Home LiteratureArticle Details
PMID: 15105136 Published · ppublish English Journal Article

Mechanisms of azole resistance in petite mutants of Candida glabrata.

Antimicrobial agents and chemotherapy ·Vol. 48 ·No. 5 ·2004-05-00 ·Pages 1788-96

Brun S, Bergès T, Poupard P, Vauzelle-Moreau C, Renier G, Chabasse D, Bouchara JP

Abstract

We previously showed that resistant colonies of Candida glabrata inside the azole inhibition zones had respiratory deficiency due to mutations in mitochondrial DNA. Here, we analyzed the mechanisms of azole resistance in petite mutants of C. glabrata obtained by exposure to fluconazole or induced by ethidium bromide. The respiratory deficiency of these mutants was confirmed by oxygraphy and flow cytometric analysis with rhodamine 123, and its mitochondrial origin was demonstrated by transmission electron microscopy and restriction endonuclease analysis of the mitochondrial DNA. Flow cytometry with rhodamine 6G suggested an increased drug efflux in mutant cells, which was further supported by Northern blot analysis of the expression of the C. glabrata CDR1 (CgCDR1) and CgCDR2 genes, encoding efflux pumps. Conversely, the expression of CgERG11, which encodes the azole target, was not affected by petite mutations, and no differences were seen in the sequence of this gene between parent isolates and mutants. Moreover, sterol analysis showed similar overall amount of sterols in parent and mutant cells, but quantitative modifications were observed in the mutants, with almost undetectable biosynthesis intermediates. Further analysis performed after separation of free sterols from steryl esters revealed a defect in sterol esterification in mutant cells, with free ergosterol representing 92% of the overall sterol content. Thus, resistance or decreased susceptibility to azoles in petite mutants of C. glabrata is associated with increased expression of CgCDR1 and, to a lesser extent, of CgCDR2. In addition, the marked increase in free ergosterol content would explain their increased susceptibility to polyenes.

MeSH Terms
Antifungal Agents/pharmacology Azoles/pharmacology Blotting, Northern Candida albicans/drug effects,genetics DNA, Mitochondrial/genetics Drug Resistance, Multiple, Fungal Flow Cytometry Fluconazole/pharmacology Fluorescent Dyes Fungal Proteins/metabolism Membrane Transport Proteins/metabolism Microbial Sensitivity Tests Microscopy, Electron Mutation/physiology Rhodamines Sterols/metabolism
Chemicals
Antifungal Agents Azoles CDR1 protein, Candida albicans DNA, Mitochondrial Fluorescent Dyes Fungal Proteins Membrane Transport Proteins Rhodamines Sterols rhodamine 6G Fluconazole
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Brun Sophie
Groupe d'Etude des Interactions Hôte-Parasite, UPRES-EA 3142, Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, 49033 Angers Cedex, France.
Bergès Thierry
Poupard Pascal
Vauzelle-Moreau Carole
Renier Gilles
Chabasse Dominique
Bouchara Jean-Philippe
References (45)
45 references, click to expand
  1. 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. 1999 Nov;43(11):2753-65 PMID: 10543759
  2. Studies on the mechanism of action of miconazole: effect of miconazole on respiration and cell permeability of Candida albicans.
    Antimicrob Agents Chemother. 1974 Apr;5(4):420-5 PMID: 15825399
  3. In-vivo selection of an azole-resistant petite mutant of Candida glabrata.
    J Med Microbiol. 2000 Nov;49(11):977-84 PMID: 11073151
  4. Mutations in yeast ARV1 alter intracellular sterol distribution and are complemented by human ARV1.
    J Biol Chem. 2000 Dec 29;275(52):40667-70 PMID: 11063737
  5. Role of ATP-binding-cassette transporter genes in high-frequency acquisition of resistance to azole antifungals in Candida glabrata.
    Antimicrob Agents Chemother. 2001 Apr;45(4):1174-83 PMID: 11257032
  6. Anaerobiosis induces complex changes in sterol esterification pattern in the yeast Saccharomyces cerevisiae.
    FEMS Microbiol Lett. 2001 Apr 1;197(1):41-5 PMID: 11287144
  7. Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial dna mutant.
    J Biol Chem. 2001 Feb 9;276(6):4020-7 PMID: 11054416
  8. Transcriptional regulation of the two sterol esterification genes in the yeast Saccharomyces cerevisiae.
    J Bacteriol. 2001 Sep;183(17):4950-7 PMID: 11489845
  9. Heme-regulated expression of two yeast acyl-CoA:sterol acyltransferases is involved in the specific response of sterol esterification to anaerobiosis.
    FEMS Microbiol Lett. 2002 Jan 2;206(1):121-5 PMID: 11786267
  10. Heterogeneous mechanisms of azole resistance in Candida albicans clinical isolates from an HIV-infected patient on continuous fluconazole therapy for oropharyngeal candidosis.
    J Antimicrob Chemother. 2002 Mar;49(3):515-24 PMID: 11864952
  11. Molecular mechanisms of fluconazole resistance in Candida dubliniensis isolates from human immunodeficiency virus-infected patients with oropharyngeal candidiasis.
    Antimicrob Agents Chemother. 2002 Jun;46(6):1695-703 PMID: 12019078
  12. The genetic basis of fluconazole resistance development in Candida albicans.
    Biochim Biophys Acta. 2002 Jul 18;1587(2-3):240-8 PMID: 12084466
  13. Gene order evolution and paleopolyploidy in hemiascomycete yeasts.
    Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9272-7 PMID: 12093907
  14. SUT1 suppresses sec14-1 through upregulation of CSR1 in Saccharomyces cerevisiae.
    FEMS Microbiol Lett. 2002 Nov 5;216(2):165-70 PMID: 12435498
  15. The complete mitochondrial genome sequence of the pathogenic yeast Candida (Torulopsis) glabrata.
    FEBS Lett. 2003 Jan 16;534(1-3):39-48 PMID: 12527359
  16. Multiple patterns of resistance to fluconazole in Candida glabrata isolates from a patient with oropharyngeal candidiasis receiving head and neck radiation.
    J Clin Microbiol. 2003 Feb;41(2):619-22 PMID: 12574256
  17. Mutagenicity of reactive oxygen and nitrogen species as detected by co-culture of activated inflammatory leukocytes and AS52 cells.
    Carcinogenesis. 2003 Feb;24(2):235-41 PMID: 12584172
  18. Relationships between respiration and susceptibility to azole antifungals in Candida glabrata.
    Antimicrob Agents Chemother. 2003 Mar;47(3):847-53 PMID: 12604511
  19. Erythromycin, an inhibitor of mitoribosomal protein biosynthesis, alters the amphotericin B susceptibility of Candida albicans.
    J Pharm Pharmacol. 2003 Feb;55(2):179-84 PMID: 12631409
  20. Disruption of mitochondrial function in Candida albicans leads to reduced cellular ergosterol levels and elevated growth in the presence of amphotericin B.
    Arch Microbiol. 2003 Apr;179(4):295-300 PMID: 12640519
  21. Respiratory-deficient mutants of Torulopsis glabrata, a yeast with circular mitochondrial deoxyribonucleic acid of 6 mu m.
    J Bacteriol. 1976 May;126(2):959-68 PMID: 944184
  22. Primary site of action of ketoconazole on Candida albicans.
    Antimicrob Agents Chemother. 1982 Jun;21(6):912-8 PMID: 6287929
  23. Effect of ketoconazole on isolated mitochondria from Candida albicans.
    Antimicrob Agents Chemother. 1982 Jun;21(6):919-24 PMID: 6287930
  24. The mitochondrial genotype can influence nuclear gene expression in yeast.
    Science. 1987 Jan 30;235(4788):576-80 PMID: 3027892
  25. Regulation of early enzymes of ergosterol biosynthesis in Saccharomyces cerevisiae.
    Biochem J. 1986 Dec 1;240(2):541-7 PMID: 2880580
  26. Isolation and analysis of ketoconazole resistant mutants of Saccharomyces cerevisiae.
    J Med Vet Mycol. 1988 Jun;26(3):153-62 PMID: 3050008
  27. Genetic and physiological analysis of azole sensitivity in Saccharomyces cerevisiae.
    J Med Vet Mycol. 1989;27(6):397-406 PMID: 2560793
  28. 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 Bacteriol. 1990 Nov;69(5):692-6 PMID: 2276986
  29. Characterization of an azole-resistant Candida glabrata isolate.
    Antimicrob Agents Chemother. 1992 Dec;36(12):2602-10 PMID: 1482129
  30. Fluconazole resistance in Candida glabrata.
    Antimicrob Agents Chemother. 1993 Sep;37(9):1962-5 PMID: 8239613
  31. Fluconazole resistance due to energy-dependent drug efflux in Candida glabrata.
    Antimicrob Agents Chemother. 1995 Aug;39(8):1696-9 PMID: 7486903
  32. Deletion of the Candida glabrata ERG3 and ERG11 genes: effect on cell viability, cell growth, sterol composition, and antifungal susceptibility.
    Antimicrob Agents Chemother. 1995 Dec;39(12):2708-17 PMID: 8593007
  33. Sterol esterification in yeast: a two-gene process.
    Science. 1996 May 31;272(5266):1353-6 PMID: 8650549
  34. The changing face of candidemia: emergence of non-Candida albicans species and antifungal resistance.
    Am J Med. 1996 Jun;100(6):617-23 PMID: 8678081
  35. Positive and negative regulation of a sterol biosynthetic gene (ERG3) in the post-squalene portion of the yeast ergosterol pathway.
    FEBS Lett. 1996 Aug 26;392(2):161-5 PMID: 8772195
  36. Isolation and characterization of fluconazole- and amphotericin B-resistant Candida albicans from blood of two patients with leukemia.
    Antimicrob Agents Chemother. 1997 Jan;41(1):196-9 PMID: 8980781
  37. Resistance to fluconazole and cross-resistance to amphotericin B in Candida albicans from AIDS patients caused by defective sterol delta5,6-desaturation.
    FEBS Lett. 1997 Jan 2;400(1):80-2 PMID: 9000517
  38. Molecular biological characterization of an azole-resistant Candida glabrata isolate.
    Antimicrob Agents Chemother. 1997 Oct;41(10):2229-37 PMID: 9333053
  39. Fluconazole resistance associated with drug efflux and increased transcription of a drug transporter gene, PDH1, in Candida glabrata.
    Antimicrob Agents Chemother. 1998 Jul;42(7):1695-701 PMID: 9661006
  40. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans.
    Clin Microbiol Rev. 1999 Jan;12(1):80-96 PMID: 9880475
  41. In-vitro resistance to azoles associated with mitochondrial DNA deficiency in Candida glabrata.
    J Med Microbiol. 1999 Jul;48(7):663-70 PMID: 10403417
  42. Cloning, sequencing, expression and allelic sequence diversity of ERG3 (C-5 sterol desaturase gene) in Candida albicans.
    Gene. 1999 Aug 5;236(1):43-51 PMID: 10433965
  43. Rhodamine 6G efflux for the detection of CDR1-overexpressing azole-resistant Candida albicans strains.
    J Antimicrob Chemother. 1999 Jul;44(1):27-31 PMID: 10459807
  44. A simple method for the isolation and purification of total lipides from animal tissues.
    J Biol Chem. 1957 May;226(1):497-509 PMID: 13428781
  45. Modulation of fluconazole sensitivity by the interaction of mitochondria and erg3p in Saccharomyces cerevisiae.
    J Antimicrob Chemother. 2000 Aug;46(2):191-7 PMID: 10933640
Article Info
Journal
Antimicrobial agents and chemotherapy
Abbr.
Antimicrob Agents Chemother
ISSN
0066-4804
Published
2004-05-00
Pages
1788-96
Language
English
Region
United States
NLM ID
0315061
PMCID
PMC400549
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]