RTA2 is involved in calcineurin-mediated azole resistance and sphingoid long-chain base release in Candida albicans

Cellular and Molecular Life Sciences

Volumn 66, Issue 1, 2009, Pages 122-134

  Jia, X M ^a   Wang, Y ^a   Jia, Y ^a   Gao, P H ^a   Xu, Y G ^a   Wang, L ^a   Cao, Y Y ^a   Cao, Y B ^a   Zhang, L X ^b   Jiang, Y Y ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Azole resistance; Calcineurin pathway; Candida albicans; RTA2; Sphingoid

Indexed keywords

CALCINEURIN; CALCIUM CHLORIDE; CYCLOHEXIMIDE; CYCLOSPORIN A; ECONAZOLE; EGTAZIC ACID; FLUCONAZOLE; FLUPHENAZINE; FUMONISIN B1; ITRACONAZOLE; KETOCONAZOLE; NYSTATIN; PYRROLE DERIVATIVE; SPHINGANINE; TACROLIMUS; TERBINAFINE; THERMOZYMOCIDIN; VORICONAZOLE;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA ALBICANS; CELL MEMBRANE; CONTROLLED STUDY; FUNGAL CELL; FUNGAL GENE; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; NONHUMAN; RTA2 GENE; SIGNAL TRANSDUCTION; WILD TYPE;

ANTIFUNGAL AGENTS; AZOLES; BIOLOGICAL TRANSPORT; CALCIUM; CANDIDA ALBICANS; CELL MEMBRANE; DRUG RESISTANCE, FUNGAL; ERGOSTEROL; FUNGAL PROTEINS; MEMBRANE PROTEINS; MICROBIAL SENSITIVITY TESTS; RHODAMINES; SPHINGOSINE; UP-REGULATION;

CANDIDA ALBICANS; SPHINGOIDEA;

EID: 58149489011     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8409-3     Document Type: Article

References (46)

1. Baddley, J. W. and Moser, S. A. (2003) Emerging fungal resistance. Clin. Lab. Med. 2004, 721-735.
2. Perea, S. and Patterson, T. F. (2002) Antifungal resistance in pathogenic fungi. Clin. Infect. Dis. 35, 1073-1080.
3. Pfaller, M. A. and Diekema, D. J. (2004) Rare and emerging opportunistic fungal pathogens:Concern for resistance beyond Candida albicans and Aspergillus fumigatus. J. Clin. Microbiol. 42, 4419-4431.
4. Akins, R. A. (2005) An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43, 285-318.
5. Prasad, R., DeWergifosse, P., Goffeau, A. and Balzi, E. (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.
6. Sanglard, D., Kuchler, K., Ischer, F., Pagani, J. L., Monod, M. and Bille, J. (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.
7. 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.
8. Prasad, R. and Kapoor, K. (2005) Multidrug resistance in yeast Candida. Int. Rev. Cytol. 242, 215-248.
9. Calabrese, D., Bille, J. and Sanglard, D. (2000) A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology 146, 2743-2754.
10. Franz, R., Kelly, S. L., Lamb, D. C., Kelly, D. E., Ruhnke, M. and Morschhauser, J. (1998) Multiple molecular mechanisms contribute to a stepwise development of fluconazole resistance in clinical Candida albicans strains. Antimicrob. Agents Chemother. 42, 3065-3072.
11. Marichal, P., Koymans, L., Willemsens, S., Bellens, D., Verhasselt, P., Luyten, W., Borgers, M., Ramaekers, F. C., Odds, F. C. and Bossche, H. V. (1999) Contribution of mutations in the cytochrome P450 14alpha-demethylase (Erg11p, Cyp51p) to azole resistance in Candida albicans. Microbiology 145, 2701-2713.
12. Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Tanabe, K., Niimi, M. and Monk, B. C. (2007) Candida albicans drug resistance another way to cope with stress. Microbiology 153, 3211.
13. Karababa, M., Valentino, E., Pardini, G., Coste, A. T., Bille, J. and Sanglard, D. (2006) CRZ1, a target of the calcineurin pathway in Candida albicans. Mol. Microbiol. 59, 1429-1451.
14. Bader, T., Schroppel, K., Bentink, S., Agabian, N., Kohler, G. and Morschhauser, J. (2006) Role of calcineurin in stress resistance,morphogenesis, and virulence of a Candida albicans wild-type strain. Infect. Immun. 74, 4366-4369.
15. Sanglard, D., Ischer, F., Marchetti, O., Entenza, J. and Bille, J. (2003) Calcineurin A of Candida albicans: Involvement in antifungal tolerance, cell morphogenesis and virulence. Mol. Microbiol. 48, 959-976.
16. Cruz, M. C., Goldstein, A. L., Blankenship, J. R., Del Poeta, M., Davis, D., Cardenas, M. E., Perfect, J. R., McCusker, J. H. and Heitman, J. (2002) Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J. 21, 546-559.
17. Steinbach, W. J., Reedy, J. L., Cramer, R. A., Jr., Perfect, J. R. and Heitman, J. (2007) Harnessing calcineurin as a novel antiinfective agent against invasive fungal infections. Nat. Rev. Microbiol. 5, 418-430.
18. Rusnak, F. and Mertz, P. (2000) Calcineurin: Form and function. Physiol. Rev. 80, 1483-1521.
19. Santos, M. and de Larrinoa, I. F. (2005) Functional characterization of the Candida albicans CRZ1 gene encoding a calcineurin-regulated transcription factor. Curr. Genet. 48, 88-100.
20. Cowen, L. E. and Lindquist, S. (2005) Hsp90 potentiates the rapid evolution of new traits: Drug resistance in diverse fungi. Science 309, 2185-2189.
21. Cowen, L. E., Carpenter, A. E., Matangkasombut, O., Fink, G. R. and Lindquist, S. (2006) Genetic architecture of Hsp90-dependent drug resistance. Eukaryot. Cell 5, 2184-2188.
22. Noble, S. M. and Johnson, A. D. (2005) Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4, 298-309.
23. Fonzi, W. A. and Irwin, M. Y. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
24. Sanglard, D., Ischer, F., Monod, M. and Bille, J. (1996) Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob. Agents Chemother. 40, 2300-2305.
25. Care, R. S., Trevethick, J., Binley, K. M. and Sudbery, P. E. (1999) The MET3 promoter: A new tool for Candida albicans molecular genetics. Mol. Microbiol. 34, 792-798.
26. Espinel-Ingroff, A., Rodríguez-Tudela, J. L. and Martínez-Suárez, J. V. (1995) Comparison of two alternative microdilution procedures with the National Committee for Clinical Laboratory Standards reference macrodilution method M27-P for in vitro testing of fluconazole-resistant and-susceptible isolates of Candida albicans. J. Clin. Microbiol. 33, 3154.
27. Wang, Y., Cao, Y. Y., Jia, X. M., Cao, Y. B., Gao, P. H., Fu, X. P., Ying, K., Chen, W. S. and Jiang, Y. Y. (2006) Cap1p is involved in multiple pathways of oxidative stress response in Candida albicans. Free Radic. Biol. Med. 40, 1201-1209.
28. Howell, S. A., Mallet, A. I. and Noble, W. C. (1990) A comparison of the sterol content of multiple isolates of the Candida albicans Darlington strain with other clinically azole-sensitive and-resistant strains. J. Appl. Microbiol. 69, 692-696.
29. Ryley, J. F., Wilson, R. G. and Barrett-Bee, K. J. (1984) Azole resistance in Candida albicans. Med. Mycol. 22, 53-63.
30. Gao, P. H., Cao, Y. B., Jia, X. M., Cao, Y. Y., Quan, H., Wang, Y. and Jiang, Y. Y. (2006) Drug susceptibilities of yeast cells are affected when expressing mutant Candida albicans drug resistance protein. Int. J. Antimicrob. Agents 28, 69-74.
31. Hirokawa, T., Boon-Chieng, S. and Mitaku, S. (1998) SOSUI: Classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378-379.
32. Kihara, A. and Igarashi, Y. (2002) Identification and characterization of a Saccharomyces cerevisiae gene, RSB1, involved in sphingoid long-chain base release. J. Biol. Chem. 277, 30048-30054.
33. Mao, C., Saba, J. D. and Obeid, L. M. (1999) The dihydrosphingosine-1- phosphate phosphatases of Saccharomyces cerevisiae are important regulators of cell proliferation and heat stress responses. Biochem. J. 342, 667-675.
34. Smriti, D. and Prasad, R. (1999) CDR1p, which confers multidrug resistance in Candida albicans, is a general phospholipid translocase. Abstr Intersci Conf Antimicrob Agents Chemother Intersci Conf Antimicrob Agents Chemother 39, 587.
35. Smriti, Krishnamurthy, S., Dixit, B. L., Gupta, C. M., Milewski, S. and Prasad, R. (2002) ABC transporters Cdr1p, Cdr2p and Cdr3p of a human pathogen Candida albicans are general phospholipid translocators. Yeast 19, 303-318.
36. Dickson, R. C., Sumanasekera, C. and Lester, R. L. (2006) Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid Res. 45, 447-465.
37. Dickson, R. C. (1998) Sphingolipid functions in Saccharomyces cerevisiae: Comparison to mammals. Annu. Rev. Biochem. 67, 27-48.
38. Martin, S. W. and Konopka, J. B. (2004) Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot. Cell 3, 675-684.
39. Dieterich, C., Schandar, M., Noll, M., Johannes, F. J., Brunner, H., Graeve, T. and Rupp, S. (2002) In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148, 497-506.
40. Moffett, S., Brown, D. A. and Linder, M. E. (2000) Lipid-dependent targeting ofGproteins into rafts. J. Biol. Chem. 275, 2191-2198.
41. Wu, M., Holowka, D., Craighead, H. G. and Baird, B. (2004) Visualization of plasmamembrane compartmentalization with patterned lipid bilayers. Proc. Natl. Acad. Sci. USA 101, 13798-13803.
42. Mukhopadhyay, K., Kohli, A. and Prasad, R. (2002) Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob. Agents Chemother. 46, 3695-3705.
43. Mukhopadhyay, K., Prasad, T., Saini, P., Pucadyil, T. J., Chattopadhyay, A. and Prasad, R. (2004) Membrane sphingolipid-ergosterol interactions are important determinants of multidrug resistance in Candida albicans. Antimicrob. Agents Chemother. 48, 1778-1787.
44. Pasrija, R., Prasad, T. and Prasad, R. (2005) Membrane raft lipid constituents affect drug susceptibilities of Candida albicans. Biochem. Soc. Trans. 33, 1219-1223.
45. Prasad, T., Saini, P., Gaur, N. A., Vishwakarma, R. A., Khan, L. A., Haq, Q. M. and Prasad, R. (2005) Functional analysis of CaIPT1, a sphingolipid biosynthetic gene involved in multidrug resistance and morphogenesis of Candida albicans. Antimicrob. Agents Chemother. 49, 3442-3452.
46. Negredo, A., Monteoliva, L., Gil, C., Pla, J. and Nombela, C. (1997) Cloning, analysis and one-step disruption of the ARG5,6gene of Candida albicans. Microbiology 143, 297-302.