Loss of mitochondrial functions associated with azole resistance in Candida glabrata results in enhanced virulence in mice

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 5, 2011, Pages 1852-1860

  Ferrari, Sélène ^a   Sanguinetti, Maurizio ^b   De Bernardis, Flavia ^c   Torelli, Riccardo ^b   Posteraro, Brunella ^b   Vandeputte, Patrick ^a   Sanglard, Dominique ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b CATHOLIC UNIVERSITY   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; FLUCONAZOLE; ITRACONAZOLE; VORICONAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BACTERIUM ISOLATE; CANDIDA GLABRATA; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE EXPRESSION; IN VITRO STUDY; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RECEPTOR UPREGULATION; STRESS;

ANIMALS; AZOLES; CANDIDA GLABRATA; COMPUTATIONAL BIOLOGY; DRUG RESISTANCE, FUNGAL; FEMALE; GENE EXPRESSION REGULATION, FUNGAL; MICE; MICE, INBRED BALB C; MICROARRAY ANALYSIS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIRULENCE;

EID: 79952413922     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01271-10     Document Type: Article

References (44)

1. Andersson, D. I. 2006. The biological cost of mutational antibiotic resistance: any practical conclusions? Curr. Opin. Microbiol. 9:461-465.
2. Bethea, E. K., B. J. Carver, A. E. Montedonico, and T. B. Reynolds. 2010. The inositol regulon controls viability in Candida glabrata. Microbiology 156:452-462.
3. Bouchara, J. P., et al. 2000. In-vivo selection of an azole-resistant petite mutant of Candida glabrata. J. Med. Microbiol. 49:977-984.
4. Brisse, S., et al. 2009. Uneven distribution of mating types among genotypes of Candida glabrata isolates from clinical samples. Eukaryot. Cell 8:287-295.
5. Brun, S., et al. 2003. Relationships between respiration and susceptibility to azole antifungals in Candida glabrata. Antimicrob. Agents Chemother. 47:847-853.
6. Brun, S., et al. 2004. Mechanisms of azole resistance in petite mutants of Candida glabrata. Antimicrob. Agents Chemother. 48:1788-1796.
7. Brun, S., et al. 2005. Biological consequences of petite mutations in Candida glabrata. J. Antimicrob. Chemother. 56:307-314.
8. Clinical and Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard, 3rd ed. CLSI document M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA.
9. De Bernardis, F., R. Lorenzini, and A. Cassone. 1999. Rat model of Candida vaginal infection, p. 735-740. In O. Zak and M. Sande (ed.), Handbook of animals models of infection. Academic Press, New York, NY.
10. De Bernardis, F., et al. 2000. Local anticandidal immune responses in a rat model of vaginal infection by and protection against Candida albicans. Infect. Immun. 68:3297-3304.
11. DeRisi, J., et al. 2000. Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants. FEBS Lett. 470:156-160.
12. Devaux, F., et al. 2001. An artificial transcription activator mimics the genome-wide properties of the yeast Pdr1 transcription factor. EMBO Rep. 2:493-498. (Pubitemid 32611345)
13. Dujon, B., et al. 2004. Genome evolution in yeasts. Nature 430:35-44. (Pubitemid 38915217)
14. Ferrari, S., et al. 2009. Gain of function mutations in CgPDR1 of Candida glabrata not only mediate antifungal resistance but also enhance virulence. PLoS Pathog. 5:e1000268.
15. Ferrari, S., M. Sanguinetti, R. Torelli, B. Posteraro, and D. Sanglard. Contribution of CgPDR1-regulated genes in enhanced virulence of azole-resistant Candida glabrata. PLoS One 6:e17589.
16. Gagnon-Arsenault, I., L. Parise, J. Tremblay, and Y. Bourbonnais. 2008. Activation mechanism, functional role and shedding of glycosylphosphatidylinositol-anchored Yps1p at the Saccharomyces cerevisiae cell surface. Mol. Microbiol. 69:982-993.
17. Ju, D., X. Wang, S.-W. Ha, J. Fu, and Y. Xie. 2010. Inhibition of proteasomal degradation of Rpn4 impairs nonhomologous end-joining repair of DNA double-strand breaks. PLoS One 5:e9877.
18. Jung, U. S., A. K. Sobering, M. J. Romeo, and D. E. Levin. 2002. Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase. Mol. Microbiol. 46:781-789.
19. Kamran, M., et al. 2004. Inactivation of transcription factor gene ACE2 in the fungal pathogen Candida glabrata results in hypervirulence. Eukaryot. Cell 3:546-552. (Pubitemid 38497992)
20. Kaur, R., B. Ma, and B. P. Cormack. 2007. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. U. S. A. 104:7628-7633.
21. Knudsen, L. F., and J. M. Curtis. 1947. The use of the angular transformation in biological assays. J. Am. Stat. Assoc. 42:282-296.
22. Maisnier-Patin, S., O. G. Berg, L. Liljas, and D. I. Andersson. 2002. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol. Microbiol. 46:355-366.
23. Miyazaki, H., et al. 1998. Fluconazole resistance associated with drug efflux and increased transcription of a drug transporter gene, PDH1, in Candida glabrata. Antimicrob. Agents Chemother. 42:1695-1701.
24. Moskvina, E., C. Schuller, C. T. Maurer, W. H. Mager, and H. Ruis. 1998. A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast 14:1041-1050. (Pubitemid 28370774)
25. Muller, H., C. Hennequin, J. Gallaud, B. Dujon, and C. Fairhead. 2008. The asexual yeast Candida glabrata maintains distinct a and alpha haploid mating types. Eukaryot. Cell 7:848-858. (Pubitemid 351968828)
26. Orkwis, B. R., D. L. Davies, C. L. Kerwin, D. Sanglard, and D. D. Wykoff. 2010. Novel acid phosphatase in Candida glabrata suggests selective pressure and niche specialization in the phosphate signal transduction pathway. Genetics 186:885-895.
27. Perocchi, F., et al. 2006. Assessing systems properties of yeast mitochondria through an interaction map of the organelle. PLoS Genet. 2:e170.
28. Posteraro, B., et al. 2006. Azole resistance of Candida glabrata in a case of recurrent fungemia. J. Clin. Microbiol. 44:3046-3047.
29. Richard, G. F., A. Kerrest, I. Lafontaine, and B. Dujon. 2005. Comparative genomics of hemiascomycete yeasts: genes involved in DNA replication, repair, and recombination. Mol. Biol. Evol. 22:1011-1023.
30. Richardson, M., and C. Lass-Florl. 2008. Changing epidemiology of systemic fungal infections. Clin. Microbiol. Infect. 14(Suppl. 4):5-24.
31. Roetzer, A., et al. 2008. Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol. Microbiol. 69:603-620.
32. Rolfes, R. J. 2006. Regulation of purine nucleotide biosynthesis: in yeast and beyond. Biochem. Soc. Trans. 34:786-790.
33. Sanglard, D., F. Ischer, and J. Bille. 2001. Role of ATP-binding-cassette transporter genes in high-frequency acquisition of resistance to azole antifungals in Candida glabrata. Antimicrob. Agents Chemother. 45:1174-1183.
34. Sanglard, D., F. Ischer, D. Calabrese, P. A. Majcherczyk, and J. Bille. 1999. 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. 43:2753-2765.
35. Sanguinetti, M., et al. 2005. Mechanisms of azole resistance in clinical isolates of Candida glabrata collected during a hospital survey of antifungal resistance. Antimicrob. Agents Chemother. 49:668-679.
36. Stead, D., et al. 2005. Proteomic changes associated with inactivation of the Candida glabrata ACE2 virulence-moderating gene. Proteomics 5:1838-1848. (Pubitemid 40686229)
37. Thomas-Chollier, et al. 2008. RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 36:W119-W127.
38. Torelli, R., et al. 2008. The ATP-binding cassette transporter-encoding gene CgSNQ2 is contributor to the CgPdr1-dependent azole resistance in Candida glabrata. Mol. Microbiol. 68:186-201.
39. Traven, A., J. M. Wong, D. Xu, M. Sopta, and C. J. Ingles. 2001. Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial DNA mutant. J. Biol. Chem. 276:4020-4027.
40. Tsai, H. F., A. A. Krol, K. E. Sarti, and J. E. Bennett. 2006. Candida glabrata PDR1, a transcriptional regulator of a pleiotropic drug resistance network, mediates azole resistance in clinical isolates and petite mutants. Antimicrob. Agents Chemother. 50:1384-1392.
41. Tsai, H. F., et al. 2010. Microarray and molecular analyses of the azole resistance mechanism in Candida glabrata oropharyngeal isolates. Antimicrob. Agents Chemother. 54:3308-3317.
42. Vermitsky, J. P., et al. 2006. Pdr1 regulates multidrug resistance in Candida glabrata: gene disruption and genome-wide expression studies. Mol. Microbiol. 61:704-722.
43. Wilson, W. A., Z. Wang, and P. J. Roach. 2002. Systematic identification of the genes affecting glycogen storage in the yeast Saccharomyces cerevisiae. Mol. Cell Prot. 1:232-242.
44. Wimalasena, T. T., et al. 2008. Impact of the unfolded protein response upon genome-wide expression patterns, and the role of Hac1 in the polarized growth, of Candida albicans. Fungal Genet. Biol. 45:1235-1247.