Membrane-active compounds activate the transcription factors Pdr1 and Pdr3 connecting pleiotropic drug resistance and membrane lipid homeostasis in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 18, Issue 12, 2007, Pages 4932-4944

  Schüller, Christoph ^a,c   Mamnun, Yasmine M ^a,c   Wolfger, Hubert ^a,d   Rockwell, Nathan ^b,e   Thorner, Jeremy ^b   Kuchler, Karl ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF VIENNA   (Austria)

^d KONRAD LORENZ INSTITUTE FOR ETHOLOGY   (Austria)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PDR1; TRANSCRIPTION FACTOR PDR3; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG RESISTANCE; GENE CONTROL; GENE SEQUENCE; GENETIC TRANSCRIPTION; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; SACCHAROMYCES CEREVISIAE;

CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CHLOROPHENOLS; DETERGENTS; DNA-BINDING PROTEINS; DRUG RESISTANCE, FUNGAL; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; HOMEOSTASIS; IONS; MEMBRANE LIPIDS; PROMOTER REGIONS (GENETICS); SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 37049010139     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-06-0610     Document Type: Article

References (66)

1. Alic, N., Higgins, V. J., Pichova, A., Breitenbach, M., and Dawes, I. W. (2003). Lipid hydroperoxides activate the mitogen-activated protein kinase Mpk1p in Saccharomyces cerevisiae. J. Biol. Chem. 278, 41849-41855.
2. Anderson, J. B., Sirjusingh, C., Parsons, A. B., Boone, C., Wickens, C., Cowen, L. E., and Kohn, L. M. (2003). Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 163, 1287-1298.
3. Baumgartner, U., Hamilton, B., Piskacek, M., Ruis, H., and Rottensteiner, H. (1999). Functional analysis of the Zn(2)Cys(6) transcription factors Oaf1p and Pip2p. Different roles in fatty acid induction of beta-oxidation in Saccharomyces cerevisiae. J. Biol. Chem. 274, 22208-22216.
4. Boorsma, A., Foat, B. C., Vis, D., Klis, F., and Bussemaker, H. J. (2005). T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res. 33, W592-W595.
5. Brazma, A. et al. (2001). Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat. Genet. 29, 365-371.
6. Carvajal, E., van den Hazel, H. B., Cybularz-Kolaczkowska, A., Balzi, E., and Goffeau, A. (1997). Molecular and phenotypic characterization of yeast PDR1 mutants that show hyperactive transcription of various ABC multidrug transporter genes. Mol. Gen. Genet. 256, 406-415.
7. Chang, S. C., Heacock, P. N., Clancey, C. J., and Dowhan, W. (1998). The PEL1 gene (renamed PGS1) encodes the phosphatidylglycero-phosphate synthase of Saccharomyces cerevisiae. J. Biol. Chem. 273, 9829-9836.
8. Chua, G., Morris, Q. D., Sopko, R., Robinson, M. D., Ryan, O., Chan, E. T., Frey, B. J., Andrews, B. J., Boone, C., and Hughes, T. R. (2006). Identifying transcription factor functions and targets by phenotypic activation. Proc. Natl. Acad. Sci. USA 103, 12045-12050.
9. Decottignies, A., Grant, A. M., Nichols, J. W., de Wet, H., McIntosh, D. B., and Goffeau, A. (1998). ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273, 12612-12622.
10. Decottignies, A., Kolaczkowski, M., Balzi, E., and Goffeau, A. (1994). Solubilization and characterization of the overexpressed PDR5 multidrug resistance nucleotide triphosphatase of yeast. J. Biol. Chem. 269, 12797-12803.
11. Delaveau, T., Delahodde, A., Carvajal, E., Subik, J., and Jacq, C. (1994). PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol. Gen. Genet. 244, 501-511.
12. DeRisi, J., van den Hazel, B., Marc, P., Balzi, E., Brown, P., Jacq, C., and Goffeau, A. (2000). Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants. FEBS Lett. 470, 156-160.
13. Des Etages, S. A., Saxena, D., Huang, H. L., Falvey, D. A., Barber, D., and Brandriss, M. C. (2001). Conformational changes play a role in regulating the activity of the proline utilization pathway-specific regulator in Saccharomyces cerevisiae. Mol. Microbiol. 40, 890-899.
14. Devaux, F., Carvajal, E., Moye-Rowley, S., and Jacq, C. (2002). Genome-wide studies on the nuclear PDR3-controlled response to mitochondrial dysfunction in yeast. FEBS Lett. 515, 25-28.
15. Devaux, F., Marc, P., Bouchoux, C., Delaveau, T., Hikkel, I., Potier, M. C., and Jacq, C. (2001). An artificial transcription activator mimics the genome-wide properties of the yeast Pdr1 transcription factor. EMBO Rep. 2, 493-498.
16. Egner, R., Mahé, Y., Pandjaitan, R., and Kuchler, K. (1995). Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 5879-5887.
17. Ellis, L.B., Roe, D., and Wackett, L.P. (2006). The University of Minnesota Biocatalysis/Biodegradation Database: the first decade. Nucleic Acids Res. 34, D517-D521.
18. Esko, J. D., and Raetz, C. R. (1980). Autoradiographic detection of animal cell membrane mutants altered in phosphatidylcholine synthesis. Proc. Natl. Acad. Sci. USA 77, 5192-5196.
19. Fardeau, V., Lelandais, G., Oldfield, A., Salin, H., Lemoine, S., Garcia, M., Tanty, V., Le Crom, S., Jacq, C., and Devaux, F. (2007). The central role of PDR1 in the foundation of yeast drug resistance. J. Biol. Chem. 282, 5063-5074.
20. Flynn, P. J., and Reece, R. J. (1999). Activation of transcription by metabolic intermediates of the pyrimidine biosynthetic pathway. Mol. Cell. Biol. 19, 882-888.
21. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., and Brown, P. O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257.
22. Gordesky, S. E., Marinetti, G. V., and Segel, G. B. (1973). The interaction of 1-fluoro-2,4-dinitrobenzene with amino-phospholipids in membranes of intact erythrocytes, modified erythrocytes, and erythrocytes ghosts. J. Membr. Biol. 14, 229-242.
23. Gordon, L. M., Sauerheber, R. D., Esgate, J. A., Dipple, I., Marchmont, R. J., and Houslay, M. D. (1980). The increase in bilayer fluidity of rat liver plasma membranes achieved by the local anesthetic benzyl alcohol affects the activity of intrinsic membrane enzymes. J. Biol. Chem. 255, 4519-4527.
24. 2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12, 586-597.
25. Guo, H., and Kohlhaw, G. B. (1996). Regulation of transcription in mammalian cells by yeast Leu3p and externally supplied inducer. FEBS Lett. 390, 191-195.
26. Hallström, T. C., Lambert, L., Schorling, S., Balzi, E., Goffeau, A., and Moye-Rowley, W. S. (2001). Coordinate control of sphingolipid biosynthesis and multidrug resistance in Saccharomyces cerevisiae. J. Biol. Chem. 276, 23674-23680.
27. Hallström, T. C., and Moye-Rowley, W. S. (1998). Divergent transcriptional control of multidrug resistance genes in Saccharomyces cerevisiae. J. Biol. Chem. 273, 2098-2104.
28. Hallström, T. C., and Moye-Rowley, W. S. (2000). Multiple signals from dysfunctional mitochondria activate the pleiotropic drug resistance pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275, 37347-37356.
29. Kaioumova, D., Kaioumov, F., Opelz, G., and Susal, C. (2001a). Toxic effects of the herbicide 2,4-dichlorophenoxyacetic acid on lymphoid organs of the rat. Chemosphere 43, 801-805.
30. Kaioumova, D., Susal, C., and Opelz, G. (2001b). Induction of apoptosis in human lymphocytes by the herbicide 2,4-dichlorophenoxyacetic acid. Hum. Immunol. 62, 64-74.
31. Kaiser, C., Michaelis, S., and Mitchell, A. (1994). Methods in Yeast Genetics. A Laboratory Course Manual, Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
32. Katzmann, D. J., Burnett, P. E., Golin, J., Mahé, Y., and Moye-Rowley, W. S. (1994). Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14, 4653-4661.
33. Katzmann, D. J., Hallström, T. C., Mahé, Y., and Moye-Rowley, W. S. (1996). Multiple Pdr1p/Pdr3p binding sites are essential for normal expression of the ATP binding cassette transporter protein-encoding gene PDR5. J. Biol. Chem. 271, 23049-23054.
34. Kean, L. S., Grant, A. M., Angeletti, C., Mahe, Y., Kuchler, K., Fuller, R. S., and Nichols, J. W. (1997). Plasma membrane translocation of fluorescent-labeled phosphatidylethanolamine is controlled by transcription regulators, PDR1 and PDR3. J. Cell Biol. 138, 255-270.
35. Kihara, A., and Igarashi, Y. (2004). Cross talk between sphingolipids and glycerophospholipids in the establishment of plasma membrane asymmetry. Mol. Biol. Cell 15, 4949-4959.
36. Lee, T. I. et al. (2002). Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298, 799-804.
37. Longtine, M. S., McKenzie, A., 3rd, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
38. MacPherson, S., Larochelle, M., and Turcotte, B. (2006). A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol. Mol. Biol. Rev. 70, 583-604.
39. Mahé, Y., Lemoine, Y., and Kuchler, K. (1996a). The ATP binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in vivo. J. Biol. Chem. 271, 25167-25172.
40. Mahé, Y., Parle-McDermott, A., Nourani, A., Delahodde, A., Lamprecht, A., and Kuchler, K. (1996b). The ATP-binding cassette multidrug transporter Snq2 of Saccharomyces cerevisiae: a novel target for the transcription factors Pdr1 and Pdr3. Mol. Microbiol. 20, 109-117.
41. Mamnun, Y. M., Pandjaitan, R., Mahe, Y., Delahodde, A., and Kuchler, K. (2002). The yeast zinc finger regulators Pdr1p and Pdr3p control pleiotropic drug resistance (PDR) as homo- and heterodimers in vivo. Mol. Microbiol. 46, 1429-1440.
42. Mamnun, Y. M., Schriller, C., and Kuchler, K. (2004). Expression regulation of the yeast PDR5 ATP-binding cassette (ABC) transporter suggests a role in cellular detoxification during the exponential growth phase. FEBS Lett. 559, 111-117.
43. Moskvina, E., Imre, E. M., and Ruis, H. (1999). Stress factors acting at the level of the plasma membrane induce transcription via the stress response element (STRE) of the yeast Saccharomyces cerevisiae. Mol. Microbiol. 32, 1263-1272.
44. Moye-Rowley, W. S. (2003). Transcriptional control of multidrug resistance in the yeast Saccharomyces cerevisisae. Prog. Nucleic Acids Res. Mol. Biol. 73, 251-279.
45. Panwar, S. L., and Moye-Rowley, W. S. (2006). Long chain base tolerance in Saccharomyces cerevisiae is induced by retrograde signals from the mitochondria. J. Biol. Chem. 281, 6376-6384.
46. Phelps, C., Gburcik, V., Suslova, E., Dudek, P., Forafonov, F., Bot, N., MacLean, M., Fagan, R. J., and Picard, D. (2006). Fungi and animals may share a common ancestor to nuclear receptors. Proc. Natl. Acad. Sci. USA 103, 7077-7081.
47. Pomorski, T., Lombardi, R., Riezman, H., Devaux, P. F., van Meer, G., and Holthuis, J. C. (2003). Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol. Biol. Cell 14, 1240-1254.
48. Reece, R. J., Beynon, L., Holden, S., Hughes, A. D., Rebora, K., and Sellick, C. A. (2006). Nutrient-regulated gene expression in eukaryotes. Biochem. Soc. Symp. 73, 85-96.
49. Rottensteiner, H., Kal, A. J., Filipits, M., Binder, M., Hamilton, B., Tabak, H. F., and Ruis, H. (1996). Pip2p: a transcriptional regulator of peroxisome proliferation in the yeast Saccharomyces cerevisiae. EMBO J. 15, 2924-2934.
50. Sellick, C. A., and Reece, R. J. (2005). Eukaryotic transcription factors as direct nutrient sensors. Trends Biochem. Sci. 30, 405-412.
51. Siegmund, A., Grant, A., Angeletti, C., Malone, L., Nichols, J. W., and Rudolph, H. K. (1998). Loss of Drs2p does not abolish transfer of fluorescence-labeled phospholipids across the plasma membrane of Saccharomyces cerevisiae. J. Biol. Chem. 273, 34399-34405.
52. Simoes, T., Teixeira, M., Fernandes, C.A.R., and Sa'-Correia, I. (2003). Adaptation of Saccharomyces cerevisiae to the herbicide 2,4-dichlorophenoxyacetic acid, mediated by Msn2p- and Msn4p-regulated genes important role of SPI1. Appl. Environ. Microbiol. 69, 4019-4028.
53. Sipos, G., and Kuchler, K. (2006). Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr. Drug Targets 7, 471-481.
54. Suwalsky, M., Benites, M., Villena, F., Aguilar, F., and Sotomayor, C. P. (1996). Interaction of 2,4-dichlorophenoxyacetic acid (2,4-D) with cell and model membranes. Biochim. Biophys. Acta 1285, 267-276.
55. Teixeira, M. C., Fernandes, A. R., Mira, N. P., Becker, J. D., and Sa-Correia, I. (2006). Early transcriptional response of Saccharomyces cerevisiae to stress imposed by the herbicide 2,4-dichlorophenoxyacetic acid. FEMS Yeast Res. 6, 230-248.
56. Teixeira, M.C., and Sa-Correia, I. (2002). Saccharomyces cerevisiae resistance to chlorinated phenoxyacetic acid herbicides involves Pdr1p-mediated transcriptional activation of TPO1 and PDR5 genes. Biochem. Biophys. Res. Commun. 292, 530-537.
57. Teixeira, M. C., Telo, J. P., Duarte, N. F., and Sa-Correia, I. (2004). The herbicide 2,4-dichlorophenoxyacetic acid induces the generation of free-radicals and associated oxidative stress responses in yeast. Biochem. Biophys. Res. Commun. 324, 1101-1107.
58. Tuschl, H., and Schwab, C. (2003). Cytotoxic effects of the herbicide 2,4-dichlorophenoxyacetic acid in HepG2 cells. Food Chem. Toxicol. 41, 385-393.
59. Vik, A., and Rine, J. (2001). Upc2p and Ecm22p, dual regulators of sterol biosynthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 6395-6405.
60. Wang, D., Zheng, F., Holmberg, S., and Kohlhaw, G. B. (1999). Yeast transcriptional regulator Leu3p. Self-masking, specificity of masking, and evidence for regulation by the intracellular level of Leu3p. J. Biol. Chem. 274, 19017-19024.
61. Wilcox, L. J., Balderes, D. A., Wharton, B., Tinkelenberg, A. H., Rao, G., and Sturley, S. L. (2002). Transcriptional profiling identifies two members of the ATP-binding cassette transporter superfamily required for sterol uptake in yeast. J. Biol. Chem. 277, 32466-32472.
62. Wolfger, H., Mahé, Y., Parle-McDermott, A., Delahodde, A., and Kuchler, K. (1997). The yeast ATP binding cassette (ABC) protein genes PDR10 and PDR15 are novel targets for the Pdr1 and Pdr3 transcriptional regulators. FEBS Lett. 418, 269-274.
63. Wolfger, H., Mamnun, Y. M., and Kuchler, K. (2001). Fungal ABC proteins: pleiotropic drug resistance, stress response and cellular detoxification. Res. Microbiol. 152, 375-389.
64. Wolfger, H., Mamnun, Y. M., and Kuchler, K. (2004). The yeast Pdr15p ATP-binding cassette (ABC) protein is a general stress response factor implicated in cellular detoxification. J. Biol. Chem. 279, 11593-11599.
65. Yano, K., and Fukasawa, T. (1997). Galactose-dependent reversible interaction of Gal3p with Gal80p in the induction pathway of Gal4p-activated genes of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94, 1721-1726.
66. Yoshimoto, H., Saltsman, K., Gasch, A. P., Li, H. X., Ogawa, N., Botstein, D., Brown, P. O., and Cyert, M. S. (2002). Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277, 31079-31088.