Identification of yeast genes involved in k+ homeostasis: Loss of membrane traffic genes affects k+ uptake

G3: Genes, Genomes, Genetics

Volumn 1, Issue 1, 2011, Pages 43-56

  Fell, Gillian L ^a,b   Munson, Amanda M ^a,c   Croston, Merriah A ^a,d   Rosenwald, Anne G ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c SHENANDOAH UNIVERSITY   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

TRK1; VPS genes

Indexed keywords

EID: 84865294191     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.111.000166     Document Type: Article

References (128)

1. Adams, A., D. E. Gottschling, C. A. Kaiser, and T. Stearns, 2997 Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
2. Ali, R., C. L. Brett, S. Mukherjee, and R. Rao, 2004 Inhibition of sodium/ proton exchange by a Rab-GTPase-activating protein regulates endosomal traffic in yeast. J. Biol. Chem. 279: 4498-4506.
3. Armstrong, W. M., and A. Rothstein, 1967 Discrimination between alkali metal cations by yeast: II. Cation interactions in transport. J. Gen. Physiol. 50: 967-988.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman et al., 1997 Short Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
5. Aw, S., D. S. Adams, D. Qiu, and M. Levin, 2008 H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mech. Dev. 125: 353-372.
6. Banuelos, M. A., and A. Rodriguez-Navarro, 1998 P-type ATPases mediate sodium and potassium effluxes in Schwanniomyces occidentalis. J. Biol. Chem. 273: 1640-1646.
7. Banuelos, M. A., M. C. Ruiz, A. Jimenez, J.-L. Souciet, S. Potier et al., 2002 Role of the Nha1 antiporter in regulating K+ influx in Saccharomyces cerevisiae. Yeast. 19: 9-15.
8. Banuelos, 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. Microbiol. 144: 2749-2778.
9. Banuelos, M. G., D. E. Moreno, D. K. Olson, Q. Nguyen, F. Ricarte et al., 2010 Genomic analysis of severe hypersensitivity to hygromycin B reveals linkage to vacuolar defects and new vacuolar gene functions in Saccharomyces cerevisiae.Curr. Genet. 56: 121-137.
10. Behnia, R., B. Panic, J. R. C. Whyte, and S. Munro, 2004 Targeting of the Arf-like GTPase Arl3p to the Golgi requires N-terminal acetylation and the membrane protein Sys1p. Nat. Cell Biol. 6: 405-413.
11. Bensen, E. S., B. G. Yeung, and G. S. Payne, 2001 Ric1p and the Ypt6p GTPase function in a common pathway required for localization of trans- Golgi network membrane proteins. Mol. Biol. Cell. 12: 13-26.
12. Bilodeau, P. S., J. L. Urbanowski, S. C. Winistorfer, and R. C. Piper, 2002 The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4: 534-539.
13. Bilodeau, P. S., S. C. Winistorfer, W. R. Kearney, A. D. Roberston, and R. C. Piper, 2003 Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins in the endosome. J. Cell Biol. 163: 237-243.
14. Bowers, K., B. P. Levi, F. I. Patel, and T. H. Stevens, 2000 The sodium/ proton exchanger Nhx1p is required for endosomal protein trafficking in the yeast Saccharomyces cerevsiae. Mol. Biol. Cell 11: 4277- 4294.
15. Boyle, E. I., S. Weng, J. Gollub, H. Jin, D. Botstein et al., 2004 GO:Term- Finder-open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics. 20: 3710-3715.
16. Brett, C. L., D. N. Tukaye, S. Mukherjee, and R. Rao, 2005 The yeast endosomal Na+K+/H+ exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Mol. Biol. Cell 16: 1396-1405.
17. Brodersen, D. E., W. M. Clemons Jr, A. P. Carter, R. J. Morgan-Warren, B. T. Wimberly et al., 2000 The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell. 103: 1143-1154.
18. Burns, N., P. B. Ross-MacDonald, G. S. Roeder, and M. Snyder, 1996 Generation, screening and analysis of lacZ fusions in yeast, pp. 61-79 in: Microbioal Genome Methods, edited by Adolph, K. W. CRC Press, Boca Raton, FL.
19. Burri, L., and T. Lithgow, 2004 A complete set of SNAREs in yeast. Traffic. 5: 45-52.
20. Cagnac, O., M. N. Aranda-Sicilia, M. Leterrier, M. P. Rodriguez-Rosales, and K. Venema, 2010 Vacuolar cation/H+ antiporters of Saccharomyces cerevisiae. J. Biol. Chem. 285: 33914-33922.
21. Cagnac, O., M. Leterrier, M. Yeager, and E. Blumwald, 2007 Identification and characterization of Vnx1p, a novel type of vacuolar monovalent cation/H+ antiporter of Saccharomyces cerevisiae. J. Biol. Chem. 282: 24284-24293.
22. Casado, C., L. Yenush, C. Melero, C. Ruiz Mdel, R. Serrano et al., 2010 Regulation of Trk-dependent potassium transport by the calcineurin pathway involves the Hal5 kinase. FEBS Lett. 584: 2415-2420.
23. Clotet, J., E. Gari, M. Aldea, and J. Arino, 1999 The yeast Ser/Thr phosphatases Sit4 an Ppz1 play opposite roles in regulation of the cell cycle. Mol. Cell. Biol. 19: 2408-2415.
24. Conboy, M. J., and M. S. Cyert, 2000 Luv1p/Rki1p/Tcs3p/Vps54p, a yeast protein that localizes to the late Golgi and early endosome, is required for normal vacuolar morphology. Mol. Biol. Cell. 11: 2429-2443.
25. Cooke, F. T., S. K. Dove, R. K. McEwen, G. Painter, A. B. Holmes et al., 1998 The stress-activated phosphatidylinositol 3-phosphate 5-kinase Fab1p is essential for vacuole function in S. cerevisiae. Curr. Biol. 8: 1219-1222.
26. Cyert, M. S., R. Kunisawa, D. Kaim, and J. Thorner, 1991 Yeast has homologs (CNA1 and CNA2 gene products) of mammalian calcineurin, a calmodulin-regulated phosphoprotein phosphatase. Proc. Natl. Acad. Sci. USA 88: 7376-7380.
27. de Nadal, E., F. Calero, J. Ramos, and J. Arino, 1999 Biochemical and genetic analyses of the role of yeast casein kinase 2 in salt tolerance. J. Bacteriol. 181: 6456-6462.
28. Dean, N., 1995 Yeast glycosylation mutants are sensitive to aminoglycosides. Proc. Natl. Acad. Sci. USA 92: 1287-1291.
29. Dubois, E., B. Scherens, F. Vierendeels, M. M. W. Ho, F. Messenguy et al., 2002 In Saccharomyces cerevisiae, the inositol polyphosphate kinase activity of Kcs1p is required for resistance to salt stress, cell wall integrity, and vacuolar morphogenesis. J. Biol. Chem. 277: 23755-23763.
30. Dudley, A. M., D. M. Janse, A. Tanay, R. Shamir, and G. M. Church, 2005 A global view of pleiotropy and phenotypically derived gene function in yeast. Mol. Syst. Biol. 1: 2005.0001.
31. Durell, S. R., and H. R. Guy, 1999 Structural models of the KtrB, TrkH, and Trk1,2 symporters based on the structure of the KcsA K(+) channel. Biophys. J. 77: 789-807.
32. Durell, S. R., Y. Hao, T. Nakamura, E. P. Bakker, and H. R. Guy, 1999 Evolutionary relationship between K+ channels and symporters. Biophys. J. 77: 775-788.
33. El Alami, M., F. Messenguy, B. Scherens, and E. Dubois, 2003 Arg82p is a bifunctional protein whose inositol polyphosphate kinase activity is essential for nitrogen and PHO gene expression but not for Mcm1p chaperoning in yeast. Mol. Microbiol. 49: 457-468.
34. Gaber, R. F., 1992 Molecular genetics of yeast ion transport. Int. Rev. Cytol. 137A: 299-353.
35. 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.
36. Gaynor, E. C., C.-Y. Chen, S. D. Emr, and T. R. Graham, 1998 ARF is required for maintenance of yeast Golgi and endosome structure and function. Mol. Biol. Cell 9: 653-670.
37. Gaynor, E. C., and S. D. Emr, 1997 COPI-independent anterograde transport: Cargo-selective ER to Golgi protein transport in yeast COPI mutants. J. Cell Biol. 136: 789-802.
38. Gerrard, S. R., N. J. Bryant, and T. H. Stevens, 2000 VPS21 controls entry of endocytosed and biosynthetic proteins into the yeast prevacuolar compartment. Mol. Biol. Cell 11: 613-626.
39. Hama, H., G. G. Tall, and B. F. Horazdovsky, 1999 Vps9p is a guanine nucleotide exchange factor involved in vesicle-mediated vacuolar protein transport. J. Biol. Chem. 274: 15284-15291.
40. Heuser, J. E., and R. G. Anderson, 1989 Hypertonic media inhibit receptormediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108: 389-400.
41. 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.
42. Honsbein, A., S. Sokolovski, C. Grefen, P. Campanoni, R. Pratelli et al., 2009 A tripartite SNARE-K+ channel complex mediates in channeldependent K+ nutrition in Arabidopsis. Plant Cell. 21: 2859-2877.
43. Horazdovsky, B. F., G. R. Busch, and S. D. Emr, 1994 VPS21 encodes a rab5-like GTP binding protein that is required for the sorting of yeast vacuolar proteins. EMBO J. 13: 1297-1309.
44. Horazdovsky, B. F., C. R. Cowles, P. Mustol, M. Holmes, and S. D. Emr, 1996 A novel RING finger protein, Vps8p, functionally interacts with the small GTPase, Vps21p, to facilitate soluble vacuolar protein localization. J. Biol. Chem. 271: 33607-33615.
45. Hudson, R. T., and R. K. Draper, 1997 Interaction of coatomer with aminoglycoside antibiotics: evidence that coatomer has at least two dilysine binding sites. Mol. Biol. Cell 8: 1901-1910.
46. Huh, W. K., J. V. Falvo, L. C. Gerke, A. S. Carroll, R. W. Howson et al., 2003 Global analysis of protein localization in budding yeast. Nature. 425: 686-691.
47. Ito, H., Y. Fukuda, K. Murata, and A. Kimura, 1983 Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153: 163-168.
48. Jochum, A., D. Jackson, H. Schwarz, R. Pipkorn, and B. Singer-Kruger, 2002 Yeast Ysl2p, homologous to Sec7 domain guanine nucleotide exchange factors, functions in endocytosis and maintenance of vacuole integrity and interacts with the Arf-like small GTPase Arl1p. Mol. Cell. Biol. 22: 4914-4928.
49. Katzmann, D. J., G. Odorizzi, and S. D. Emr, 2002 Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3: 893- 905.
50. Katzmann, D. J., C. J. Stefan, M. Babst, and S. D. Emr, 2003 Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162: 413-423.
51. Ko, C. H., A. M. Buckley, and R. F. Gaber, 1990 TRK2 is required for low affinity K+ transport in Saccharomyces cerevisiae. Genetics. 125: 305-312.
52. 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.
53. Laemmli, U. K., 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
54. Larkin, J. M., M. S. Brown, J. L. Goldstein, and R. G. Anderson, 1983 Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell. 33: 273-285.
55. Larkin, J. M., W. C. Donzell, and R. G. Anderson, 1985 Modulation of intracellular potassium and ATP: effects on coated pit function in fibroblasts and hepatocytes. J. Cell. Physiol. 124: 372-378.
56. Larkin, J. M.,W. C. Donzell, and R. G. Anderson, 1986 Potassium-dependent assembly of coated pits: new coated pits form as planar clathrin lattices. J. Cell Biol. 103: 2619-2627.
57. Ledbetter, M. L. S., and M. Lubin, 1977 Control of protein synthesis in human fibroblasts by intracellular potassium. Exp. Cell Res. 105: 223- 236.
58. Levin, M., T. Thorlin, K. R. Robinson, T. Nogi, and M. Mercola, 2002 Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell. 111: 77-89.
59. Li, B., and J. R. Warner, 1996 Mutation of the Rab6 homologue of Saccharomyces cerevisiae, YPT6, inhibits both early Golgi function and ribosome biosynthesis. J. Biol. Chem. 271: 16813-16819.
60. Liu, Y.-W., C.-F. Huang, K.-B. Huang, and F.-J. S. Lee, 2005 Role for Gcs1p in regulation of Arl1p at trans-Golgi compartments. Mol. Biol. Cell 16: 4024-4033.
61. Love, S. L., C. M. A. Manlandro, C. J. Testa, A. E. Thomas, K.-E. Tryggestad et al., 2004 The yeast genes, ARL1 and CCZ1, interact to control membrane traffic and ion homeostasis. Biochem. Biophys. Res. Commun. 319: 840-846.
62. Lowe, S. L., S. H. Wong, and W. Hong, 1996 The mammalian ARF-like protein 1 (Arl1) is associated with the Golgi complex. J. Cell Sci. 109: 209-220.
63. Lu, L., H. Horstmann, C. Ng, and W. Hong, 2001 Regulation of Golgi structure and function by ARF-like protein 1 (Arl1). J. Cell Sci. 114: 4534-4555.
64. Lubin, M., 1964 Intracellular potassium and control of protein synthesis. Fed. Proc. 23: 994-1001.
65. Lubin, M., 1967 Intracellular potassium and macromolecular synthesis in mammalian cells. Nature. 213: 451-453.
66. Lubin, M., and H. L. Ennis, 1964 On the role of intracellular potassium in protein synthesis. Biochim. Biophys. Acta. 80: 614-631.
67. 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.
68. Manlandro, C. M. A., D. H. Haydon, and A. G. Rosenwald, 2005 The ability of Sit4p to promote K+ efflux via Nha1p is modulated by Sap155p and Sap185p. Eukaryot. Cell 4: 1041-1049.
69. Manohar, M., H. Mei, A. J. Franklin, E. M. Sweet, T. Shigaki et al., 2010 Zebrafish (Danio rerio) endomembrane antiporter similar to a yeast cation/H(+) transporter is required for neural crest development. Biochemistry. 49: 6557-6566.
70. Maresova, L., and H. Sychrova, 2005 Physiological characterization of Saccharomyces cerevisiae kha1 deletion mutants. Mol Micro. 55: 588-600.
71. Maresova, L., and H. Sychrova, 2010 Genetic interactions among the Arl1 GTPase and intracellular Na+/H+ antiporters in pH homeostasis and cation detoxification. FEM. Yeast Res. 10: 802-811.
72. Maresova, L. E. Urbankova, D. Gaskova, and H. Sychrova, 2006 Measurements of plasma membrane potential changes in Saccharomyces cerevisiae cells reveal the importance of the Tok1 channel in membrane potential maintenance. FEM. Yeast Res. 6: 1039-1046.
73. Masuda, C. A., J. Ramirez, A. Pena, and M. Montero-Lomeli, 2000 Regulation of monovalent ion homeostasis and pH by the Ser-Thr protein phosphatase SIT4 in Saccharomyces cerevsiae. J. Biol. Chem. 275: 30957-30961.
74. Michel, B., C. Lozano, M. Rodríguez, R. Coria, J. Ramírez et al., 2006 The yeast potassium transporter TRK2 is able to substitute for TRK1 in its biological function under low K and low pH conditions. Yeast. 23: 581-589.
75. Mulet, J. M., M. P. Leube, S. J. Kron, G. Rios, G. R. Fink et al., 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.
76. Munro, S., 2005 The Arf-like GTPase Arl1 and its role in membrane traffic. Biochem. Soc. Trans. 33: 601-605.
77. Munson, A. M., D. H. Haydon, S. L. Love, G. L. Fell, V. R. Palanivel et al., 2004a Yeast ARL1 encodes a regulator of K+ influx. J. Cell Sci. 117: 2309-2320.
78. Munson, A. M., S. L. Love, J. Shu, V. R. Palanivel, and A. G. Rosenwald, 2004b ARL1 participates with ATC1/LIC4 to regulate responses of yeast cells to ions. Biochem. Biophys. Res. Commun. 315: 617-623.
79. Nass, R., K. W. Cunningham, and R. Rao, 1997 Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast is enhanced by mutations in the plasma membrane H+-ATPase: Insights into mechanisms of sodium tolerance. J. Biol. Chem. 272: 26145-26152.
80. Nass, R., and R. Rao, 1998 Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast: Implications for vauole biogenesis. J. Biol. Chem. 273: 21054-21060.
81. 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: 2515-2524.
82. Navarrete, C., S. Petrezselyova, L. Barreto, J. Martinez, J. Zahradka et al., 2010 Lack of main K+ uptake systems in Saccharomyces cerevisiae cells affects yeast performance in both potassium-sufficient and potassiumlimiting conditions. FEM. Yeast Res. 10: 508-517.
83. Nickerson, D. P., C. L. Brett, and A. J. Merz, 2009 Vps-C complexes: Gatekeeperss of endolysosomal traffic. Curr. Opin. Cell Biol. 21: 543-551.
84. Nishikawa, S., and A. Nakano, 1993 Identification of a gene required for membrane protein retention in the early secretory pathway. Proc. Natl. Acad. Sci. USA 90: 8179-8183.
85. O'Brien, M. C., and D. B. McKay, 1995 How potassium affects the activity of the molecular chaparone Hsc70: I. Potassium is required for optimal ATPase activity. J. Biol. Chem. 270: 2247-2250.
86. Oka, T., and M. Krieger, 2005 Multi-component protein complexes and Golgi membrane trafficking. J. Biochem. 137: 109-114.
87. Panic, B., J. R. Whyte, and S. Munro, 2003 The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus. Curr. Biol. 13: 405-410.
88. Pérez-Valle, J., H. Jenkins, S. Merchan, V. Montiel, J. Ramos et al., 2007 Key role for intracellular K+ and protein kinases Sat4/Hal4 and Hal5 in the plasma membrane stabilization of yeast nutrient transporters. Mol. Cell. Biol. 27: 5725-5736.
89. Perkins, J., and G. M. Gadd, 1993 Accumulation and intracellular compartmentation of lithium ions in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 107: 255-260.
90. Perlin, D. S., C. L. Brown, and J. E. Haber, 1988 Membrane potential defect in hygromycin B-resistant pma1 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 263: 18118-18122.
91. Perlin, D. S., S. L. Harris, D. Seto-Young, and J. E. Haber, 1989 Defective H +-ATPase of hygromycin B-resistant pma1 mutants from Saccharomyces cerevisiae. J. Biol. Chem. 264: 21857-21864.
92. Poon, P. P., D. Cassel, A. Spang, M. Rotman, E. Pick et al., 1999 Retrograde transport from the yeast Golgi is mediated by two ARF GAP proteins with overlapping function. EMBO J. 18: 555-564.
93. Posas, F., M. Camps, and J. Arino, 1995 The PPZ protein phosphatases are important determinants of salt tolerance in yeast cells. J. Biol. Chem. 270: 13036-13041.
94. 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.
95. Radisky, D. C., W. B. Snyder, S. D. Emr, and J. Kaplan, 1997 Characterization of VPS41, a gene required for vacuolar trafficking and high-affinity iron transport in yeast. Proc. Natl. Acad. Sci. USA 94: 5662-5666.
96. Ramirez, J., O. Ramirez, C. Saldana, R. Coria, and A. Pena, 1998 A Saccharomyces cerevisiae mutant lacking a K+/H+ exchanger. J. Bacteriol. 180: 5860-5865.
97. Ramos, J., R. Aligo, R. Haro, and A. Rodriguez-Navarro, 1994 TRK2 is not a low-affinity potassium transporter in Saccharomyces cerevisiae. J. Bacteriol. 176: 249-252.
98. Raya, A., Y. Kawakami, C. Rodriguez-Esteban, M. Ibanes, D. Rasskin-Gutman et al., 2004 Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature. 427: 121-128.
99. Roberts, C. J., C. K. Raymond, C. T. Yamashiro, and T. H. Stevens, 1991 Methods for studying the yeast vacuole. Methods Enzymol. 194: 644-661.
100. Robinson, J. S., D. J. Klionsky, L. M. Banta, and S. D. Emr, 1988 Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol. 8: 4936-4948.
101. Rodriguez-Navarro, A., 2000 Potassium transport in fungi and plants. Biochim. Biophys. Acta. 1469: 1-30.
102. Rosenwald, A. G., M. A. Rhodes, H. Van Valkenburgh, V. Palanivel, G. Chapman et al., 2002 ARL1 and membrane traffic in Saccharomyces cerevisiae. Yeast. 19: 1039-1056.
103. Ruiz, A., I. Muñoz, R. Serrano, A. González, E. Simón et al., 2004a Functional characterization of the Saccharomyces cerevisiae VHS3 gene. A regulatory subunit of the Ppz1 protein phosphatase with novel, phosphatase-unrelated functions. J. Biol. Chem. 279: 34421- 34430.
104. Ruiz, A., M. C. Ruiz, M. A. Sanchez-Garrido, J. Arino, and J. Ramos, 2004b The ppz protein phosphatases regulate Trk-independent potassium influx in yeast. FEBS Lett. 578: 58-62.
105. Santos, B., A. Duran, and M. Valdivieso, 1997 CHS5, a gene involved in chitin synthesis and mating in Saccharomyces cerevisiae. Mol. Cell. Biol. 17: 2485-2496.
106. Sato, M., K. Sato, S. Nishikawa, A. Hirata, J. Kato et al., 1999 The yeast RER2 gene, identified by endoplasmic reticulum protein localization mutations, encodes cis-prenyltransferase, a key enzyme in dolichol synthesis. Mol. Cell. Biol. 19: 471-483.
107. Sherman, F., G. Fink, and C. Lawrence, 1974 Methods in Yeast Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
108. Siniossoglou, S., S. Y. Peak-Chew, and H. R. B. Pelham, 2000 Ric1p and Rgp1p form a complex that catalyses nucleotide exchange on Ypt6p. EMBO J. 19: 4885-4894.
109. Springael, J. Y., E. Nikko, B. Andre, and A. M. Marini, 2002 Yeast Npi3/ Bro1 is involved in ubiquitin-dependent control of permease trafficking. FEBS Lett. 517: 103-109.
110. Strom, M., P. Vollmer, T. J. Tan, and D. Gallwitz, 1993 A yeast GTPaseactivating protein that interacts specifically with a member of the Ypt/Rab family. Nature. 361: 736-739.
111. Sutton, A., D. Immanuel, and K. T. Arndt, 1991 The SIT4 protein phosphatase functions in late G1 for progression into S phase. Mol. Cell. Biol. 11: 2133-2148.
112. Sychrova, H., J. Ramirez, and A. Pena, 1999 Involvement of Nha1 antiporter in regulation of intracellular pH in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 171: 167-172.
113. Szafer, E., M. Rotman, and D. Cassel, 2001 Regulation of GTP hydrolysis on ADP-ribosylation factor-1 at the Golgi membrane. J. Biol. Chem. 276: 47834-47839.
114. van Berkel, M. A., M. Rieger, S. te Heesen, A. F. Ram, H. van den Ende et al., 1999 The Saccharomyces cerevisiae CWH8 gene is required for full levels of dolichol-linked oligosaccharides in the endoplasmic reticulum and for efficient N-glycosylation. Glycobiology. 9: 243-253.
115. Vargas, R. C., R. García-Salcedo, S. Tenreiro, M. C. Teixeira, A. R. Fernandes et al., 2007 Saccharomyces cerevisiae multidrug resistance transporter Qdr2 is implicated in potassium uptake, providing a physiological advantage to quinidine-stressed cells. Eukaryot. Cell 6: 134-142.
116. Vercauteren, D., R. E. Vandenbroucke, A. T. Jones, J. Rejman, J. Demeester et al., 2010 The use of inhibitors to study endocytic pathways of gene carriers: Optimization and pitfalls. Mol. Ther. 18: 561-569.
117. Wang, C. W., P. E. Stromhaug, E. J. Kauffman, L. S. Weisman, and D. J. Klionsky, 2003 Yeast homotypic vacuole fusion requires the Ccz1-Mon1 complex during the tethering/docking stage. J. Cell Biol. 163: 973-985.
118. Wilbanks, S. M., and D. B. McKay, 1995 How potassium affects the activity of the molecular chaperone Hsc70: II. Potassium binds specifically in the ATPase active site. J. Biol. Chem. 270: 2251-2257.
119. Will, E., and D. Gallwitz, 2001 Biochemical characterization of Gyp6p, a Ypt/Rab-specific GTPase-activating protein from yeast. J. Biol. Chem. 276: 12135-12139.
120. Winzeler, E. A., D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson et al., 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 285: 901-906.
121. Withee, J. L., R. Sen, and M. S. Cyert, 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.
122. Wurmser, A. E., T. K. Sato, and S. D. Emr, 2000 New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151: 551- 562.
123. Yamamoto, A., D. B. DeWald, I. V. Boronenkov, R. A. Anderson, S. D. Emr et al., 1995 Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast. Mol. Biol. Cell. 6: 525- 539.
124. Yenush, L., S. Merchan, J. Holmes, and R. Serrano, 2005 pH-responsive posttranslational regulation of the Trk1 potassium transporter by the type 1-related Ppz1 phosphatase. Mol. Cell. Biol. 25: 8683-8692.
125. Yenush, L., J. M. Mulet, J. Arino, and R. Serrano, 2002 The Ppz protein phosphatases are key regulators of K+ and pH homeostasis: implications for salt tolerance, cell wall integrity and cell cycle progression. EMBO J. 21: 920-929.
126. Zeng, G. F., M. Pypaert, and C. L. Slayman, 2004 Epitope tagging of the yeast K(+) carrier Trk2p demonstrates folding that is consistent with a channel-like structure. J. Biol. Chem. 279: 3003-3013.
127. Zhang, T., J. J. Caffrey, and S. B. Shears, 2001 The transcriptional regulator, Arg82, is a hybrid kinase with both monophosphoinositol and diphosphoinositol polyphosphate synthase activity. FEBS Lett. 494: 208-212.
128. Zhdankina, O., N. L. Strand, J. M. Redmond, and A. L. Boman, 2001 Yeast GGA proteins interact with GTP-bound Arf and facilitate transport through the Golgi. Yeast. 18: 1-18.