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Revista Latinoamericana de Microbiología

2000, Number 4

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Microbiología 2000; 42 (4)

Cation/Proton Exchangers in Yeast.

Ramírez J, Peña A

Language: Spanish
References: 121
Page: 181-187
PDF size: 78.30 Kb.


ABSTRACT

Cation/proton antiporters are membrane proteins found throughout the eukaryotic and prokaryotic kingdoms. These proteins exchange cations (Na + or K + ) for protons (H + ) across cytoplasmic and organelle membranes. They therefore link the electrochemical potential of the cations (DμNa + or DμK + ) and the hydrogen (DμH + ) ions, maintained across the biological membranes. The transmembrane ion cycle consists of two process, the formation of an electrochemical potential for a particular ion, followed by a reaction or reactions which recycle the ion back down its electrochemical gradient. These systems are central in the regulation of internal pH and prevent the excessive accumulation of monovalent cations in the cells. Here we review the various cation/proton antiporters that have been described in yeast cells and their properties.


REFERENCES

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  2. Bañuelos, M. A., H. Sychrova, C. Bleykasten-Grosshans, J. L. Souciet, and S. Potier. 1998. The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux. Microbiology 144:2749-2758.

  3. Brewster, J. L., T. de Valoir, N. D. Dwyer, E. Winter, and M. C. Gustin. 1993. An osmosensing signal transduction pathway in yeast. Science 259:1760-1763.

  4. Brierley, G. P. 1976. The uptake and extrusion of monovalent cations by isolated heart mitochondria. Mol. Cell. Biochem. 10:41-63.

  5. Camarasa, C., S. Prieto, R. Ros, J. M. Salmon, and P. Barre. 1996. Evidence for a selective and electroneutral K+/H+-exchanger in Saccharomyces cerevisiae using plasma membrane vesicles. Yeast 12:1301-1313.

  6. Dibrov, P., and Fliegel, L. 1998. Comparative molecular analysis of Na+/H+ exchangers: a unified model for Na+/H+ antiport? FEBS Lett. 424:1-5.

  7. Emilio M.G., and H. P. Menano. 1975. The excretion of hydrogen ion by the isolated amphibian skin: effects of antidiuretic hormone and amiloride. Biochim. Biophys. Acta 382:344-352.

  8. Fliegel, L., and O. Fröhlich. 1993. The Na+/H+ exchanger: an update on structure, regulation and cardiac physiology. Biochem. J. 296:273-285.

  9. Gaber, R. F., C. A. Styles, and G. R. Fink. 1988. TRK1 encodes a plasma membrane protein requiered for highaffinity potassium transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2848-2859.

  10. Gaxiola, R., I. F. 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.

  11. Glaser, H. U., D. Thomas, R. Gaxiola, F. Montrichard, Y. Surdin-Kerjan, and R. Serrano. 1993. Salt tolerance and methionine biosyntesis in Saccharomyces cerevisiae involve a putative phosphatase gene. EMBO J. 12:3105-3110.

  12. Haro, R., B. Garciadeblas, and A. Rodríguez-Navarro. 1991. A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett. 291:189-191.

  13. Harold, F. M., and D. Papineau. 1972. Cation transport and electrogenesis II proton and sodium extrusion. J. Membrane Biol. 8:45-62.

  14. http://genome-www.stanford.edu/Saccharomyces/

  15. Ivey, D. M., A. A. Guffanti, J. S. Bossewitch, E. Padan, and T. A. Krulwich. 1991. Molecular cloning and sequencing of a gene from alkaliphilic Bacillus firmus OF4 that functionally complements an Escherichia coli strain carrying a deletion in the nhaA Na+/H+ antiporter gene. J. Biol. Chem. 266:23483-23489.

  16. Jia, Z. P., N. McCullough, R. Martel, S. Hemmingsen, and P. G. Young. 1992. Gene amplification at a locus encoding a putative Na+/H+ antiporter confers sodium and litium tolerance in fission yeast. EMBO J. 11:1631-1640.

  17. Kakar, S. S., F. Mahdi, X. Li, and K. D. Garlid. 1989. Reconstitution of the mitochondrial non-selective Na+/H+ (K+/H+ ) antiporter into proteoliposomes. J. Biol. Chem. 264:5846-5851.

  18. Kinclová, O., S. Potier, and H. Sychrová. Functional study of the Saccharomyces cerevisiae plasma me mbrane antiporter Nha1. 18th Small Meeting on Yeast Transport and Energetics. Ouro Preto, Brasil; 14 al 17 de septiembre de 2000.

  19. Kleyman, T. R., C. Asher, E. J. Jr. Cragoe, and H. Garty. 1987. Effects of amiloride analogues on Na+ transport in toad bladder membrane vesicles. Evidence for two electrogenic transporters with different affinities toward pyrazinecarboxamides. J. Biol. Chem. Jun 262:8566-73.

  20. Ko, C. H., and R. F. Gaber. 1991. TRK1 and TRK2 encode structurally related K+ transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:4266-4273.

  21. Krulwich T. A. 1983. Na+/H+ antiporters. Biochim. Biophys. Acta 726:254-264.

  22. Maathuis F. J. M., and D. Sanders. 1992. Plant me mbrane transport. Curr. Opin. Cell Biol. 4:661-669.

  23. Marshall, C. J. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Op. Gen. Dev. 4:82-89.

  24. Malpartida, F., and R. Serrano. 1981. Proton translocation catalized by the purified yeast plasma membrane ATPase reconstituted in liposomes. FEBS Lett. 131:351-354.

  25. Manon, S., and M. Guérin. 1992. K+/H+ exchange in yeast mitochondria: sensitivity to inhibitors, solubilization ond reconstitution of the activity in proteoliposomes. Biochim. Biophys. Acta 1108:169-176.

  26. Masuda C. A., J. Ramírez, A. Peña, and M. Montero-Lomeli. 2000. Regulation of monovalent ion homeostasis and pH by the SER-THR protein phosphatase SIT4 in Saccharomyces cerevisiae. J. Biol. Chem. 275:30957-30961.

  27. Mitchell, P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191:144-148

  28. Mitchell, P., and J. Moyle. 1967. Acid-base titration across the membrane system of rat liver mitochondria. Biochem. J. 105:1147-1162.

  29. Mitchell, P., and J. Moyle. 1969. Translocation of some anions cations and acids in rat liver mitochondria. Eur. J. Bichem. 9:149-155.

  30. Munro, A. W., G. Y. Ritchi, A. J. Lamb, R. M. Douglas, and I. R. Booth. 1991. The cloning and DNA sequence of the gene for the glutathione-regulated potassium-

  31. efflux system KefC of Escherichia coli. Mol. Microbiol. 5:607-616.

  32. Mulet, J. M., M. P. Leube, S. J. Kron, G. Rios, G. R. Fink, and R. Serrano. 1999. A novel mechanism of ion homeostasis and salt tolerance in yeast: the Hal4 and Hal5 protein kinases modulate the Trk1-Trk2 potassium transporter. Mol. Cell. Biol. 19:3328-3337.

  33. Mürer, H., V. Hopfer, and R. Kinne. 1976. Sodium/proton antiport in brush-border-membrane vesicles is olated from rat small intestine and kidney. Biochem. J. 154:597-604.

  34. Navarre, C., and A. Goffeau. 2000. Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J. 19:2515-2525.

  35. Nass, R., K. W. Cunningham, and R. Rao. 1997. Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast enhanced by mutations in the plasma membrane H+-ATPase. J. Biol. Chem. 272:26145-26152.

  36. Nass, R., and R. Rao. 1998. Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast. J. Biol. Chem. 273:21054-21060.

  37. Numata, M., N. L. Petrecca, and J. Orlowski. 1998. Identification of a mitochondrial Na+/H+ exchanger. J. Biol. Chem. 273:6951-6959.

  38. Orlowski, J., and S. Grinstein. 1997. Na+/H+ exchangers of mammalian cells. J. Biol. Chem. 272:22373-22376.

  39. Paulsen, I. T., M. K. Sliwinski, B. Nelissen, A. Go ffeau, and M. H. Saier. 1998. Unified inventory of established and putative transporters encoded within the complete genome of Saccharomyces cerevisiae. FEBS Lett. 430:116-125.

  40. Padan, E., N. Maisler, D. Taglicht, R. Karpel, and S. Schuldiner. 1989. Deletion of ant in E. coli reveals its function in adaptation to high salinity and an alternative Na+/H+ antiporter system(s). J. Biol. Chem. 264:20297-30302.

  41. Padan, E., and S. Schuldiner. 1993. Na+/H+ antiporters, molecular devices that couple the Na+ and H+ circulation in cells. J. Bioener. Biomem. 25:647-669.

  42. Padan, E., and S. Schuldiner. 1994. Molecular physiology of Na+/H+ antiporters, key transporters in circulation of Na+ and H+ in cells. Biochim. Biophys. Acta 1185:129-151.

  43. Padan, E., and S. Schuldiner. 1994. Molecular phisiology of the Na+/H+ antiporter in Escherichia coli. J. Exp. Biol. 196:443-456.

  44. Padan, E., D. Zilberstein, and S. Schuldiner. 1981. pH homeostasis in bacteria. Biochim. Biophys. Acta 650:151-166.

  45. Peña, A., G. Cinco, A. Gómez-Puyou, and M. Tuena. 1972. Effects of the pH of the incubation medium on glycolysis and respiration in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 153:413-425.

  46. Peña, A., and J. Ramírez. 1991. An energy-dependent efflux system for potassium ions in yeast. Biochim. Biophys. Acta 1068:237-244.

  47. Pitts R. F. 1966. The renal metabolism of ammonia. Physiologist 9:97-109.

  48. Posas, F., S. M. Wurgler-Murphy, T. Maeda, E. A. Witten, T. C. Thai, and H. Saito. 1996. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “Twocomponent” osmosensor. Cell 86:865-875.

  49. Prior, C., S. Potier, J. L. Souciet, and H. Sychrova. 1996. Characterization of the NHA1 gene encoding a Na+/H+ antiporter of the yeast Saccharomyces cerevisiae. FEBS Lett. 387:89-93.

  50. Ramírez, J., A. Peña, and M. Montero-Lomelí. 1996. H+/K+ exchanger in reconstituted yeast plasma me mbrane vesicles. Biochim. Biophy. Acta 1285:175-182.

  51. Ramírez, J., O. Ramírez, C. Saldaña, R. Coria, and A. Peña. 1998. A Saccharomyces cerevisiae mutant lacking a K+/H+ exchanger. J. Bacteriol. 180:5860-5865.

  52. Rodríguez-Navarro, A., and J. Ramos. 1984. Dual system for potassium transport in Saccharomyces cerevisiae. J. Bacteriol. 159:940-945.

  53. Rodríguez-Navarro, A., and E. D. Sancho. 1979. Cation exchanges of yeast in the absence of magnesium. Biochim. Biophys. Acta 552:322-330.

  54. Rothstein, A. 1974. Relationship of cation influxes and effluxes in yeast. J. Gen. Physiol. 64:608-621.

  55. Serrano, R., M. C. Kielland-Brandt, and G. R. Fink. 1986. Yeast plasma membrane ATPase is essential for growth and has homology with (Na+/K+), K+- and Ca2+- ATPases. Nature 319:689-693.

  56. Serrano, R. 1996. Salt tolerance in plants and microorganisms: toxicity targets and defense mechanisms. Int. Rev. Cytol. 165:1-52.

  57. Supplement to Nature (1997) 387:issue No. 6632S.

  58. Sychrova, H., J. Ramírez, and A. Peña. 1999. Involvement of Nha1 antiporter in regulation of intracellular pH in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 171:167-172.

  59. Welihinda, A. A., R. J. Trumbly, K. D. Garlid, and A. D. Beavis. 1993. On the regulation of Na+/H+ and K+/ H+ antiport in yeast mitochondria: evidence for the absence of an Na+-selective Na+/H+ antiporter. Biochim. Biophys. Acta 1144:367-373.

  60. West, I. C., and P. Mitchell. 1974. Proton/sodium ion antiport in Escherichia coli. Biochem. J. 144:87-90.

  61. Whitlock, R.T., and H. O. Wheeler. 1969. Hydrogen ion transport by isolated rabbit gallbladder. Am. J. Physiol. 217:310-316.

  62. André, B. 1995. An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11:1575-1611.

  63. Bañuelos, M. A., H. Sychrova, C. Bleykasten-Grosshans, J. L. Souciet, and S. Potier. 1998. The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux. Microbiology 144:2749-2758.

  64. Brewster, J. L., T. de Valoir, N. D. Dwyer, E. Winter, and M. C. Gustin. 1993. An osmosensing signal transduction pathway in yeast. Science 259:1760-1763.

  65. Brierley, G. P. 1976. The uptake and extrusion of monovalent cations by isolated heart mitochondria. Mol. Cell. Biochem. 10:41-63.

  66. Camarasa, C., S. Prieto, R. Ros, J. M. Salmon, and P. Barre. 1996. Evidence for a selective and electroneutral K+/H+-exchanger in Saccharomyces cerevisiae using plasma membrane vesicles. Yeast 12:1301-1313.

  67. Dibrov, P., and Fliegel, L. 1998. Comparative molecular analysis of Na+/H+ exchangers: a unified model for Na+/H+ antiport? FEBS Lett. 424:1-5.

  68. Emilio M.G., and H. P. Menano. 1975. The excretion of hydrogen ion by the isolated amphibian skin: effects of antidiuretic hormone and amiloride. Biochim. Biophys. Acta 382:344-352.

  69. Fliegel, L., and O. Fröhlich. 1993. The Na+/H+ exchanger: an update on structure, regulation and cardiac physiology. Biochem. J. 296:273-285.

  70. Gaber, R. F., C. A. Styles, and G. R. Fink. 1988. TRK1 encodes a plasma membrane protein requiered for highaffinity potassium transport in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2848-2859.

  71. Gaxiola, R., I. F. 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.

  72. Glaser, H. U., D. Thomas, R. Gaxiola, F. Montrichard, Y. Surdin-Kerjan, and R. Serrano. 1993. Salt tolerance and methionine biosyntesis in Saccharomyces cerevisiae involve a putative phosphatase gene. EMBO J. 12:3105-3110.

  73. Haro, R., B. Garciadeblas, and A. Rodríguez-Navarro. 1991. A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett. 291:189-191.

  74. Harold, F. M., and D. Papineau. 1972. Cation transport and electrogenesis II proton and sodium extrusion. J. Membrane Biol. 8:45-62.

  75. http://genome-www.stanford.edu/Saccharomyces/

  76. Ivey, D. M., A. A. Guffanti, J. S. Bossewitch, E. Padan, and T. A. Krulwich. 1991. Molecular cloning and sequencing of a gene from alkaliphilic Bacillus firmus OF4 that functionally complements an Escherichia coli strain carrying a deletion in the nhaA Na+/H+ antiporter gene. J. Biol. Chem. 266:23483-23489.

  77. Jia, Z. P., N. McCullough, R. Martel, S. Hemmingsen, and P. G. Young. 1992. Gene amplification at a locus encoding a putative Na+/H+ antiporter confers sodium and litium tolerance in fission yeast. EMBO J. 11:1631-1640.

  78. Kakar, S. S., F. Mahdi, X. Li, and K. D. Garlid. 1989. Reconstitution of the mitochondrial non-selective Na+/H+ (K+/H+ ) antiporter into proteoliposomes. J. Biol. Chem. 264:5846-5851.

  79. Kinclová, O., S. Potier, and H. Sychrová. Functional study of the Saccharomyces cerevisiae plasma me mbrane antiporter Nha1. 18th Small Meeting on Yeast Transport and Energetics. Ouro Preto, Brasil; 14 al 17 de septiembre de 2000.

  80. Kleyman, T. R., C. Asher, E. J. Jr. Cragoe, and H. Garty. 1987. Effects of amiloride analogues on Na+ transport in toad bladder membrane vesicles. Evidence for two electrogenic transporters with different affinities toward pyrazinecarboxamides. J. Biol. Chem. Jun 262:8566-73.

  81. Ko, C. H., and R. F. Gaber. 1991. TRK1 and TRK2 encode structurally related K+ transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:4266-4273.

  82. Krulwich T. A. 1983. Na+/H+ antiporters. Biochim. Biophys. Acta 726:254-264.

  83. Maathuis F. J. M., and D. Sanders. 1992. Plant me mbrane transport. Curr. Opin. Cell Biol. 4:661-669.

  84. Marshall, C. J. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Op. Gen. Dev. 4:82-89.

  85. Malpartida, F., and R. Serrano. 1981. Proton translocation catalized by the purified yeast plasma membrane ATPase reconstituted in liposomes. FEBS Lett. 131:351-354.

  86. Manon, S., and M. Guérin. 1992. K+/H+ exchange in yeast mitochondria: sensitivity to inhibitors, solubilization ond reconstitution of the activity in proteoliposomes. Biochim. Biophys. Acta 1108:169-176.

  87. Masuda C. A., J. Ramírez, A. Peña, and M. Montero-Lomeli. 2000. Regulation of monovalent ion homeostasis and pH by the SER-THR protein phosphatase SIT4 in Saccharomyces cerevisiae. J. Biol. Chem. 275:30957-30961.

  88. Mitchell, P. 1961. Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191:144-148

  89. Mitchell, P., and J. Moyle. 1967. Acid-base titration across the membrane system of rat liver mitochondria. Biochem. J. 105:1147-1162.

  90. Mitchell, P., and J. Moyle. 1969. Translocation of some anions cations and acids in rat liver mitochondria. Eur. J. Bichem. 9:149-155.

  91. Munro, A. W., G. Y. Ritchi, A. J. Lamb, R. M. Douglas, and I. R. Booth. 1991. The cloning and DNA sequence of the gene for the glutathione-regulated potassium-efflux system KefC of Escherichia coli. Mol. Microbiol. 5:607-616.

  92. Mulet, J. M., M. P. Leube, S. J. Kron, G. Rios, G. R. Fink, and R. Serrano. 1999. A novel mechanism of ion homeostasis and salt tolerance in yeast: the Hal4 and Hal5 protein kinases modulate the Trk1-Trk2 potassium transporter. Mol. Cell. Biol. 19:3328-3337.

  93. Mürer, H., V. Hopfer, and R. Kinne. 1976. Sodium/proton antiport in brush-border-membrane vesicles is olated from rat small intestine and kidney. Biochem. J. 154:597-604.

  94. Navarre, C., and A. Goffeau. 2000. Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J. 19:2515-2525.

  95. Nass, R., K. W. Cunningham, and R. Rao. 1997. Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast enhanced by mutations in the plasma membrane H+-ATPase. J. Biol. Chem. 272:26145-26152.

  96. Nass, R., and R. Rao. 1998. Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast. J. Biol. Chem. 273:21054-21060.

  97. Numata, M., N. L. Petrecca, and J. Orlowski. 1998. Identification of a mitochondrial Na+/H+ exchanger. J. Biol. Chem. 273:6951-6959.

  98. Orlowski, J., and S. Grinstein. 1997. Na+/H+ exchangers of mammalian cells. J. Biol. Chem. 272:22373-22376.

  99. Paulsen, I. T., M. K. Sliwinski, B. Nelissen, A. Go ffeau, and M. H. Saier. 1998. Unified inventory of established and putative transporters encoded within the complete genome of Saccharomyces cerevisiae. FEBS Lett. 430:116-125.

  100. Padan, E., N. Maisler, D. Taglicht, R. Karpel, and S. Schuldiner. 1989. Deletion of ant in E. coli reveals its function in adaptation to high salinity and an alternative Na+/H+ antiporter system(s). J. Biol. Chem. 264:20297-30302.

  101. Padan, E., and S. Schuldiner. 1993. Na+/H+ antiporters, molecular devices that couple the Na+ and H+ circulation in cells. J. Bioener. Biomem. 25:647-669.

  102. Padan, E., and S. Schuldiner. 1994. Molecular physiology of Na+/H+ antiporters, key transporters in circulation of Na+ and H+ in cells. Biochim. Biophys. Acta 1185:129-151.

  103. Padan, E., and S. Schuldiner. 1994. Molecular phisiology of the Na+/H+ antiporter in Escherichia coli. J. Exp. Biol. 196:443-456.

  104. Padan, E., D. Zilberstein, and S. Schuldiner. 1981. pH homeostasis in bacteria. Biochim. Biophys. Acta 650:151-166.

  105. Peña, A., G. Cinco, A. Gómez-Puyou, and M. Tuena. 1972. Effects of the pH of the incubation medium on glycolysis and respiration in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 153:413-425.

  106. Peña, A., and J. Ramírez. 1991. An energy-dependent efflux system for potassium ions in yeast. Biochim. Biophys. Acta 1068:237-244.

  107. Pitts R. F. 1966. The renal metabolism of ammonia. Physiologist 9:97-109.

  108. Posas, F., S. M. Wurgler-Murphy, T. Maeda, E. A. Witten, T. C. Thai, and H. Saito. 1996. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “Twocomponent” osmosensor. Cell 86:865-875.

  109. Prior, C., S. Potier, J. L. Souciet, and H. Sychrova. 1996. Characterization of the NHA1 gene encoding a Na+/H+ antiporter of the yeast Saccharomyces cerevisiae. FEBS Lett. 387:89-93.

  110. Ramírez, J., A. Peña, and M. Montero-Lomelí. 1996. H+/K+ exchanger in reconstituted yeast plasma me mbrane vesicles. Biochim. Biophy. Acta 1285:175-182.

  111. Ramírez, J., O. Ramírez, C. Saldaña, R. Coria, and A. Peña. 1998. A Saccharomyces cerevisiae mutant lacking a K+/H+ exchanger. J. Bacteriol. 180:5860-5865.

  112. Rodríguez-Navarro, A., and J. Ramos. 1984. Dual system for potassium transport in Saccharomyces cerevisiae. J. Bacteriol. 159:940-945.

  113. Rodríguez-Navarro, A., and E. D. Sancho. 1979. Cation exchanges of yeast in the absence of magnesium. Biochim. Biophys. Acta 552:322-330.

  114. Rothstein, A. 1974. Relationship of cation influxes and effluxes in yeast. J. Gen. Physiol. 64:608-621.

  115. Serrano, R., M. C. Kielland-Brandt, and G. R. Fink. 1986. Yeast plasma membrane ATPase is essential for growth and has homology with (Na+/K+), K+- and Ca2+- ATPases. Nature 319:689-693.

  116. Serrano, R. 1996. Salt tolerance in plants and microorganisms: toxicity targets and defense mechanisms. Int. Rev. Cytol. 165:1-52.

  117. Supplement to Nature (1997) 387:issue No. 6632S.

  118. Sychrova, H., J. Ramírez, and A. Peña. 1999. Involvement of Nha1 antiporter in regulation of intracellular pH in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 171:167-172.

  119. Welihinda, A. A., R. J. Trumbly, K. D. Garlid, and A. D. Beavis. 1993. On the regulation of Na+/H+ and K+/ H+ antiport in yeast mitochondria: evidence for the absence of an Na+-selective Na+/H+ antiporter. Biochim. Biophys. Acta 1144:367-373.

  120. West, I. C., and P. Mitchell. 1974. Proton/sodium ion antiport in Escherichia coli. Biochem. J. 144:87-90.

  121. Whitlock, R.T., and H. O. Wheeler. 1969. Hydrogen ion transport by isolated rabbit gallbladder. Am. J. Physiol. 217:310-316.




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