Chloride homeostasis in Saccharomyces cerevisiae: High affinity influx, V-ATPase-dependent sequestration, and identification of a candidate Cl - sensor

Journal of General Physiology

Volumn 131, Issue 4, 2008, Pages 379-391

  Jennings, Michael L ^a   Cui, Jian ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BICARBONATE; BROMIDE ION; CARRIER PROTEIN; CHLORIDE ION; FORMIC ACID; NITRATE; SULFATE; WATER;

ACIDIFICATION; ARTICLE; CELL MEMBRANE; CHLORIDE TRANSPORT; CULTURE MEDIUM; FUNGAL CELL; FUNGUS CULTURE; GENE DELETION; NONHUMAN; OPEN READING FRAME; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; STEADY STATE;

BICARBONATES; BIOLOGICAL TRANSPORT, ACTIVE; BROMIDES; CELL MEMBRANE; CHLORIDES; CULTURE MEDIA; HOMEOSTASIS; HYDROGEN-ION CONCENTRATION; KINETICS; LIGANDS; NITRATES; OSMOLAR CONCENTRATION; RADIOISOTOPES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; SULFITES; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES;

EID: 41649117596     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200709905     Document Type: Article

References (76)

1. - channels. Nature. 427:803-807.
2. + exchanger. J. Gen. Physiol. 126:563-570.
3. 3 exchangers. J. Nephrol. 15:S41-S53.
4. - cotransporter family. Biochem. Biophys. Res. Commun. 217:150-153.
5. Ballarin-Denti, A., C.L. Slayman, and H. Kuroda. 1994. Small lipid-soluble cations are not membrane voltage probes for Neurospora or Saccharomyces. Biochim. Biophys. Acta. 1190:43-56.
6. Bertl, A., E. Blumwald, R. Coronado, R. Eisenberg, G. Findlay, D. Gradmann, B. Hille, K. Köhler, H.A. Kolb, E. MacRobbie, et al. 1992. Electrical measurements on endomembranes. Science. 258:873-874.
7. Bertl, A., and C.L. Slayman. 1990. Cation-selective channels in the vacuolar membrane of Saccharomyces: dependence on calcium, redox state, and voltage. Proc. Natl. Acad. Sci. USA. 87:7824-7828.
8. - across the tonoplast of the green alga Eremoshpaera viridis. Plant Physiol. 109:1317-1326.
9. +-independent current. FEBS Lett. 447:115-120.
10. Cherest, H., J.C. Davidian, D. Thomas, V. Benes, W. Ansorge, and Y. Surdin-Kerjan. 1997. Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics. 145:627-635.
11. Chuang, S.-M., L. Chen, D. Lambertson, M. Anand, T.G. Kinzy, and K. Madura. 2005. Proteasome-mediated degradation of contranslattionally damaged proteins involves translation elongation factor 1A. Mol. Cell. Biol. 25:403-413.
12. Conway, E.J., and M. Downey. 1950. An outer metabolic region of the yeast cell. Biochem. J. 47:347-355.
13. Cookson, S.J., L.E. Williams, and A.J. Miller. 2005. Light-dark changes in cytosolic nitrate pools depend on nitrate reductase activity in Arabidopsis leaf cells. Plant Physiol. 138:1097-1105.
14. Coury, L.A., J.E.M. McGeoch, G. Guidotti, and J.L. Brodsky. 1999. The yeast Saccharomyces cerevisiae does not sequester chloride but can express a functional mammalian chloride channel. FEMS Microbiol. Lett. 179:327-332.
15. Davis-Kaplan, S.R., C.C. Askwith, A.C. Bengtzen, D. Radisky, and J. Kaplan. 1998. Chloride is an allosteric effector of copper assembly for the yeast multicopper oxidase Fet3p: an unexpected role for intraellular chloride channels. Proc. Natl. Acad. Sci. USA. 95:13641-13645.
16. De Angeli, A., D. Monachello, G. Ephritikhine, J.M. Frachisse, S. Thomine, F. Gamale, and H. Barbier-Brygoo. 2006. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature. 442:939-942.
17. Deloménie, C., E. Foti, E. Flock, V. Diderot, D. Porquet, C. Dupuy, and J. Bonaly. 2007. A new homolog of FocA transporters identified in cadmium-resistant Euglena gracilis. Biochem. Biophys. Res. Commun. 358:455-461.
18. Dunham, P.B., G.W. Stewart, and J.C. Ellory. 1980. Chloride-activated passive potassium transport in human erythrocytes. Proc. Natl. Acad. Sci. USA. 77:1711-1715.
19. Dutzler, R., E.B. Campbell, M. Cadene, B.T. Chait, and R. MacKinnon. 2002. X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature. 415:287-294.
20. Dutzler, R., E.B. Campbell, and R. MacKinnon. 2003. Gating the selectivity filter in ClC chloride channels. Science. 300:108-112.
21. Flis, K., P. Bednarczyk, R. Hordejuk, A. Szewczyk, V. Berest, K. Dolowy, A. Edelman, and A. Kurlandzka. 2002. The Gef1 protein of Saccharomyces cerevisiae is associated with chloride channel activity. Biochem. Biophys. Res. Commun. 294:1144-1150.
22. +)-ATPases. J. Biol. Chem. 274:12951-12954.
23. Forsberg, H., and P.O. Ljungdahl. 2001. Sensors of extracellular nutrients in Saccharomyces cerevisiae. Curr. Genet. 40:91-109.
24. Forte, M., D. Adelsberger-Mangan, and M. Colombini. 1987. Purification and characterization of the voltage-dependent anion channel from the outer mitochondrial membrane of yeast. J. Membr. Biol. 99:65-72.
25. Fröhlich, O., and R.B. Gunn. 1986. Erythrocyte anion transport: the kinetics of a single-site obligatory exchange system. Biochim. Biophys. Acta. 864:169-194.
26. Gamba, G. 2005. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol. Rev. 85:423-493.
27. Gaxiola, R.A., R. Rao, A. Sherman, P. Grisafi, S.L. Alper, and G.R. Fink. 1999. The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci. USA. 96:1480-1485.
28. Gaxiola, R.A., D.S. Yuan, R.D. Klausner, and G.R. Flink. 1998. The yeast CLC chloride channel functions in cation homeostasis. Proc. Natl. Acad. Sci. USA. 95:4046-4050.
29. Gillen, C.M., and B. Forbush. 1999. Functional interaction of the K-Cl cotransporter (KCC1) with the Na-K-Cl cotransporter in HEK-293 cells. Am. J. Physiol. 276:C328-C336.
30. Greene, J.R., N.H. Brown, B.J. DiDomenico, J. Kaplan, and D.J. Eide. 1993. The GEF1 gene of Saccharomyces cerevisiae encodes an integral membrane protein; mutations in which have effects on respiration and iron-limited growth. Mol. Gen. Genet. 241:542-553.
31. Groves, J.D., P. Falson, M. LeMaire, and M.J.A. Tanner. 1996. Functional cell surface expression of the anion transport domain of human red cell band 3 (AE1) in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 93:12245-12250.
32. Gunn, R.B., M. Dalmark, D.C. Tosteson, and J.O. Wieth. 1973. Characteristics of chloride transport in human red blood cells. J. Gen. Physiol. 61:185-206.
33. Gustin, M.C., B. Martinac, Y. Saimi, M.R. Culbertson, and C. Kung. 1986. Ion channels in yeast. Science. 233:1195-1200.
34. Haas, M., and B. Forbush. 1998. The Na-K-Cl cotransporters. J. Bioenerg. Biomembr. 30:161-172.
35. Hess, D.C., W. Lu, J.D. Rabinowitz, and D. Botstein. 2006. Ammonium toxicity and potasssium limitation in yeast. PLoS Biol. 4:e351.
36. Huh, W.-K., J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O' Shea. 2003. Global analysis of protein localization in budding yeast. Nature. 425:686-691.
37. Isenring, P., S.C. Jacoby, J.A. Payne, and B. Forbush. 1998. Comparison of Na-K-Cl cotransporters. NKCC1, NKCC2, and the HEK cell Na-K-Cl cotransporters. J. Biol. Chem. 273:11295-11301.
38. Jennings, M.L., T.R. Howren, J. Cui, M. Winters, and R. Hannigan. 2007. Transport and regulatory characteristics of the yeast bicarbonate transporter homolog Bor1p. Am. J. Physiol. Cell Physiol. 293:C468-476.
39. Jentsch, T.J., T. Friedrich, A. Schriever, and H. Yamada. 1999. The CLC chloride channel family. Pflugers. Arch. 437:783-795.
40. Jentsch, T.J., V. Stein, F. Weinreich, and A.A. Zdebik. 2002. Molecular structure and physiological function of chloride channels. Physiol. Rev. 82:503-568.
41. Jiang, Q., D. Mak, S. Devidas, E.M. Schweibert, A. Bragin, Y. Zhang, W.R. Skach, W.B. Guggino, J.K. Foskett, and J.F. Engelhardt. 1998. Cystic fibrosis transmembrane conductance regulator-associated ATP release is controlled by a chloride sensor. J. Cell Biol. 143:645-657.
42. +-ATPase. Microbiol. Mol. Biol. Rev. 70:177-191.
43. + transporters in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:4266-4273.
44. Kuroda, T., H. Bihler, E. Bashi, C.L. Slayman, and A. Rivetta. 2004. Chloride channel function in the yeast TRK-potassium transporters. J. Membr. Biol. 198:177-192.
45. 2+); level and pump-leak turnover in intact red cells measured using an incorporated Ca chelator. Nature. 298:478-481.
46. - across the plasma membrane. FEMS Yeast Res. 7:1218-1229.
47. Lu, J., M. Karadsheh, and E. Delpire. 1999. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J. Neurobiol. 39:558-568.
48. Lue, N.F., and R.D. Kornberg. 1987. Accurate initiation at RNA polymerase II promoters in extracts from Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 84:8839-8843.
49. Lytle, C., and B. Forbush. 1996. Regulatory phosphorylation of the secretory Na-K-Cl cotransporter: modulation by cytoplasmic Cl. Am. J. Physiol. 270:C437-C448.
50. Lytle, C., and T. McManus. 2002. Coordinate modulation of Na-K-2Cl cotransport and K-Cl cotransport by cell volume and chloride. Am. J. Physiol. Cell Physiol. 283:C1422-C1431.
51. 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.
52. Makuc, J., S. Paiva, M. Schauen, R. Krämer, B. André, M. Casal, C. Leão, and E. Boles. 2001. The putative monocarboxylate permeases of the yeast Saccharomyces cerevisiae do not transport monocarboxylic acids across the plasma membrane. Yeast. 18:1131-1143.
53. +-ATPase. Biochim. Biophys. Acta. 1469:133-157.
54. +-ATPase. J. Biol. Chem. 272:26145-26152.
55. + exchanger in a late endosomal compartment of yeast. Implications for vacuole biogenesis. J. Biol. Chem. 273:21054-21060.
56. + exchanger, Nhx1, confers osmotolerance following acute hypertonic shock. Microbiology. 145:3221-3228.
57. Plant, P.J., M.F. Manolson, S. Grinstein, and N. Demaurex. 1999. Alternative mechanisms of vacuolar acidification in H(+)-ATPase-deficient yeast. J. Biol. Chem. 274:37270-37279.
58. Preston, R.A., R.F. Murphy, and E.W. Jones. 1989. Assay of vacuolar pH in yeast and identification of acidification-defective mutants. Proc. Natl. Acad. Sci. USA. 86:7027-7031.
59. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature. 397:251-255.
60. Rivetta, A., C. Slayman, and T. Kuroda. 2005. Quantitative modeling of chloride conductance in yeast TRK potassium transporters. Biophys. J. 89:2412-2426.
61. Rodriguez-Navarro, A., and J. Ramos. 1984. Dual system for potassium transport in Saccharomyces cerevisiae. J. Bacteriol. 159:940-945.
62. - transporters. Pflugers. Arch. 447:495-509.
63. Roomans, G.M., G.A.J. Kuypers, A.P.R. Theuvenet, and G.W.F.H. Borst-Pauwels. 1979. Kinetics of sulfate uptake by yeast. Biochim. Biophys. Acta. 551:197-206.
64. Rothstein, A. 1974. Relationship of cation influxes and effluxes in yeast. J. Gen. Physiol. 64:608-621.
65. Russell, J.M. 2000. Sodium-potassium-chloride cotransport. Physiol. Rev. 80:211-276.
66. 2 and COOH terminus of the yeast ClC putative chloride channel Gef1p. J. Biol. Chem. 273:15110-15118.
67. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
68. Soleimani, M., and J. Xu. 2006. SLC26 chloride/base exchangers in the kidney in health and disease. Semin. Nephrol. 26:375-385.
69. Suppmann, B., and G. Sawers. 1994. Isolation and characterization of hypophosphite resistant mutants of Escherichia coli: identification of the FocA protein encoded by the pfl operon, as a putative formate transporter. Mol. Microbiol. 11:965-982.
70. Takano, J., K. Noguchi, M. Yasumori, M. Kobayashi, Z. Gajdos, K. Miwa, H. Hayashi, T. Yoneyama, and T. Fujiwara. 2002. Arabidopsis boron transporter for xylem loading. Nature. 420:337-340.
71. Takano, J., M. Kobayashi, Y. Noda, and T. Fujiwara. 2007. Saccharomyces cerevisiae Bor1 is a boron exporter and a key determinant of boron tolerance. FEMS Microbiol. Lett. 267:230-235.
72. Tarran, R., B.E. Argent, and M.A. Gray. 2000. Regulation of a hyperpolarization-activated chloride current in murine respiratory ciliated cells. J. Physiol. 524:353-364.
73. Tosteson, D.C., and J.F. Hoffman. 1960. Regulation of cell volume by active cation transport in high and low potassium sheep red cells. J. Gen. Physiol. 44:169-194.
74. Vacata, V., A. Kotyk, and K. Sigler. 1981. Membrane potentials in yeast cells measured by direct and indirect methods. Biochim. Biophys. Acta. 643:265-268.
75. Wada, Y., and Y.A.Y. Ohsumi. 1992. Chloride transport of yeast vacuolar membrane vesicles: a study of in vitro vacuolar acidification. Biochim. Biophys. Acta. 1101:296-302.
76. Wiemken, A., and M. Dürr. 1974. Characterization of amino acid pools in the vacuolar compartment of Saccharomyces cerevisiae. Arch. Microbiol. 101:45-57.