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Institut de Microbiologie, Centre Hospitalier Universitaire Vaudois (CHUV), 1011 Lausanne, Switzerland
Service de Dermatologie, Centre Hospitalier Universitaire Vaudois (CHUV), 1011 Lausanne, Switzerland
3Author for correspondence: Dominique Sanglard. Tel: +41 21 3144083. Fax: +41 21 3144060. e-mail: dsanglar@eliot.unil.ch
ABSTRACT
Resistance to azole antifungal agents in Candida albicans can be mediated by multidrug efflux transporters. In a previous study, we identified at least two such transporters, Cdr1p and Benp, which belong to the class of ATP-binding cassette (ABC) transporters and of major facilitators, respectively. To isolate additional factors potentially responsible for resistance to azole antifungal agents in C. albicans, the hypersusceptibility of a Saccharomyces cerevisiae multidrug transporter mutant, 
pdr5, to these agents was complemented with a C. albicans genomic library. Several new genes were isolated, one of which was a new ABC transporter gene called CDR2 (Candida drug resistance). The protein Cdr2p encoded by this gene exhibited 84% identity with Cdr1p and could confer resistance to azole antifungal agents, to other antifungals (terbinafine, amorolfine) and to a variety of metabolic inhibitors. The disruption of CDR2 in the C. albicans strain CAF4-2 did not render cells more susceptible to these substances. When the disruption of CDR2 was performed in the background of a mutant in which CDR1 was deleted, the resulting double cdr1 cdr2 mutant was more susceptible to these agents than the single cdr1 mutant. The absence of hypersusceptibility of the single cdr2 mutant could be explained by the absence of CDR2 mRNA in azole-susceptible C albicans strains. CDR2 was overexpressed, however, in clinical C. albicans isolates resistant to azole antifungal agents as described previously for CDR1, but to levels exceeding or equal to those reached by CDR1. Interestingly, CDR2 expression was restored in cdr1 mutants reverting spontaneously to wild-type levels of susceptibility to azole antifungal agents. These data demonstrate that CDR2 plays an important role in mediating the resistance of C. albicans to azole antifungal agents.
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S. Perea, J. L. Lopez-Ribot, W. R. Kirkpatrick, R. K. McAtee, R. A. Santillan, M. Martinez, D. Calabrese, D. Sanglard, and T. F. Patterson Prevalence of Molecular Mechanisms of Resistance to Azole Antifungal Agents in Candida albicans Strains Displaying High-Level Fluconazole Resistance Isolated from Human Immunodeficiency Virus-Infected Patients Antimicrob. Agents Chemother., October 1, 2001; 45(10): 2676 - 2684. [Abstract] [Full Text]
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K. Maebashi, M. Niimi, M. Kudoh, F. J. Fischer, K. Makimura, K. Niimi, R. J. Piper, K. Uchida, M. Arisawa, R. D. Cannon, et al. Mechanisms of fluconazole resistance in Candida albicans isolates from Japanese AIDS patients J. Antimicrob. Chemother., May 1, 2001; 47(5): 527 - 536. [Abstract] [Full Text] [PDF]
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 M. Jasinski, Y. Stukkens, H. Degand, B. Purnelle, J. Marchand-Brynaert, and M. Boutry A Plant Plasma Membrane ATP Binding Cassette-Type Transporter Is Involved in Antifungal Terpenoid Secretion PLANT CELL, May 1, 2001; 13(5): 1095 - 1107. [Abstract] [Full Text]
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D. Sanglard, F. Ischer, and J. Bille Role of ATP-Binding-Cassette Transporter Genes in High-Frequency Acquisition of Resistance to Azole Antifungals in Candida glabrata Antimicrob. Agents Chemother., April 1, 2001; 45(4): 1174 - 1183. [Abstract] [Full Text]
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F. Mignini, R. Prasad, and E. Borowski Unusual Susceptibility of a Multidrug-Resistant Yeast Strain to Peptidic Antifungals Antimicrob. Agents Chemother., January 1, 2001; 45(1): 223 - 228. [Abstract] [Full Text]
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O. Marchetti, J. M. Entenza, D. Sanglard, J. Bille, M. P. Glauser, and P. Moreillon Fluconazole plus Cyclosporine: a Fungicidal Combination Effective against Experimental Endocarditis Due to Candida albicans Antimicrob. Agents Chemother., November 1, 2000; 44(11): 2932 - 2938. [Abstract] [Full Text]
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D. Calabrese, J. Bille, and D. Sanglard A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole Microbiology, November 1, 2000; 146(11): 2743 - 2754. [Abstract] [Full Text]
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J.-P. BOUCHARA, R. ZOUHAIR, S. LE BOUDOUIL, G. RENIER, R. FILMON, D. CHABASSE, J.-N. HALLET, and A. DEFONTAINE In-vivo selection of an azole-resistant petite mutant of Candida glabrata J. Med. Microbiol., November 1, 2000; 49(11): 977 - 984. [Abstract] [Full Text] [PDF]
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K. W. Henry, J. T. Nickels, and T. D. Edlind Upregulation of ERG Genes in Candida Species by Azoles and Other Sterol Biosynthesis Inhibitors Antimicrob. Agents Chemother., October 1, 2000; 44(10): 2693 - 2700. [Abstract] [Full Text]
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C. N. Lyons and T. C. White Transcriptional Analyses of Antifungal Drug Resistance in Candida albicans Antimicrob. Agents Chemother., September 1, 2000; 44(9): 2296 - 2303. [Abstract] [Full Text]
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O. Marchetti, P. Moreillon, M. P. Glauser, J. Bille, and D. Sanglard Potent Synergism of the Combination of Fluconazole and Cyclosporine in Candida albicans Antimicrob. Agents Chemother., September 1, 2000; 44(9): 2373 - 2381. [Abstract] [Full Text]
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A. C. Andrade, G. Del Sorbo, J. G. M. Van Nistelrooy, and M. A. D. Waard The ABC transporter AtrB from Aspergillus nidulans mediates resistance to all major classes of fungicides and some natural toxic compounds Microbiology, August 1, 2000; 146(8): 1987 - 1997. [Abstract] [Full Text]
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F. Barchiesi, D. Calabrese, D. Sanglard, L. Falconi Di Francesco, F. Caselli, D. Giannini, A. Giacometti, S. Gavaudan, and G. Scalise Experimental Induction of Fluconazole Resistance in Candida tropicalis ATCC 750 Antimicrob. Agents Chemother., June 1, 2000; 44(6): 1578 - 1584. [Abstract] [Full Text]
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 L. E. Cowen, D. Sanglard, D. Calabrese, C. Sirjusingh, J. B. Anderson, and L. M. Kohn Evolution of Drug Resistance in Experimental Populations of Candida albicans J. Bacteriol., March 15, 2000; 182(6): 1515 - 1522. [Abstract] [Full Text]
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S. Wirsching, S. Michel, G. Köhler, and J. Morschhäuser Activation of the Multiple Drug Resistance Gene MDR1 in Fluconazole-Resistant, Clinical Candida albicans Strains Is Caused by Mutations in a trans-Regulatory Factor J. Bacteriol., January 15, 2000; 182(2): 400 - 404. [Abstract] [Full Text]
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T. Yamada-Okabe, T. Mio, N. Ono, Y. Kashima, M. Matsui, M. Arisawa, and H. Yamada-Okabe Roles of Three Histidine Kinase Genes in Hyphal Development and Virulence of the Pathogenic Fungus Candida albicans J. Bacteriol., December 1, 1999; 181(23): 7243 - 7247. [Abstract] [Full Text]
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P. Marichal, J. Gorrens, L. Laurijssens, K. Vermuyten, C. Van Hove, L. Le Jeune, P. Verhasselt, D. Sanglard, M. Borgers, F. C. S. Ramaekers, et al. Accumulation of 3-Ketosteroids Induced by Itraconazole in Azole-Resistant Clinical Candida albicans Isolates Antimicrob. Agents Chemother., November 1, 1999; 43(11): 2663 - 2670. [Abstract] [Full Text]
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D. Sanglard, F. Ischer, D. Calabrese, P. A. Majcherczyk, and J. Bille The ATP Binding Cassette Transporter Gene CgCDR1 from Candida glabrata Is Involved in the Resistance of Clinical Isolates to Azole Antifungal Agents Antimicrob. Agents Chemother., November 1, 1999; 43(11): 2753 - 2765. [Abstract] [Full Text]
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M. E. Cardenas, M. C. Cruz, M. Del Poeta, N. Chung, J. R. Perfect, and J. Heitman Antifungal Activities of Antineoplastic Agents: Saccharomyces cerevisiae as a Model System To Study Drug Action Clin. Microbiol. Rev., October 1, 1999; 12(4): 583 - 611. [Abstract] [Full Text] [PDF]
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B. Favre, M. Didmon, and N. S. Ryder Multiple amino acid substitutions in lanosterol 14{alpha}-demethylase contribute to azole resistance in Candida albicans Microbiology, October 1, 1999; 145(10): 2715 - 2725. [Abstract] [Full Text] [PDF]
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K. W. Henry, M. C. Cruz, S. K. Katiyar, and T. D. Edlind Antagonism of Azole Activity against Candida albicans following Induction of Multidrug Resistance Genes by Selected Antimicrobial Agents Antimicrob. Agents Chemother., August 1, 1999; 43(8): 1968 - 1974. [Abstract] [Full Text]
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S. E. Koshlukova, T. L. Lloyd, M. W. B. Araujo, and M. Edgerton Salivary Histatin 5 Induces Non-lytic Release of ATP from Candida albicans Leading to Cell Death J. Biol. Chem., July 2, 1999; 274(27): 18872 - 18879. [Abstract] [Full Text] [PDF]
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J. L. Lopez-Ribot, R. K. McAtee, S. Perea, W. R. Kirkpatrick, M. G. Rinaldi, and T. F. Patterson Multiple Resistant Phenotypes of Candida albicans Coexist during Episodes of Oropharyngeal Candidiasis in Human Immunodeficiency Virus-Infected Patients Antimicrob. Agents Chemother., July 1, 1999; 43(7): 1621 - 1630. [Abstract] [Full Text]
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V. Perepnikhatka, F. J. Fischer, M. Niimi, R. A. Baker, R. D. Cannon, Y.-K. Wang, F. Sherman, and E. Rustchenko Specific Chromosome Alterations in Fluconazole-Resistant Mutants of Candida albicans J. Bacteriol., July 1, 1999; 181(13): 4041 - 4049. [Abstract] [Full Text]
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K. C. Ha and T. C. White Effects of Azole Antifungal Drugs on the Transition from Yeast Cells to Hyphae in Susceptible and Resistant Isolates of the Pathogenic Yeast Candida albicans Antimicrob. Agents Chemother., April 1, 1999; 43(4): 763 - 768. [Abstract] [Full Text]
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A.-M. Alarco and M. Raymond The bZip Transcription Factor Cap1p Is Involved in Multidrug Resistance and Oxidative Stress Response in Candida albicans J. Bacteriol., February 1, 1999; 181(3): 700 - 708. [Abstract] [Full Text]
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D. Talibi and M. Raymond Isolation of a Putative Candida albicans Transcriptional Regulator Involved in Pleiotropic Drug Resistance by Functional Complementation of a pdr1 pdr3 Mutation in Saccharomyces cerevisiae J. Bacteriol., January 1, 1999; 181(1): 231 - 240. [Abstract] [Full Text]
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R. Franz, S. L. Kelly, D. C. Lamb, D. E. Kelly, M. Ruhnke, and J. Morschhäuser Multiple Molecular Mechanisms Contribute to a Stepwise Development of Fluconazole Resistance in Clinical Candida albicans Strains Antimicrob. Agents Chemother., December 1, 1998; 42(12): 3065 - 3072. [Abstract] [Full Text]
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J. L. Lopez-Ribot, R. K. McAtee, L. N. Lee, W. R. Kirkpatrick, T. C. White, D. Sanglard, and T. F. Patterson Distinct Patterns of Gene Expression Associated with Development of Fluconazole Resistance in Serial Candida albicans Isolates from Human Immunodeficiency Virus-Infected Patients with Oropharyngeal Candidiasis Antimicrob. Agents Chemother., November 1, 1998; 42(11): 2932 - 2937. [Abstract] [Full Text]
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K. A. Marr, C. N. Lyons, T. Rustad, R. A. Bowden, and T. C. White Rapid, Transient Fluconazole Resistance in Candida albicans Is Associated with Increased mRNA Levels of CDR Antimicrob. Agents Chemother., October 1, 1998; 42(10): 2584 - 2589. [Abstract] [Full Text]
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K. Ziegelbauer Decreased Accumulation or Increased Isoleucyl-tRNA Synthetase Activity Confers Resistance to the Cyclic beta -Amino Acid BAY 10-8888 in Candida albicans and Candida tropicalis Antimicrob. Agents Chemother., July 1, 1998; 42(7): 1581 - 1586. [Abstract] [Full Text]
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H. Miyazaki, Y. Miyazaki, A. Geber, T. Parkinson, C. Hitchcock, D. J. Falconer, D. J. Ward, K. Marsden, and J. E. Bennett Fluconazole Resistance Associated with Drug Efflux and Increased Transcription of a Drug Transporter Gene, PDH1, in Candida glabrata Antimicrob. Agents Chemother., July 1, 1998; 42(7): 1695 - 1701. [Abstract] [Full Text]
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G. P. Moran, D. Sanglard, S. M. Donnelly, D. B. Shanley, D. J. Sullivan, and D. C. Coleman Identification and Expression of Multidrug Transporters Responsible for Fluconazole Resistance in Candida dubliniensis Antimicrob. Agents Chemother., July 1, 1998; 42(7): 1819 - 1830. [Abstract] [Full Text]
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