Calcineurin A of Candida albicans: Involvement in antifungal tolerance, cell morphogenesis and virulence

Molecular Microbiology

Volumn 48, Issue 4, 2003, Pages 959-976

  Sanglard, Dominique ^a   Ischer, Françoise ^a   Marchetti, Oscar ^a   Entenza, José ^a   Bille, Jacques ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; AMOROLFINE; ANTIFUNGAL AGENT; BREFELDIN A; CAFFEINE; CALCINEURIN; CALCINEURIN A; CALCIUM ION; CALCOFLUOR WHITE; CONGO RED; CYCLOSPORIN A; DODECYL SULFATE SODIUM; FLUCONAZOLE; FLUPHENAZINE; FUNGAL RNA; ITRACONAZOLE; MYCOPHENOLIC ACID; REAGENT; TERBINAFINE; UNCLASSIFIED DRUG; VORICONAZOLE;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CANDIDA ALBICANS; CANDIDIASIS; CELL VIABILITY; CONTROLLED STUDY; DNA SEQUENCE; DRUG TOLERANCE; FLUORESCENCE MICROSCOPY; FUNGICIDAL ACTIVITY; FUNGUS GROWTH; GROWTH INHIBITION; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SERUM; VIRULENCE;

ANTIFUNGAL AGENTS; BLOTTING, SOUTHERN; CALCINEURIN; CANDIDA ALBICANS; DRUG RESISTANCE, MICROBIAL; FLUCONAZOLE; GENE DELETION; GENES, FUNGAL; MICROBIAL SENSITIVITY TESTS; MORPHOGENESIS; VIRULENCE;

ANIMALIA; CANDIDA; CANDIDA ALBICANS; FUNGI;

EID: 0038016755     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03495.x     Document Type: Article

References (50)

1. Bartizal, K., Gill, C.J., Abruzzo, G.K., Flattery, A.M., Kong, L., Scott, P.M., et al. (1997) In vitro preclinical evaluation studies with the echinocandin antifungal MK-0991 (L-743,872). Antimicrob Agents Chemother 41: 2326-2332.
2. Bonilla, M., Nastase, K.K., and Cunningham, K.W. (2002) Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J 21: 2343-2353.
3. Boustany, L.M., and Cyert, M.S. (2002) Calcineurin-dependent regulation of Crz1p nuclear export requires Msn5p and a conserved calcineurin docking site. Genes Dev 16: 608-619.
4. Breuder, T., Hemenway, C.S., Movva, N.R., Cardenas, M.E., and Heitman, J. (1994) Calcineurin is essential in cyclosporin A- and FK506-sensitive yeast strains. Proc Natl Acad Sci USA 91: 5372-5376.
5. Chaudhuri, B., Hammerle, M., and Furst, P. (1995) The interaction between the catalytic A subunit of calcineurin and its autoinhibitory domain, in the yeast two-hybrid system, is disrupted by cyclosporin A and FK506. FEBS Lett 357: 221-226.
6. Cruz, M.C., Del Poeta, M., Wang, P., Wenger, R., Zenke, G., Quesniaux, V.F., et al. (2000) Immunosuppressive and nonimmunosuppressive cyclosporine analogs are toxic to the opportunistic fungal pathogen Cryptococcus neoformans via cyclophilin-dependent inhibition of calcineurin. Antimicrob Agents Chemother 44: 143-149.
7. Cruz, M.C., Fox, D.S., and Heitman, J. (2001) Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J 20: 1020-1032.
8. Cruz, M.C., Goldstein, A.L., Blankenship, J.R., Del Poeta, M., Davis, D., Cardenas, M.E., et al. (2002) Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J 21: 546-559.
9. Cunningham, K.W., and Fink, G.R. (1994) Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases. J Cell Biol 124: 351-363.
10. Cyert, M.S. (2001) Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Annu Rev Genet 35: 647-672.
11. Denis, V., and Cyert, M.S. (2002) Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156: 29-34.
12. Douglas, C.M., D'Ippolito, J.A., Shei, G.J., Meinz, M., Onishi, J., Marrinan, J.A., et al. (1997) Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob Agents Chemother 41: 2471-2479.
13. Edlind, T., Smith, L., Henry, K., Katiyar, S., and Nickels, J. (2002) Antifungal activity in Saccharomyces cerevisiae is modulated by calcium signalling. Mol Microbiol 46: 257-268.
14. Fonzi, W.A., and Irwin, MY. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728.
15. Fox, D.S., Cruz, M.C., Sia, R.A., Ke, H., Cox, G.M., Cardenas, M.E., and Heitman, J. (2001) Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol Microbiol 39: 835-849.
16. Garrett-Engele, P., Moilanen, B., and Cyert, M.S. (1995) Calcineurin, the Ca2+/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar H(+)-ATPase. Mol Cell Biol 15: 4103-4114.
17. Hanahan, D. (1985) Techniques for transformation of E. coli. In DNA Cloning. A Practical Approach. Glover, D.M. (ed.). Oxford: IRL Press, pp. 109-135.
18. Hemenway, C.S., and Heitman, J. (1999) Calcineurin. Structure, function and inhibition. Cell Biochem Biophys 30: 115-151.
19. Hube, B., Monod, M., Schofieid, D.A., Brown, A.J., and Gow, N.A. (1994) Expression of seven members of the gene family encoding secretory aspartyl proteinases in Candida albicans. Mol Microbiol 14: 87-99.
20. Kontoyiannis, D.P., and Lewis, R.E. (2002) Antifungal drug resistance of pathogenic fungi. Lancet 359: 1135-1144.
21. Krajewska-Kulak, E., and Niczyporuk, W. (1998) Effects of cyclosporin A on mycelial transformation of Candida albicans cells in human serum. J Eur Acad Dermatol Venereol 10: 191-192.
22. Liu, H. (2001) Transcriptional control of dimorphism in Candida albicans. Curr Opin Microbiol 4: 728-735.
23. Marchetti, O., Entenza, J.M., Sanglard, D., Bille, J., Glauser, M.P., and Moreillon, P. (2000a) Fluconazole plus cyclosporine: a fungicidal combination effective against experimental endocarditis due to Candida albicans. Antimicrob Agents Chemother 44: 2932-2938.
24. Marchetti, O., Moreillon, P., Glauser, M.P., Bille, J., and Sanglard, D. (2000b) Potent synergism of the combination of fluconazole and cyclosporine in Candida albicans. Antimicrob Agents Chemother 44: 2373-2381.
25. Marr, K.A., Rustad, T.R., Rex, J.H., and White, T.C. (1999) The trailing end point phenotype in antifungal susceptibility testing is pH dependent. Antimicrob Agents Chemother 43: 1383-1386.
26. Matheos, D.P., Kingsbury, T.J., Ahsan, U.S., and Cunningham, K.W. (1997) Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev 11: 3445-3458.
27. Mendoza, I., Quintero, F.J., Bressan, R.A., Hasegawa, P.M., and Pardo, J.M. (1996) Activated calcineurin confers high tolerance to ion stress and alters the budding pattern and cell morphology of yeast cells. J Biol Chem 271: 23061-23067.
28. de Micheli, M., Bille, J., Schueller, C., and Sanglard, D. (2002) A common drug-responsive element mediates the upregulation of the Candida albicans ABC transporters CDR1 and CDR2, two genes involved in antifungal drug resistance. Mol Microbiol 43: 1197-1214.
29. Mio, T., Adachi-Shimizu, M., Tachibana, Y., Tabuchi, H., Inoue, S.B., Yabe, T., et al. (1997) Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSC1/FKS1 and its involvement in beta-1,3-glucan synthesis. J Bacteriol 179: 4096-4105.
30. Muller, F.M., Lyman, C.A., and Walsh, T.J. (1999) Antimicrobial peptides as potential new antifungals. Mycoses 42: 77-82.
31. National Committee for Clinical Laboratory Standards (1995) Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeast. Tentative Standard M27-A. Villanova, PA: National Committee for Clinical Laboratory Standards.
32. Odom, A., Muir, S., Lim, E., Toffaletti, D.L., Perfect, J., and Heitman, J. (1997) Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J 16: 2576-2589.
33. Polizotto, R.S., and Cyert, M.S. (2001) Calcineurin-dependent nuclear import of the transcription factor Crz1p requires Nmd5p. J Cell Biol 154: 951-960.
34. Prokisch, H., Yarden, O., Dieminger, M., Tropschug, M., and Barthelmess, I.B. (1997) Impairment of calcineurin function in Neurospora crassa reveals its essential role in hyphal growth, morphology and maintenance of the apical Ca2+ gradient. Mol Gen Genet 256: 104-114.
35. Roman, R.M., Lomri, N., Braunstein, G., Feranchak, A.P., Simeoni, L.A., Davison, A.K., et al. (2001) Evidence for multidrug resistance-1 P-glycoprotein-dependent regulation of cellular ATP permeability. J Membr Biol 183: 165-173.
36. Rusnak, F., and Mertz, P. (2000) Calcineurin: form and function. Physiol Rev 80: 1483-1521.
37. Sabath, L.D., Wheeler, N., Laverdiere, M., Blazevic, D., and Wilkinson, B.J. (1977) A new type of penicillin resistance of Staphylococcus aureus. Lancet 1: 443-447.
38. Sanglard, D. (2002) Resistance of human fungal pathogens to antifungal drugs. Curr Opin Microbiol 5: 379-385.
39. Sanglard, D., and Bille, J. (2002) Current understanding of the mode of action and of resistance mechanisms to conventional and emerging antifungal agents for treatment of Candida infections. In Candida and Candidiasis. Calderone, R. (ed.). Washington, DC: American Society for Microbiology Press, pp. 349-383.
40. 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.
41. 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.
42. Sanglard, D., Ischer, F., Monod, M., and Bille, J. (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.
43. Stathopoulos, A.M., and Cyert, M.S. (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev 11: 3432-3444.
44. Stathopoulos-Gerontides, A., Guo, J.J., and Cyert, M.S. (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev 13: 798-803.
45. Warenda, A.J., and Konopka, J.B. (2002) Septin function in Candida albicans morphogenesis. Mol Biol Cell 13: 2732-2746.
46. White, T.C., Marr, K.A., and Bowden, R.A. (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11: 382-402.
47. Withee, J.L., Mulholland, J., Jeng, R., and Cyert, M.S. (1997) An essential role of the yeast pheromone-induced Ca2+ signal is to activate calcineurin. Mol Biol Cell 8: 263-277.
48. Yoshida, T., Toda, T., and Yanagida, M. (1994) A calcineurin-like gene ppb1+ in fission yeast: mutant defects in cytokinesis, cell polarity, mating and spindle pole body positioning. J Cell Sci 107: 1725-1735.
49. Yoshimoto, H., Saltsman, K., Gasch, A.P., Li, H.X., Ogawa, N., Botstein, D., et al. (2002) Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J Biol Chem 277: 31079-31088.
50. Zhao, C., Jung, U.S., Garrett-Engele, P., Roe, T., Cyert, M.S., and Levin, D.E. (1998) Temperature-induced expression of yeast FKS2 is under the dual control of protein kinase C and calcineurin. Mol Cell Biol 18: 1013-1022.