Analysis of a fungus-specific transcription factor family, the Candida albicans zinc cluster proteins, by artificial activation

Molecular Microbiology

Volumn 89, Issue 5, 2013, Pages 1003-1017

  Schillig, Rebecca ^a   Morschhäuser, Joachim ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; FLUCONAZOLE; MULTIDRUG RESISTANCE PROTEIN; PROTEIN CDR1; PROTEIN MRR1; PROTEIN TAC1; PROTEIN UPC2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG; ZINC CLUSTER TRANSCRIPTION FACTOR;

ANTIFUNGAL RESISTANCE; ARTICLE; ARTIFICIAL ACTIVATION; CANDIDA ALBICANS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA LIBRARY; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS ISOLATION; GAIN OF FUNCTION MUTATION; GENE OVEREXPRESSION; GENE TARGETING; MOLECULAR LIBRARY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; TRANSCRIPTION INITIATION;

CANDIDA ALBICANS; FUNGI;

ANTIFUNGAL AGENTS; CANDIDA ALBICANS; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; FUNGAL PROTEINS; GENETICS, MICROBIAL; MOLECULAR BIOLOGY; MYCOLOGY; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; ZINC;

EID: 84883141533     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12327     Document Type: Article

References (49)

1. Abbas, C.A., and Sibirny, A.A. (2011) Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev 75: 321-360.
2. Askew, C., Sellam, A., Epp, E., Mallick, J., Hogues, H., Mullick, A., etal. (2011) The zinc cluster transcription factor Ahr1p directs Mcm1p regulation of Candida albicans adhesion. Mol Microbiol 79: 940-953.
3. Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., Smith, J., and Struhl, K. (1989) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
4. Banerjee, M., Thompson, D.S., Lazzell, A., Carlisle, P.L., Pierce, C., Monteagudo, C., etal. (2008) UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol Biol Cell 19: 1354-1365.
5. Braun, B.R., Hoog, M.V., d'Enfert, C., Martchenko, M., Dungan, J., Kuo, A., etal. (2005) A human-curated annotation of the Candida albicans genome. PLoS Genet 1: 36-57.
6. Chen, C., Pande, K., French, S.D., Tuch, B.B., and Noble, S.M. (2011) An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe 10: 118-135.
7. Chiranand, W., McLeod, I., Zhou, H., Lynn, J.J., Vega, L.A., Myers, H., etal. (2008) CTA4 transcription factor mediates induction of nitrosative stress response in Candida albicans. Eukaryot Cell 7: 268-278.
8. Chua, G., Morris, Q.D., Sopko, R., Robinson, M.D., Ryan, O., Chan, E.T., etal. (2006) Identifying transcription factor functions and targets by phenotypic activation. Proc Natl Acad Sci USA 103: 12045-12050.
9. Coste, A., Selmecki, A., Forche, A., Diogo, D., Bougnoux, M.E., d'Enfert, C., etal. (2007) Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 6: 1889-1904.
10. Coste, A.T., Karababa, M., Ischer, F., Bille, J., and Sanglard, D. (2004) TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2. Eukaryot Cell 3: 1639-1652.
11. Coste, A.T., Ramsdale, M., Ischer, F., and Sanglard, D. (2008) Divergent functions of three Candida albicans zinc-cluster transcription factors (CTA4, ASG1 and CTF1) complementing pleiotropic drug resistance in Saccharomyces cerevisiae. Microbiology 154: 1491-1501.
12. Coste, A.T., Crittin, J., Bauser, C., Rohde, B., and Sanglard, D. (2009) Functional analysis of cis- and trans-acting elements of the Candida albicans CDR2 promoter with a novel promoter reporter system. Eukaryot Cell 8: 1250-1267.
13. 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.
14. Dunkel, N., Liu, T.T., Barker, K.S., Homayouni, R., Morschhäuser, J., and Rogers, P.D. (2008) A gain-of-function mutation in the transcription factor Upc2p causes upregulation of ergosterol biosynthesis genes and increased fluconazole resistance in a clinical Candida albicans isolate. Eukaryot Cell 7: 1180-1190.
15. Flowers, S.A., Barker, K.S., Berkow, E.L., Toner, G., Chadwick, S.G., Gygax, S.E., etal. (2012) Gain-of-function mutations in UPC2 are a frequent cause of ERG11 upregulation in azole-resistant clinical isolates of Candida albicans. Eukaryot Cell 11: 1289-1299.
16. Hikkel, I., Lucau-Danila, A., Delaveau, T., Marc, P., Devaux, F., and Jacq, C. (2003) A general strategy to uncover transcription factor properties identifies a new regulator of drug resistance in yeast. J Biol Chem 278: 11427-11432.
17. Homann, O.R., Dea, J., Noble, S.M., and Johnson, A.D. (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 5: e1000783.
18. Knight, S.A., Lesuisse, E., Stearman, R., Klausner, R.D., and Dancis, A. (2002) Reductive iron uptake by Candida albicans: role of copper, iron and the TUP1 regulator. Microbiology 148: 29-40.
19. Le Crom, S., Devaux, F., Marc, P., Zhang, X., Moye-Rowley, W.S., and Jacq, C. (2002) New insights into the pleiotropic drug resistance network from genome-wide characterization of the YRR1 transcription factor regulation system. Mol Cell Biol 22: 2642-2649.
20. Liu, H., Gravelat, F.N., Chiang, L.Y., Chen, D., Vanier, G., Ejzykowicz, D.E., etal. (2010) Aspergillus fumigatus AcuM regulates both iron acquisition and gluconeogenesis. Mol Microbiol 78: 1038-1054.
21. Liu, T.T., Znaidi, S., Barker, K.S., Xu, L., Homayouni, R., Saidane, S., etal. (2007) Genome-wide expression and location analyses of the Candida albicans Tac1p regulon. Eukaryot Cell 6: 2122-2138.
22. MacPherson, S., Akache, B., Weber, S., De Deken, X., Raymond, M., and Turcotte, B. (2005) Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes. Antimicrob Agents Chemother 49: 1745-1752.
23. 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.
24. Marmorstein, R., Carey, M., Ptashne, M., and Harrison, S.C. (1992) DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356: 408-414.
25. Martchenko, M., Levitin, A., Hogues, H., Nantel, A., and Whiteway, M. (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol 17: 1007-1013.
26. 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.
27. Morschhäuser, J. (2010) Regulation of multidrug resistance in pathogenic fungi. Fungal Genet Biol 47: 94-106.
28. Morschhäuser, J., Barker, K.S., Liu, T.T., Blaβ-Warmuth, J., Homayouni, R., and Rogers, P.D. (2007) The transcription factor Mrr1p controls expression of the MDR1 efflux pump and mediates multidrug resistance in Candida albicans. PLoS Pathog 3: e164.
29. Oh, J., Fung, E., Schlecht, U., Davis, R.W., Giaever, G., St Onge, R.P., etal. (2010) Gene annotation and drug target discovery in Candida albicans with a tagged transposon mutant collection. PLoS Pathog 6: e1001140.
30. Reuß, O., and Morschhäuser, J. (2006) A family of oligopeptide transporters is required for growth of Candida albicans on proteins. Mol Microbiol 60: 795-812.
31. Reuß, O., Vik, Å., Kolter, R., and Morschhäuser, J. (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127.
32. Ruhnke, M., Eigler, A., Tennagen, I., Geiseler, B., Engelmann, E., and Trautmann, M. (1994) Emergence of fluconazole-resistant strains of Candida albicans in patients with recurrent oropharyngeal candidosis and human immunodeficiency virus infection. J Clin Microbiol 32: 2092-2098.
33. Saidane, S., Weber, S., De Deken, X., St-Germain, G., and Raymond, M. (2006) PDR16-mediated azole resistance in Candida albicans. Mol Microbiol 60: 1546-1562.
34. 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.
35. Sasse, C., Schillig, R., Dierolf, F., Weyler, M., Schneider, S., Mogavero, S., etal. (2011) The transcription factor Ndt80 does not contribute to Mrr1-, Tac1-, and Upc2-mediated fluconazole resistance in Candida albicans. PLoS ONE 6: e25623.
36. Sasse, C., Dunkel, N., Schäfer, T., Schneider, S., Dierolf, F., Ohlsen, K., and Morschhäuser, J. (2012) The stepwise acquisition of fluconazole resistance mutations causes a gradual loss of fitness in Candida albicans. Mol Microbiol 86: 539-556.
37. Sasse, C., Hasenberg, M., Weyler, M., Gunzer, M., and Morschhäuser, J. (2013) White-opaque switching of Candida albicans allows immune evasion in an environment-dependent fashion. Eukaryot Cell 12: 50-58.
38. Schubert, S., Rogers, P.D., and Morschhäuser, J. (2008) Gain-of-function mutations in the transcription factor MRR1 are responsible for overexpression of the MDR1 efflux pump in fluconazole-resistant Candida dubliniensis strains. Antimicrob Agents Chemother 52: 4274-4280.
39. Schubert, S., Barker, K.S., Znaidi, S., Schneider, S., Dierolf, F., Dunkel, N., etal. (2011a) Regulation of efflux pump expression and drug resistance by the transcription factors Mrr1, Upc2, and Cap1 in Candida albicans. Antimicrob Agents Chemother 55: 2212-2223.
40. Schubert, S., Popp, C., Rogers, P.D., and Morschhäuser, J. (2011b) Functional dissection of a Candida albicans zinc cluster transcription factor, the multidrug resistance regulator Mrr1. Eukaryot Cell 10: 1110-1121.
41. Silver, P.M., Oliver, B.G., and White, T.C. (2004) Role of Candida albicans transcription factor Upc2p in drug resistance and sterol metabolism. Eukaryot Cell 3: 1391-1397.
42. Tsao, S., Rahkhoodaee, F., and Raymond, M. (2009) Relative contributions of the Candida albicans ABC transporters Cdr1p and Cdr2p to clinical azole resistance. Antimicrob Agents Chemother 53: 1344-1352.
43. Tsuji, G., Kenmochi, Y., Takano, Y., Sweigard, J., Farrall, L., Furusawa, I., etal. (2000) Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and Pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 38: 940-954.
44. Vandeputte, P., Ischer, F., Sanglard, D., and Coste, A.T. (2011) In vivo systematic analysis of Candida albicans Zn2-Cys6 transcription factors mutants for mice organ colonization. PLoS ONE 6: e26962.
45. Vandeputte, P., Pradervand, S., Ischer, F., Coste, A.T., Ferrari, S., Harshman, K., and Sanglard, D. (2012) Identification and functional characterization of Rca1, a transcription factor involved in both antifungal susceptibility and host response in Candida albicans. Eukaryot Cell 11: 916-931.
46. Woloshuk, C.P., Foutz, K.R., Brewer, J.F., Bhatnagar, D., Cleveland, T.E., and Payne, G.A. (1994) Molecular characterization of aflR, a regulatory locus for aflatoxin biosynthesis. Appl Environ Microbiol 60: 2408-2414.
47. Znaidi, S., De Deken, X., Weber, S., Rigby, T., Nantel, A., and Raymond, M. (2007) The zinc cluster transcription factor Tac1p regulates PDR16 expression in Candida albicans. Mol Microbiol 66: 440-452.
48. Znaidi, S., Weber, S., Al-Abdin, O.Z., Bomme, P., Saidane, S., Drouin, S., etal. (2008) Genomewide location analysis of Candida albicans Upc2p, a regulator of sterol metabolism and azole drug resistance. Eukaryot Cell 7: 836-847.
49. Zordan, R.E., Miller, M.G., Galgoczy, D.J., Tuch, B.B., and Johnson, A.D. (2007) Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans. PLoS Biol 5: e256.