Isolation of a putative Candida albicans transcriptional regulator involved in pleiotropic drug resistance by functional complementation of a pdr1 pdr3 mutation in Saccharomyces cerevisiae

Journal of Bacteriology

Volumn 181, Issue 1, 1999, Pages 231-240

  Talibi, Driss ^a,b   Raymond, Martine ^a  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FLUCONAZOLE;

ANTIBIOTIC RESISTANCE; ARTICLE; CANDIDA ALBICANS; GENE INACTIVATION; GENE ISOLATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION;

CANDIDA ALBICANS; SACCHAROMYCES CEREVISIAE;

EID: 0032902758     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.1.231-240.1999     Document Type: Article

References (68)

1. Alarco, A.-M., I. Balan, D. Talihi, N. Mainville, and M. Raymond. 1997. API-mediated multidrug resistance in Saccharomyces cerrvisiae requires FLR1 encoding a transporter of the major facilatator superfamily. J. Biol. Chem. 272:19304-19313.
2. Albertson, G. D., M. Niimi, R. D. Cannon, and H. F. Jenkinson. 1996. Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrob. Agents Chemother. 40:2835-2841.
3. Bailey, D. A., P. J. Feldmann, M. Bovev, N. A. Gow, and A. J. Brown. 1996. The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeasl cell wall proteins. J. Bacteriol. 178:5353-5350.
4. Balan, I., A.-M. Alarco, and M. Raymond. 1997. The Candida alhicans CDK3 uene codes for an opaque-phase ABC transporter. J. Bacteriol. 179:7210-7218.
5. Balzi, E., W. Chen, S. Ulaszewski, E. Capieaux, and A Goffeau. 1987. The multidrug resistance gene PDR1 from Saccharonmyces cerevisiae. J. Biol. Chem. 262:16871-16879.
6. Balzi, E., and A. Goffeau. 1995. Yeast multidrug resistance-the PDR network. J. Bioenerg. Biomembr. 27:71-76.
7. Balzi, E., M. Wang, S. Leterme, L. Van Dyck, and A. Goffeau. 1994. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269:2206-2214.
8. Baudin, A., O. Ozier-Kalogeropoulos, A. Dennuel, F. Lacroute, and C. Cullin. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3331).
9. Bissinger, P. H., and K. Kuchler. 1994. Molecular cloning and expression of the Saachraromyces cerevisiae STSI gene product. A yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem. 269:4180-4186.
10. Boeke, J. D., F. LaCroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346.
11. Bossier, P., L. Fernandes, D. Rocha, and C. Rodrigues-Pousada. 1993. Over-expression of YAP2, coding for a new yAP protein, and YAP1 in Saccharomyces cerevisiae alleviates growth inhibition caused by 1,10-phenanthroline. J. Biol. Chem. 268:23640-23645.
12. Carvajal, E., H. B. van den Hazel, A. Cybularz-Kolaczkowska, E. Balzi, and A. Goffeau. 1997. Molecular and phenotypic eharacterization of yeast PDR1 mutants that show hyperactive transcription of various ABC multidrug transporter genes. Mol. Gen. Genet. 256:406-415.
13. Chin, K. C., G. G. Li, and J. P. Ting. 1997. Importance of acidic, proline/ serine/threonine-rich, and GTP-hinding regions in the major histocompatibilily complex class II transactivator: generation of transdominant-negative mutants. Proc. Natl. Acad. Sci. USA 94:2501-2506.
14. Coleman, S. T., E. Tseng, and W. S. Moye-Rowley. 1997. Saccharomyces cerevisiae basic region-leucine zipper protein regulatory networks converge at the ATR1 structural gene. J. Biol. Chem. 272:23224-23230.
15. Crute, B. E., A. F. Lewis, Z. Wu, J. H. Bushweller, and N. A. Speck. 1996. Biochemical and biophysical properties of the core-bindinu factor α2 (AML1) DNA-binding domain J. Biol. Chem. 271:26251-26260.
16. Cui, Z., D). Hirata, E. Tsuchiya, H. Osada, and T. Miyakawa. 1996. The multidrug resistance-associated protein (MRP) subfamily (Yrs1/Yor1) of Saccharomyce.s cerevisiae is important for the tolerance to a broad range of organic unions. J. Biol. Chem. 271:14712-14716.
17. Decottignies, A., L. Lambert, P. Catty, H. Degand, E. A. Epping, W. S. Move-Rowley, E. Balzi, and A. Goffeau. 1995. Identification and characterization of SNQ2, a new multidrug ATP binding cassette transporter of the yeast plasma membrane. J. Biol. Chem. 270:18150-18157.
18. Delahodde, A., T. Delaveau, and C. Jacq. 1995. Positive autoregulation of the yeast transcription factor Pdr3p, which is involved in control of drug resistance. Mol. Cell. Biol. 15:4043-4051.
19. Delaveau, T., A. Delahodde, E. Carvajal, J. Subik, and C. Jacq. 1994. PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol. Gen. Genet. 244:501-511.
20. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
21. Dexter, D., W. S. Maye-Rowley, A. L. Wu, and J. Golin. 1994. Mutations in the yeast PDR4. PDR7. PDR7 and PDR9 pleiotropic (multiple) drug resistance loci affect the transcript level of an ATP binding cassette transporter encoding gene. PDR5. Genetics 136:505-515.
22. Dixon, D. M., M. M. McNeil, M. L. Cohen, B. G. Gellin, and J. R. La Montagne. 1996. Fungal infections: a growing threat. Public Health Rep. 111:226-235.
23. Donahue, T. F., and A. M. Cigan. 1990. Sequence and structural requirements for efficient translation in yeast. Methods Einzymol. 185:366-372.
24. Dupont, B. F., F. Dromer, and L. Improvisi. 1996. The problem of azole resistance in Candida. J. Mycol. Med. 6:12-19.
25. Fling, M. E., J. Kopf, A. Tamarkin, J. A. Gorman, H. A. Smith, and Y. Koltin. 1991. Analysis of a Candida alhinms gene that encodes a novel mechanism for resistance to benomyl and methotrexate, Mol. Gen. Genet. 227:318-329.
26. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
27. Gietz, R. D., R. H. Schiestl, A. R. Willems, and R. A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355-360.
28. Guo, Z., and F. Sherman. 1996. 3′-end-forming signals of yeast mRNA. Trends Biochem. Sci. 21:477-481.
29. Hahn, S., S. Buratowski, P. A. Sharp, and L. Guartente. 1989. Yeast TATA-binding protein TFIID binds to TATA elements with both consensus and nonconsensus DNA sequences. Proc;. Natl. Acad. Sei. USA 86:5718-5722.
30. Hallstrom, T. C., and W. S. Moye-Rowley. 1998. Divergent transcriptional control of multidrug resistance genes in Saccharomyces cerevisiae. J. Biol. Chem. 273:2098-2104.
31. Hellauer, K., M. H. Rochon, and B. Turcotle. 1996 A novel DNA binding motif for yeasl zinc cluster proteins: the Leu3p and Pdr3p transcriptional activators recognize everted repeats. Mol. Cell. Biol. 16:6096-6102.
32. Hertle, K., E. Haase, and M. Brendel. 1991. The SNQ3 gene of Saccharomyces cerevisiae confers hyper-resistance to several functionally unrelated chemicals. Curr. Genet. 19:429-433.
33. Hirata, D., K. Yano, K. Miyahara, and T. Miyakawa. 1994. Saccharomyces cerevisiae YDRI. which encodes a member of the ATP-hinding cassette (ABC) superfamily, is required for multidrug resistance. Curr. Genet. 26: 285-294.
34. Katzmann, D. J., P. E. Burnett, J. Golin, Y. Mahe, and W. S. Moye-Rowley. 1994. Transcriptional control of the yeasl PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14:4653-4661.
35. Katzmann, D. J., T. C. Hallstrom, Y. Mähe, and W. S. Moye-Rowley. 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.
36. Katzmann, D. J., T. C. Hallstrom, M. Voet, W. Wysock, J. Golin, G. Volckaert, and W. S. Moye-Rowley. 1995. Expression of an ATP-hinding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Sacckaromyces cerevisiae. Mol. Cell. Biol. 15:6875-6883.
37. Lai, M. H., and D. R. Kirsch. 1989. Nucleotide sequence of cytochrome P450 LlA1 (lanosterol 14 α-demethylase) from Candida albicans. Nucleic Acids Res. 17:804.
38. Leppert, G., R. McDevitt, S. C. Falco, T. K. Van Dyk, M. B. Ficke, and J. Golin. 1990. Cloning by gene amplification of two loci conferring multiple drug resistance in Saccharomyces. Genetics 125:13-20.
39. Maenza, J. R., W. G. Merz, M. J. Romagnoli, J. C. Keruly, R. D. Moore, and J. E. Gallant. 1997. Infection due to fluconazole-resistant Candida in patients with AIDS - prevalence and microbiology. Clin. Infect. Dis. 24:28-34.
40. Magee, B. B., and P. T. Magee. 1997. WO-2, a stable aneuploid derivative of Candida albicans strain WO-1, can switch from white to opaque and form hyphae. Microbiology (Reading) 143:289-295.
41. Mahé, Y., A. Parle-McDermott, A. Nourani, A. Delahodde, A. Lamprecht, and K. Kuchler. 1996. 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.
42. Martens, J. A., J. Genereaux, A. Saleh, and C. J. Brandi. 1996. Transcriptional activation by yeast PDR1p is inhibited by its association with NGG1p/ ADA3p. J. Biol. Chem. 271:15884-15890.
43. Meyers, S., W. Schauer, E. Balzi, M. Wagner, A. Goffeau, and J. Golin. 1992. Interaction of the yeast pleiotropic drug resistance genes PDR1 and PDR5. Curr. Genet. 21:431-436.
44. Nourani, A., D. Papajova, A. Delahodde, C. Jacq, and J. Subik. 1997. Clustered amino acid substitutions in (he yeast transcription regulator Pdr3p increase pleiotropic drug resistance and identify a new central regulatory domain. Mol. Gen. Genet. 256:397-405.
45. Nourani, A., M. Wesolowski-Louvel, T. Delaveau, C. Jacq, and A. Delahodde. 1997. Multiple-drug-resistance phenomenon in the yeast Saccharomyces cerevisiae: involvement of two hexose transporters. Mol. Cell. Biol. 17:5453-5460.
46. Ogawa, A., T. Hashida-Okado, M. Endo, H. Yoshioka, T. Tsuruo, K. Takesako, and I. Kato. 1998. Role of ABC transporters in aureobasidin A resistance. Antimicrob. Agents Chemother. 42:755-761.
47. Prasad, R., P. Dewergifosse, A. Goffeau, and E. Balzi. 1995. Molecular cloning and characterization of a novel gene of Candida albicans. CDR1. conferring multiple resistance to drugs and antifungals. Curr. Genet. 27:320-329.
48. Reece, R. J., and M. Ptashne. 1993. Determinants of binding-site specificity among yeast C6 zinc cluster proteins. Science 261:909-911.
49. Rex, J. H., M. G. Rinaldi, and M. A. Pfaller. 1995. Resistance of Candida species to fluconazole. Antimicrob. Agents Chemother. 39:1-8.
50. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
51. Rosenbluh, A., M. Mevarech, Y. Koltin, and J. A. Gorman. 1985. Isolation of genes from Candida albicans by complementation in Saccharomyces cerevisiae. Mol. Gen. Genet. 200:500-502.
52. Sanglard, D., F. Ischer, M. Monod, and J. Bille. 1996. Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob. Agents Chemother. 40:2300-2305.
53. Sanglard, D., F. Ischer, M. Monod, and J. Bille. 1997. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 143: 405-416.
54. Sanglard, D., K. Kuchler, F. Ischer, J. L. Pagani, M. Monod, and J. Bille. 1995. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob. Agents Chemother. 39:2378-2386.
55. Schjerling, P., and S. Holmberg. 1996. Comparative amino acid sequence analysis of the C6 zinc cluster family of transcriptional regulators. Nucleic Acids Res. 24:4599-4607.
56. Schnell, N., B. Krems, and K. D. Entian. 1992. The PARI (YAP1/SNQ3) gene of Saccharomyces cerevisiae, a c-jun homologue, is involved in oxygen metabolism. Curr. Genet. 21:269-273.
57. Servos, J., E. Haase, and M. Brendel. 1993. Gene SNQ2 of Saccharomyces cerevisiae, which confers resistance to 4-nitroquinoline-N-oxide and other chemicals, encodes a 169 kDa protein homologous to ATP-dependent permeases. Mol. Gen. Genet. 236:214-218.
58. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
59. Stephen, D. W., S. L. Rivers, and D. J. Jamieson. 1995. The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol. Microbiol. 16:415-423.
60. Strich, R., R. T. Surosky, C. Steber, E. Dubois, F. Messenguy, and R. E. Esposito. 1994. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8:796-810.
61. Treitel, M. A., and M. Carlson. 1995. Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc. Natl. Acad. Sci. USA 92:3132-3136.
62. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982 Distantly related sequences in the α-and β-subunits of ATP synthase, myosin, kinases, and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 8:945-951.
63. Wemmie, J. A., M. S. Szczypka, D. J. Thiele, and W. S. Moye-Rowley. 1994. Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. J. Biol. Chem. 269:32592-32597.
64. Wendler, F., H. Bergler, K. Prutej, H. Jungwirth, G. Zisser, K. Kuchler, and G. Hogenauer. 1997. Diazaborine resistance in the yeast Saccharomyces cerevisiae reveals a link between YAP1 and the pleiotropic drug resistance genes PDR1 and PDR3. J. Biol. Chem. 272:27091-27098.
65. Wenzel, T. J., A. W. Teunissen, and H. Y. de Steensma. 1995. PDA1 mRNA: a standard for quantitation of mRNA in Saccharomyces cerevisiae superior to ACT1 mRNA. Nucleic Acids Res. 23:883-884.
66. Whiteway, M., D. Dignard, and D. Y. Thomas. 1992. Dominant negative selection of heterologous genes: isolation of Candida albicans genes that interfere with Saccharomyces cerevisiae mating factor-induced cell cycle arrest. Proc. Natl. Acad. Sci. USA 89:9410-9414.
67. Wolfger, H., Y. Mahé, A. Parle-McDermott, A. Delahodde, and K. Kuchler. 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.
68. Wu, A., J. A. Wemmie, N. P. Edgington, M. Goebl, J. L. Guevara, and W. S. Moye-Rowley. 1993. Yeast bZip proteins mediate pleiotropic drug and metal resistance. J. Biol. Chem. 268:18850-18858.