dependent phosphoprotein phosphatase (calcineurin) and cAMP-dependent protein kinase. Mol Gen Genet 249:257–264
     [Google Scholar]
  21. Hong S. P., Carlson M. 2007; Regulation of Snf1 protein kinase in response to environmental stress. J Biol Chem 282:16838–16845
     [Google Scholar]
  22. Hong S. P., Leiper F. C., Woods A., Carling D., Carlson M. 2003; Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci U S A 100:8839–8843
     [Google Scholar]
  23. Janke C., Magiera M. M., Rathfelder N., Taxis C., Reber S., Maekawa H., Moreno-Borchart A., Doenges G., Schwob E. other authors 2004; A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21:947–962
     [Google Scholar]
  24. Jiang R., Carlson M. 1996; Glucose regulates protein interactions within the yeast SNF1 protein kinase complex. Genes Dev 10:3105–3115
     [Google Scholar]
  25. Jiang R., Carlson M. 1997; The Snf1 protein kinase and its activating subunit, Snf4, interact with distinct domains of the Sip1/Sip2/Gal83 component in the kinase complex. Mol Cell Biol 17:2099–2106
     [Google Scholar]
  26. Johnston M. 1999; Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet 15:29–33
     [Google Scholar]
  27. Koehler C. M., Myers A. M. 1997; Serine-threonine protein kinase activity of Elm1p, a regulator of morphologic differentiation in Saccharomyces cerevisiae . FEBS Lett 408:109–114
     [Google Scholar]
  28. Lamb T. M., Mitchell A. P. 2003; The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae . Mol Cell Biol 23:677–686
     [Google Scholar]
  29. Lamb T. M., Xu W., Diamond A., Mitchell A. P. 2001; Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 276:1850–1856
     [Google Scholar]
  30. Marquez J. A., Serrano R. 1996; Multiple transduction pathways regulate the sodium-extrusion gene PMR2/ENA1 during salt stress in yeast. FEBS Lett 382:89–92
     [Google Scholar]
  31. McCartney R. R., Schmidt M. C. 2001; Regulation of Snf1 kinase. Activation requires phosphorylation of threonine 210 by an upstream kinase as well as a distinct step mediated by the Snf4 subunit. J Biol Chem 276:36460–36466
     [Google Scholar]
  32. McCartney R. R., Rubenstein E. M., Schmidt M. C. 2005; Snf1 kinase complexes with different beta subunits display stress-dependent preferences for the three Snf1-activating kinases. Curr Genet 47:335–344
     [Google Scholar]
  33. Mendizabal I., Pascual-Ahuir A., Serrano R., de Larrinoa I. F. 2001; Promoter sequences regulated by the calcineurin-activated transcription factor Crz1 in the yeast ENA1 gene. Mol Genet Genomics 265:801–811
     [Google Scholar]
  34. Mendoza I., Rubio F., Rodriguez-Navarro A., Pardo J. M. 1994; The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae . J Biol Chem 269:8792–8796
     [Google Scholar]
  35. Mendoza I., Quintero F. J., Bressan R. A., Hasegawa P. M., Pardo J. M. 1996; Activated calcineurin confers high tolerance to ion stress and alters the budding pattern and cell morphology of yeast cells. J Biol Chem 271:23061–23067
     [Google Scholar]
  36. Moreno F., Ahuatzi D., Riera A., Palomino C. A., Herrero P. 2005; Glucose sensing through the Hxk2-dependent signalling pathway. Biochem Soc Trans 33:265–268
     [Google Scholar]
  37. Nath N., McCartney R. R., Schmidt M. C. 2003; Yeast Pak1 kinase associates with and activates Snf1. Mol Cell Biol 23:3909–3917
     [Google Scholar]
  38. Nehlin J. O., Ronne H. 1990; Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J 9:2891–2898
     [Google Scholar]
  39. Niedenthal R. K., Riles L., Johnston M., Hegemann J. H. 1996; Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12:773–786
     [Google Scholar]
  40. Ostling J., Ronne H. 1998; Negative control of the Mig1p repressor by Snf1p-dependent phosphorylation in the absence of glucose. Eur J Biochem 252:162–168
     [Google Scholar]
  41. Platara M., Ruiz A., Serrano R., Palomino A., Moreno F., Arino J. 2006; The transcriptional response of the yeast Na+-ATPase ENA1 gene to alkaline stress involves three main signaling pathways. J Biol Chem 281:36632–36642
     [Google Scholar]
  42. Proft M., Serrano R. 1999; Repressors and upstream repressing sequences of the stress-regulated ENA1 gene in Saccharomyces cerevisiae : bZIP protein Sko1p confers HOG-dependent osmotic regulation. Mol Cell Biol 19:537–546
     [Google Scholar]
  43. Proft M., Pascual-Ahuir A., de Nadal E., Arino J., Serrano R., Posas F. 2001; Regulation of the Sko1 transcriptional repressor by the Hog1 MAP kinase in response to osmotic stress. EMBO J 20:1123–1133
     [Google Scholar]
  44. Rep M., Proft M., Remize F., Tamas M., Serrano R., Thevelein J. M., Hohmann S. 2001; The Saccharomyces cerevisiae Sko1p transcription factor mediates HOG pathway-dependent osmotic regulation of a set of genes encoding enzymes implicated in protection from oxidative damage. Mol Microbiol 40:1067–1083
     [Google Scholar]
  45. Rose M. D., Winston F., Hieter P. 1990 Methods in Yeast Genetics: a Laboratory Course Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  46. Rubenstein E. M., McCartney R. R., Zhang C., Shokat K. M., Shirra M. K., Arndt K. M., Schmidt M. C. 2008; Access denied: Snf1 activation loop phosphorylation is controlled by availability of the phosphorylated threonine 210 to the PP1 phosphatase. J Biol Chem 283:222–230
     [Google Scholar]
  47. Ruiz A., Arino J. 2007; Function and regulation of the Saccharomyces cerevisiae ENA sodium ATPase system. Eukaryot Cell 6:2175–2183
     [Google Scholar]
  48. Schmidt M. C., McCartney R. R. 2000; β -Subunits of Snf1 kinase are required for kinase function and substrate definition. EMBO J 19:4936–4943
     [Google Scholar]
  49. Serrano R., Rodriguez-Navarro A. 2001; Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404
     [Google Scholar]
  50. Serrano R., Marquez J. A., Rios G. 1997; Crucial factors in salt stress tolerance. In Yeast Stress Responses pp 000–000 Edited by Hohmann S., Mager W. H. Austin, TX: Landes;
     [Google Scholar]
  51. Serrano R., Mulet J. M., Rios G., Marques J. A., De Larrinoa I. F., Leube M. P., Mendizabal I., Pascual-Ahuir A., Proft M., Ros R., Montesinos C. 1999; A glimpse of the mechanisms of ion homeostasis during salt stress. J Exp Bot 50:1023–1036
     [Google Scholar]
  52. Serrano R., Ruiz A., Bernal D., Chambers J. R., Arino J. 2002; The transcriptional response to alkaline pH in Saccharomyces cerevisiae : evidence for calcium-mediated signalling. Mol Microbiol 46:1319–1333
     [Google Scholar]
  53. Sherman F., Fink G. R., Hicks J. B. 1983 Methods in Yeast Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  54. Sutherland C. M., Hawley S. A., McCartney R. R., Leech A., Stark M. J., Schmidt M. C., Hardie D. G. 2003; Elm1p is one of three upstream kinases for the Saccharomyces cerevisiae SNF1 complex. Curr Biol 13:1299–1305
     [Google Scholar]
  55. Thomas B. J., Rothstein R. 1989; Elevated recombination rates in transcriptionally active DNA. Cell 56:619–630
     [Google Scholar]
  56. Vincent O., Carlson M. 1999; Gal83 mediates the interaction of the Snf1 kinase complex with the transcription activator Sip4. EMBO J 18:6672–6681
     [Google Scholar]
  57. Vincent O., Townley R., Kuchin S., Carlson M. 2001; Subcellular localization of the Snf1 kinase is regulated by specific beta subunits and a novel glucose signaling mechanism. Genes Dev 15:1104–1114
     [Google Scholar]
  58. Vyas V. K., Kuchin S., Carlson M. 2001; Interaction of the repressors Nrg1 and Nrg2 with the Snf1 protein kinase in Saccharomyces cerevisiae . Genetics 158:563–572
     [Google Scholar]
  59. Vyas V. K., Berkey C. D., Miyao T., Carlson M. 2005; Repressors Nrg1 and Nrg2 regulate a set of stress-responsive genes in Saccharomyces cerevisiae . Eukaryot Cell 4:1882–1891
     [Google Scholar]
  60. Wadskog I., Forsmark A., Rossi G., Konopka C., Oyen M., Goksor M., Ronne H., Brennwald P., Adler L. 2006; The yeast tumor suppressor homologue Sro7p is required for targeting of the sodium pumping ATPase to the cell surface. Mol Biol Cell 17:4988–5003
     [Google Scholar]
  61. Withee J. L., Sen R., Cyert M. S. 1998; Ion tolerance of Saccharomyces cerevisiae lacking the Ca2+/CaM-dependent phosphatase (calcineurin) is improved by mutations in URE2 or PMA1. Genetics 149:865–878
     [Google Scholar]
  62. Yang X., Jiang R., Carlson M. 1994; A family of proteins containing a conserved domain that mediates interaction with the yeast SNF1 protein kinase complex. EMBO J 13:5878–5886
     [Google Scholar]
  63. Ye T., Garcia-Salcedo R., Ramos J., Hohmann S. 2006; Gis4, a new component of the ion homeostasis system in the yeast Saccharomyces cerevisiae . Eukaryot Cell 5:1611–1621
     [Google Scholar]
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The pathway by which the yeast protein kinase Snf1p controls acquisition of sodium tolerance is different from that mediating glucose regulation
Microbiology 154, 2814 (2008); https://doi.org/10.1099/mic.0.2008/020149-0
/content/journal/micro/10.1099/mic.0.2008/020149-0
/content/journal/micro/10.1099/mic.0.2008/020149-0
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