The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans

Journal of Bacteriology

Volumn 181, Issue 3, 1999, Pages 700-708

  Alarco, Anne Marie ^a   Raymond, Martine ^a  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1,10 PHENANTHROLINE; 4 NITROQUINOLINE 1 OXIDE; ABC TRANSPORTER; ANTIFUNGAL AGENT; BREFELDIN A; CADMIUM; CERULENIN; DIAMIDE; FLUCONAZOLE; HYDROGEN PEROXIDE; OXIDIZING AGENT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; FUNGUS MUTANT; GENE DELETION; MULTIDRUG RESISTANCE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION;

CANDIDA ALBICANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0032891070     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.3.700-708.1999     Document Type: Article

References (60)

1. Alarco, A.-M., I. Balan, D. Talibi, N. Mainville, and M. Raymond. 1997. AP1-mediated multidrug resistance in Saccharomyces cerevisiae requires FLRI encoding a transporter of the major facilitator superfamily. J. Biol. Chem. 272:19304-19313.
2. Alhertson, 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. Balan, I., A.-M. Alarco, and M. Raymond. 1997. The Candida albicans CDR3 gene codes for an opaque-phase ABC transporter. J. Bacteriol. 179:7210-7218.
4. Balzi, E., and A. Goffeau. 1995. Yeast multidrug resistance: the PDR network. J. Bioenerg. Biomembr. 27:71-76.
5. Billard, P., H. Dumond, and M. Bolotin-Fukuhara. 1997. Characterization of an AP-1-like transcription factor that mediates an oxidative stress response in Kluyveromyces lactis. Mol. Gen. Genet. 257:62-70.
6. 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.
7. Bossier, P., L. Fernandes, D. Rocha, and C. Rodrigues-Pousada. 1993. Overexpression 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.
8. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
9. Carlson, M., and D, Botstein. 1982. Two differentially regulated mRNAs with different 5′ ends encode secreted intracellular forms of yeast invertase. Cell 28:145-154.
10. Clark, F. S., T. Parkinson, C. A. Hitchcock, and N. A. R. Gow. 1996. Correlation between rhodamine 123 accumulation and azole sensitivity in Candida species: possible role for drug efflux in drug resistance. Antimicrob. Agents Chemother. 40:414-425.
11. 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.
12. Collinson, L. P., and I. W. Dawes. 1992. Inducibility of the response of yeast cells to peroxide stress. J. Gen. Microbiol. 138:329-335.
13. Diamond, R. D., C. A. Lyman, and D. R. Wysong. 1991. Disparate effects of interferon-gamma and tumor necrosis factor-alpha on early neutrophil respiratory burst and fungicidal responses to Candida albicans hyphae in vitro. J. Clin. Investig. 87:711-720.
14. Dupont, B. F., F. Dromer, and L. Improvisi. 1996. The problem of azole resistance in Candida. J. Mycol. Med. 6:12-19.
15. Fernandes, L., C. Rodrigues-Pousada, and K. Struhl. 1997. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol. Cell. Biol. 17:6982-6993.
16. Fling, M. E., J. Kopf, A. Tamarkin, J. A. Gorman, H. A. Smith, and Y. Koltin. 1991. Analysis of a Candida albicans gene that encodes a novel mechanism for resistance to benomyl and methotrexate. Mol. Gen. Genet. 227:318-329.
17. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
18. 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.
19. Goldway, M., D. Teff, R. Schmidt, A. B. Oppenheim, and Y. Koltin. 1995. Multidrug resistance in Candida albicans: disruption of the BEN' gene. Antimicrob. Agents Chemother. 39:422-426.
20. Grant, C. M., L. P. Collinson, J.-H. Roe, and I. W. Dawes. 1996. Yeast glulathione reductase is required for protection against oxidative stress and is a target gene tor yAP-1 transcriptional regulation. Mol. Microbiol. 21:171-179.
21. 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.
22. Hitchcock, C. A. 1993. Resistance of Candida albicans to azole antifungal agents. Biochem. Soc. Trans. 21:1039-1047.
23. Hussain, M., and J. Lenard. 1991. Characterization of PDR4, a Saccharomyces cerevisiae gene that confers pleiotropic drug resistance in high-copy number: identity with YAP1. encoding a transcriptional activator. Gene 101: 149-152.
24. Kelly, R., S. M. Miller, M. B. Kurtz, and D. R. Kirsch. 1987. Directed mutagenesis in Candida albicans: one-step gene disruption to isolate ura3 mutants. Mol. Cell. Biol. 7:199-208.
25. Kosower, N. S., and E. M. Kosower. 1987. Formation of disulfides with diamide. Methods Enzymol. 143:264-270.
26. Kuge, S., and N. Jones. 1994. YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J. 13:655-664.
27. Kuge, S., N. Jones, and A, Nomoto. 1997. Regulation of yAP-1 nuclear localisation in response to oxidative stress. EMBO J. 16:1710-1720.
28. Kuge, S., T. Toda, N. Iizuka, and A. Nomoto. 1998. Crm1 (XpoI) dependent nuclear export of the budding yeast transcription factor yAP-1 is sensitive to oxidative stress. Genes Cells 3:521-532.
29. Kurtz, M. B., M. W. Cortelyou, S. M. Miller, M. Lai, and D. R. Kirsch. 1987. Development of autonomously replicating plasmids for Candida albicans. Mol. Cell. Biol. 7:209-217.
30. 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.
31. Moran, G. P., D. Sanglard, S. M. Donnelly, D. B. Shanley, D. J. Sullivan, and D. C. Coleman. 1998. Identification and expression of multidrug transporters responsible for fluconazole resistance in Candida dubliniensis. Antimicrob. Agents Chemother. 42:1819-1830.
32. Morgan, B. A., G. R. Banks, W. M. Toone, D. Raitt, S. Kuge, and L. H. Johnston. 1997. The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J. 16:1035-1044.
33. Moye-Rowley, W. S., K. D. Harshman, and C. S. Parker. 1989. Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. Genes Dev. 3:283-292.
34. Murphy, J. W. 1991. Mechanisms of natural resistance to human pathogenic fungi. Annu. Rev. Microbiol. 45:509-538.
35. Park, K. S., J. Kwon, and S. Y. Choi. 1998. Cloning, characterization, and expression of the C1P2 gene induced under cadmium stress in Candida sp. FEMS Microbiol. Lett. 162:325-330.
36. Parkinson, T., D. J. Falconer, and C. A. Hitchcock. 1995. Fluconazole resistance due to energy-dependent drug efflux in Candida glabrata. Antimicrob. Agents Chemother. 39:1696-1699.
37. Polley, S. D., and M. X. Caddick. 1996. Molecular characterisation of mcaB, a novel gene affecting nitrogen metabolite repression in Aspergillus nidulans. FEBS Lett. 388:200-205.
38. Rex, J. H., M. G. Rinaldi, and M. A. Pfaller. 1995. Resistance of Candida species to fluconazole. Antimicrob. Agents Chemother. 39:1-8.
39. 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, N.Y.
40. Sambrook, J., E. F. Fritsch, and T. Manialis. 1989. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
41. Sanglard, D., F. Ischer, L. Koymans, and J. Bille. 1998. Amino acid substitutions in the cytochrome P-450 lanosterol 14-α-demethylase (CYP51A1) from azole-resistant Candida albicans clinical isolates contribute to resistance to azole antifungal agents. Antimicrob. Agents Chemother. 42:241-253.
42. 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.
43. Sanglard, D., K. Ischer, M. Monod, and J. Bille. 1997. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new nniltidrug ABC transporter gene. Microbiology 143: 405-416.
44. 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.
45. Schnell, N., and K. D. Entian. 1991. Identification and characterization of a Saccharomyces cerevisiae gene (PAR1) conferring resistance to iron chelators. Eur. J. Biochem. 200:487-493.
46. 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.
47. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
48. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
49. 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.
50. Takeuchi, T., K. Miyahara, D. Hirata, and T. Miyakawa. 1997. Mutational analysis of Yap1 protein, an AP-1-like transcriptional activator of Saccharomyces cerevisiae. FEBS Lett. 416:339-343.
51. Toda, T., M. Shimanuki, and M. Yanagida. 1991. Fission yeast genes that confer resistance to staurosporinc encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev. 5:60-73.
52. Toone, W. M., S. Kuge, M. Samuels, B. A. Morgan, T. Toda, and N. Jones. 1998. Regulation of the fission yeast transcription factor PAP1 by oxidative stress: requirement for the nuclear export factor Crml (exportin) and the stress-activated map kinase Sty1/Spc1. Genes Dev. 12:1453-1463.
53. Vanden Bossche, H., P. Marichal, F. C. Odds, L. Le Jeune, and M. C. Coene. 1992. Characterization of an azole-resistam Candida glabrata isolate. Antimicrob. Agents Chemother. 36:2602-2610.
54. Wagner, D. K., C. Collins-Lech, and P. G. Sohnle. 1986. Inhibition of neutrophil killing of Candida albicans pseudohyphae by substances which quench hypochlorous acid and chloramines. Infect. Immun. 51:731-735.
55. 2 and diamide. J. Biol. Chem. 272:7908-7914.
56. 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.
57. Wemmie, J. A., A. L. Wu, K. D. Harshman, C. S. Parker, and W. S. Moye-Rowley. 1994. Transcriptional activation mediated by the yeast AP-1 protein is required for normal cadmium tolerance. J. Biol. Chem. 269:14690-14697.
58. White, T. C. 1997. Increased mRNA levels of ERG16, CDR, and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob. Agents Chemother. 41:1482-1487.
59. 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.
60. Wu, A. L., and W. S. Moye-Rowley. 1994. GSHI, which encodes γ-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol. Cell. Biol. 14:5832-5839.