A novel mechanism of ion homeostasis and salt tolerance in yeast: The Hal4 and Hal5 protein kinases modulate the Trk1-Trk2 potassium transporter

Molecular and Cellular Biology

Volumn 19, Issue 5, 1999, Pages 3328-3337

  Mulet, Jose M ^a   Leube, Martin P ^a,c   Kron, Stephen J ^b,d   Rios, Gabino ^a   Fink, Gerald R ^b   Serrano, Ramon ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c PlantTec Biotechnologie GmbH   (Germany)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; HYGROMYCIN B; LITHIUM; POTASSIUM; PROTEIN KINASE; SODIUM; TETRAMETHYLAMMONIUM;

ARTICLE; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; ENZYME REGULATION; GENE DISRUPTION; GENE DOSAGE; GENE ISOLATION; GENE OVEREXPRESSION; HOMEOSTASIS; HYPERPOLARIZATION; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; REGULATORY MECHANISM; SODIUM BALANCE; YEAST;

SACCHAROMYCES CEREVISIAE;

EID: 0032931992     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.5.3328     Document Type: Article

References (79)

1. Alepuz, P. M., K. W. Cunningham, and F. Estruch. 1997. Glucose repression affects ion homeostasis in yeast through the regulation of the stress-activated ENA1 gene. Mol. Microbiol. 26:91-98.
2. André, B. 1995. An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11:1575-1611.
3. +-ATPase activity in renal tubule cells. Proc. Natl. Acad. Sci. USA 89:7394-7397.
4. Benito, B., F. Portillo, and R. Lagunas. 1992. In vivo activation of the yeast plasma membrane ATPase during nitrogen starvation. Identification of the regulatory domain that controls activation. FEBS Lett. 300:271-274.
5. Broach, J. R., J. N. Strathern, and J. B. Hicks. 1979. Transformation in yeast: development of a hybrid cloning vector and isolation of the CAN1 gene. Gene 8:121-133.
6. +-ATPase gene is controlled by the promoter binding factor TUF. J. Biol. Chem. 264:7437-7446.
7. Carlson, M., and D. Botstein. 1982. Two differentially regulated mRNAs with different 5′ ends encode secreted and intracellular forms of yeast invertase. Cell 28:145-154.
8. 2+ ATPases in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2226-2237.
9. Dichtl, B., A. Stevens, and D. Tollervey. 1997. Lithium toxicity in yeast is due to inhibition of RNA processing enzymes. EMBO J. 16:7184-7195.
10. Epstein, W. 1986. Osmoregulation by potassium transport in Escherichia coli. FEMS Microbiol. Rev. 39:73-78.
11. +-ATPase by glucose. Interactions between domains and identification of new regulatory sites. J. Biol. Chem. 269:10393-10399.
12. +-ATPase by casein kinase I. J. Biol. Chem. 271:32064-32072.
13. Ferrando, A., S. J. Kron, G. Rios, G. R. Fink, and R. Serrano. 1995. Regulation of cation transport in Saccharomyces cerevisiae by the salt tolerance gene HAL3. Mol. Cell. Biol. 15:5470-5481.
14. Gaber, R. F., C. A. Styles, and G. R. Fink. 1988. TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2848-2859.
15. Galcheva-Gargova, Z., B. Derijard, I.-H. Wu, and R. J. Davis. 1994. An osmosensing signal transduction pathway in mammalian cells. Science 265: 806-808.
16. +-ATPase by glucose. Cloning and characterization of a new gene involved in its regulation. J. Biol. Chem. 269:18076-18082.
17. Garciadeblas, B., F. Rubio, F. J. Quintero, M. A. Bañuelos, R. Haro, and A. Rodriguez-Navarro. 1993. Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol. Gen. Genet. 236:363-368.
18. Gaxiola, R., I. F. de Larrinoa, J. M. Villalba, and R. Serrano. 1992. A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J. 11:3157-3164.
19. Gläser, H.-U., D. Thomas, R. Gaxiola, F. Montrichard, Y. Surdin-Kerjan, and R. Serrano. 1993. Salt tolerance and methionine biosynthesis in Saccharomyces cerevisiae involve a putative phosphatase gene. EMBO J. 12:3105-3110.
20. Gomez, M. J., K. Luyten, and J. Ramos. 1996. The capacity to transport potassium influences sodium tolerance in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 135:157-160.
21. Gustin, M. C., X.-L. Zhou, B. Martinac, and C. Kung. 1988. A mechano-sensitive ion channel in the yeast plasma membrane. Science 242:762-765.
22. Guthrie, C., and G. R. Fink (ed.). 1991. Guide to yeast genetics and molecular biology. Academic Press, Inc., New York, N.Y.
23. Haro, R., B. Garciadeblas, and A. Rodriguez-Navarro. 1991. A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett. 291:189-191.
24. Haro, R., M. A. Bañuelos, F. J. Quintero, F. Rubio, and A. Rodriguez-Navarro. 1993. Genetic basis of sodium exclusion and sodium tolerance in yeast. A model for plants. Physiol. Plant. 89:868-874.
25. Hein, C., J.-Y. Springael, C. Volland, R. Haguenauer-Tsapis, and B. André. 1995. NPI1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:77-87.
26. Hill, J. E., A. M. Myers, T. J. Koerner, and A. Tzagoloff. 1986. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2:163-167.
27. Hunter, T., and G. D. Plowman. 1997. The protein kinases of budding yeast: six score and more. Trends Biochem. Sci. 22:14-22.
28. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
29. Jones, J. S., and L. Prakash. 1990. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast 6:363-366.
30. Kaouass, M., M. Audette, D. Ramotar, S. Verma, D. de Montigny, I. Gamache, K. Torossian, and R. Poulin. 1997. The STK2 gene, which encodes a putative Ser/Thr protein kinase, is required for high-affinity spermidine transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:2994-3004.
31. Kakimura, Y., T. Maruyama, T. Nozaki, Y. Wada, Y. Ohsumi, and K. Igarashi. 1995. Cloning of the gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 216:985-992.
32. + transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 4266-4273.
33. Ko, C. H., and R. F. Gaber. 1993. Roles of multiple glucose transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:638-648.
34. Kwon, H. M., and J. S. Handler. 1995. Cell volume regulated transporters of compatible osmolytes. Curr. Opin. Cell Biol. 7:465-471.
35. + uptake in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:926-935.
36. Lifton, R. P. 1996. Molecular genetics of human blood pressure variation. Science 272:676-680.
37. Liu, H., J. Krizek, and A. Bretscher. 1992. Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics 132:665-673.
38. Lodish, H., D. Baltimore, A. Berk, S. L. Zipursky, P. Matsudaira, and J. Darnell. 1995. Molecular cell biology, p. 633-668. W. H. Freeman & Co., New York, N.Y.
39. Madrid, R., M. J. Gomez, J. Ramos, and A. Rodriguez-Navarro. 1998. Ectopic potassium uptake in trk1 trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential. J. Biol. Chem. 273:14838-14844.
40. Marquez, J. A., and R. Serrano. 1996. Multiple transduction pathways regulate the sodium-extrussion gene PMR2/ENA1 during salt stress. FEBS Lett. 382:89-92.
41. Matheos, D. P., T. J. Kinsbury, U. S. Ahsan, and K. W. Cunningham. 1997. Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev. 11:3445-3458.
42. McCusker, J. H., D. Perlin, and J. E. Haber. 1987. Pleiotropic plasma membrane ATPase mutations of Saccharomyces cerevisiae. Mol. Cell. Biol. 7: 4082-4088.
43. Mendizabal, I., G. Ríos, J. M. Mulet, R. Serrano, and I. F. de Larrinoa. 1998. Yeast putative transcription factors involved in salt tolerance. FEBS Lett. 425:323-328.
44. Mendoza, I., F. Rubio, A. Rodriguez-Navarro, and J. M. Pardo. 1994. The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J. Biol. Chem. 269:8792-8796.
45. Mewes, H. W., K. Albermann, M. Bähr, D. Frishman, A. Gleissner, J. Hani, K. Heumann, K. Kleine, A. Maieri, S. G. Oliver, F. Pfeiffer, and A. Zollner. 1997. Overview of the yeast genome. Nature 387(Suppl.):7-61.
46. Murguía, J. R., J. M. Bellés, and R. Serrano. 1995. A salt-sensitive 3′(2′),5′-bisphosphate nucleotidase involved in sulfate activation. Science 267:232-234.
47. Murguía, J. R., J. M. Bellés, and R. Serrano. 1996. The yeast HAL2 nucleotidase is an in vivo target of salt toxicity. J. Biol. Chem. 271:29029-29033.
48. Nadal, E., J. Clotet, F. Posas, R. Serrano, N. Gomez, and J. Ariño. 1998. The yeast halotolerance determinant Hal3p is an inhibitory subunit of the Ppz1p Ser/Thr protein phosphatase. Proc. Natl. Acad. Sci. USA 95:7357-7362.
49. Nakamura, T., Y. Liu, D. Hirata, H. Namba, S. Harada, T. Hirokawa, and T. Miyakawa. 1993. Protein phosphatase type 2B (calcineurin)-mediated, FK-506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J. 12:4063-4071.
50. Nozaki, T., K. Nishimura, A. J. Michael, T. Maruyama, Y. Kakinuma, and K. Igarashi. 1996. A second gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 228:452-458.
51. Perlin, D., C. Brown, and J. E. Haber. 1988. Membrane potential defect in hygromycin B-resistant mutants of Saccharomyces cerevisiae. J. Biol. Chem. 263:18118-18122.
52. +-ATPase and identification of a regulatory domain at the carboxyl-terminus. FEBS Lett. 247:381-385.
53. Posas, F., M. Camps, and J. Ariño. 1995. The PPZ protein phosphatases are important determinants of salt tolerance in yeast cells. J. Biol. Chem. 270: 13036-13041.
54. Proft, M., and R. Serrano. 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.
55. Ramos, J., R. Haro, and A. Rodriguez-Navarro. 1990. Regulation of potassium fluxes in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1029:211-217.
56. Ramos, J., R. Alijo, R. Haro, and A. Rodriguez-Navarro. 1994. TRK2 is not a low-affinity potassium transporter in Saccharomyces cerevisiae. J. Bacteriol. 176:249-252.
57. Rios, G., A. Ferrando, and R. Serrano. 1997. Mechanisms of salt tolerance conferred by overexpression of the HAL1 gene in Saccharomyces cerevisiae. Yeast 13:515-528.
58. Robinson, L. C., E. J. A. Hubbard, P. R. Graves, A. A. DePaoli-Roach, P. J. Roach, C. Kung, D. W. Haas, C. H. Hagedorn, M. Goebl, M. R. Culbertson, and M. Carlson. 1992. Yeast casein kinase I homologues: an essential gene pair. Proc. Natl. Acad. Sci. USA 89:28-32.
59. Rothstein, A. 1964. Membrane function and physiological activity of microorganisms, p. 23-39. In J. F. Hoffman (ed.), The cellular functions of membrane transport. Prentice-Hall, Englewood Cliffs, N.J.
60. Saccharomyces Genome Database. http://genome-www.stanford.edu/Saccharomyces/.
61. Serrano, R. 1983. In vivo glucose activation of yeast plasma membrane ATPase. FEBS Lett. 156:11-14.
62. Serrano, R. 1989. Structure and function of plasma membrane ATPase. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:61-94.
63. Serrano, R. 1991. Transport across yeast vacuolar and plasma membranes, p. 523-585. In J. R. Broach, E. W. Jones and J. R. Pringle (ed.), The molecular and cellular biology of the yeast Saccharomyces. Genomic dynamics, protein synthesis and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
64. Serrano, R. 1996. Salt tolerance in plants and microorganisms: toxicity targets and defense mechanisms. Int. Rev. Cytol. 165:1-52.
65. Siderius, M., and W. H. Mager. 1997. General stress response: in search of a common denominator, p. 213-230. In S. Hohmann and W. H. Mager (ed.), Yeast stress responses. Springer-Verlag KG, Berlin, Germany.
66. Skala, J., B. Purnelle, M. Crouzet, M. Aigle, and A. Goffeau. 1991. The open reading frame YCR101 located on chromosome III from Saccharomyces cerevisiae is a putative protein kinase. Yeast 7:651-655.
67. Stanbrough, M., and B. Magasanik. 1995. Transcriptional and posttranscriptional regulation of the general amino-acid permease of Saccharomyces cerevisiae. J. Bacteriol. 177:94-102.
68. Stathopoulos, A., and M. S. Cyert. 1997. Calcineurin acts through the CRZ1/ TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev. 11:3432-3444.
69. Stein, W. D. 1990. Channels, carriers, and pumps. An introduction to membrane transport. Academic Press, Inc., New York, N.Y.
70. +-ATPase. Yeast 5:307-319.
71. Vandenbol, M., J.-C. Jauniaux, and M. Grenson. The Saccharomyces cerevisiae NPR1 gene required for the activity of ammonia-sensitive amino acid permeases encode a protein kinase homologue. Mol. Gen. Genet. 222:393-399.
72. +-ATPase. J. Biol. Chem. 270: 19659-19667.
73. Wach, A., A. Brachat, R. Pohlmann, and P. Philippsen. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793-1808.
74. Wallis, J. W., G. Chrebet, G. Brodsky, M. Rolfe, and R. Rothstein. 1989. A hyperrecombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58:409-419.
75. + pump in the yeast plasma membrane. EMBO J. 14:3870-3882.
76. 2+/CaM-dependent phosphatase (calcineurin) is improved by mutations in URE2 or PMA1. Genetics 149:865-878.
77. Wright, M. B., J. Ramos, M. J. Gomez, K. Moulder, M. Scherrer, G. Munson, and R. F. Gaber. 1997. Potassium transport by amino acid permeases in Saccharomyces cerevisiae. J. Biol. Chem. 272:13647-13652.
78. Wurgler-Murphy, S. M., and H. Saito. 1997. Two-component signal transducers and MAPK cascades. Trends Biochem. Sci. 22:172-176.
79. Wyn Jones, R. G., and A. Pollard. 1983. Proteins, enzymes and inorganic ions, p. 528-562. In A. Laüchli and A. Pirson (ed.), Encyclopedia of plant physiology, new series, vol. 15B. Springer, Berlin, Germany.