Abc1p is a multidrug efflux transporter that tips the balance in favor of innate azole resistance in Candida krusei

Antimicrobial Agents and Chemotherapy

Volumn 53, Issue 2, 2009, Pages 354-369

  Lamping, Erwin ^a   Ranchod, Amrita ^a   Nakamura, Kenjirou ^b   Tyndall, Joel D A ^a   Niimi, Kyoko ^a   Holmes, Ann R ^a   Niimi, Masakazu ^c   Cannon, Richard D ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b NIPPON DENTAL UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; ABC TRANSPORTER; ABC TRANSPORTER A1; AMPHOTERICIN B; AUREOBASIDIN A; CERULENIN; CYCLOHEXIMIDE; CYTOCHALASIN D; DOXYCYCLINE; FLUCONAZOLE; FLUCYTOSINE; FUNGAL PROTEIN; KETOCONAZOLE; LATRUNCULIN A; MONENSIN; NIGERICIN; NYSTATIN; PROTEIN ABC1P; PROTEIN ERG11P; PYRROLE; RHODAMINE 123; TERBINAFINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UPC2P; TRIFLUOPERAZINE; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ANTIFUNGAL RESISTANCE; ARTICLE; CANDIDA KRUSEI; CONTROLLED STUDY; DNA SEQUENCE; DRUG SENSITIVITY; DRUG TARGETING; ERG11 GENE; FUNGAL GENE; FUNGAL STRAIN; GENE EXPRESSION; GENE FREQUENCY; GENE ISOLATION; GENE SEQUENCE; INVERSE POLYMERASE CHAIN REACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; YEAST;

AMINO ACID SEQUENCE; ANIMALS; ANTIFUNGAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; AZOLES; BLOTTING, NORTHERN; BLOTTING, SOUTHERN; CANDIDA; CANDIDIASIS; CELL MEMBRANE; CHROMOSOMES, FUNGAL; DRUG RESISTANCE, FUNGAL; ENDOPLASMIC RETICULUM; HUMANS; PHENOTYPE; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE;

EID: 59749098790     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01095-08     Document Type: Article

References (56)

1. Akins, R. A. 2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43:285-318.
2. Anderson, J. B. 2005. Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat. Rev. Microbiol. 3:547-556.
3. Cannon, R. D., E. Lamping, A. R. Holmes, K. Niimi, K. Tanabe, M. Niimi, and B. C. Monk. 2007. Candida albicans drug resistance another way to cope with stress. Microbiology 153:3211-3217.
4. Clark, F. S., T. Parkinson, C. A. Hitchcock, and N. A. Gow. 1996. Correlation between rhodamine 123 accumulation and azole sensitivity in Candida species: possible role for drug efflux in drug resistance. Antimicrob. Agents Chemother. 40:419-425.
5. Cowen, L. E., and S. Lindquist. 2005. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309:2185-2189.
6. Cruz, M. C., A. L. Goldstein, J. R. Blankenship, M. Del Poeta, D. Davis, M. E. Cardenas, J. R. Perfect, J. H. McCusker, and J. Heitman. 2002. Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J. 21:546-559.
7. Decottignies, A., A. M. Grant, J. W. Nichols, H. de Wet, D. B. McIntosh, and A. Goffeau. 1998. ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem. 273:12612- 12622.
8. de Micheli, M., J. Bille, C. Schueller, and D. Sanglard. 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.
9. Eddine, A. N., J. P. von Kries, M. V. Podust, T. Warrier, S. H. Kaufmann, and L. M. Podust. 2008. X-ray structure of 4,4′- dihydroxybenzophenone mimicking sterol substrate in the active site of sterol 14α-demethylase (CYP51). J. Biol. Chem. 283:15152-15159.
10. Ernst, R., P. Kueppers, C. M. Klein, T. Schwarzmueller, K. Kuchler, and L. Schmitt. 2008. A mutation of the H-loop selectively affects rhodamine transport by the yeast multidrug ABC transporter Pdr5. Proc. Natl. Acad. Sci. USA 105:5069-5074.
11. Fukuoka, T., D. A. Johnston, C. A. Winslow, M. J. de Groot, C. Burt, C. A. Hitchcock, and S. G. Filler. 2003. Genetic basis for differential activities of fluconazole and voriconazole against Candida krusei. Antimicrob. Agents Chemother. 47:1213-1219.
12. Grant, S. M., and S. P. Clissold. 1990. Fluconazole. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic potential in superficial and systemic mycoses. Drugs 39:877-916.
13. Guinea, J., M. Sanchez-Somolinos, O. Cuevas, T. Pelaez, and E. Bouza. 2006. Fluconazole resistance mechanisms in Candida krusei: the contribution of efflux-pumps. Med. Mycol. 44:575-578.
14. Holmes, A. R., S. Tsao, S. W. Ong, E. Lamping, K. Niimi, B. C. Monk, M. Niimi, A. Kaneko, B. R. Holland, J. Schmid, and R. D. Cannon. 2006. Heterozygosity and functional allelic variation in the Candida albicans efflux pump genes CDR1 and CDR2. Mol. Microbiol. 62:170-186.
15. Jacobsen, M. D., N. A. Gow, M. C. Maiden, D. J. Shaw, and F. C. Odds. 2007. Strain typing and determination of population structure of Candida krusei by multilocus sequence typing. J. Clin. Microbiol. 45:317-323.
16. Katiyar, S. K., and T. D. Edlind. 2001. Identification and expression of multidrug resistance-related ABC transporter genes in Candida krusei. Med. Mycol. 39:109-116.
17. Katzmann, D. J., T. C. Hallstrom, Y. Mahe, and W. S. Moye-Rowley. 1996. Multiple Pdr1p/Pdr3p binding sites are essential for normal expression of the ATP binding cassette transporter protein-encoding gene PDR5. J. Biol. Chem. 271:23049-23054.
18. Kelly, S. L., A. Arnoldi, and D. E. Kelly. 1993. Molecular genetic analysis of azole antifungal mode of action. Biochem. Soc. Trans. 21:1034-1038.
19. Kontoyiannis, D. P., and R. E. Lewis. 2002. Antifungal drug resistance of pathogenic fungi. Lancet 359:1135-1144.
20. Lamping, E., B. C. Monk, K. Niimi, A. R. Holmes, S. Tsao, K. Tanabe, M. Niimi, Y. Uehara, and R. D. Cannon. 2007. Characterization of three classes of membrane proteins involved in fungal azole resistance by functional hyperexpression in Saccharomyces cerevisiae. Eukaryot. Cell 6:1150-1165.
21. Lengeler, K. B., G. M. Cox, and J. Heitman. 2001. Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect. Immun. 69:115-122.
22. Litvintseva, A. P., X. Lin, I. Templeton, J. Heitman, and T. G. Mitchell. 2007. Many globally isolated AD hybrid strains of Cryptococcus neoformans originated in Africa. PLoS Pathog. 3:e114.
23. MacPherson, S., B. Akache, S. Weber, X. De Deken, M. Raymond, and B. Turcotte. 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.
24. MacPherson, S., M. Larochelle, and B. Turcotte. 2006. A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol. Mol. Biol. Rev. 70:583-604.
25. Marichal, P., J. Gorrens, M. C. Coene, L. Le Jeune, and H. Vanden Bossche. 1995. Origin of differences in susceptibility of Candida krusei to azole antifungal agents. Mycoses 38:111-117.
26. Mukherjee, P. K., D. J. Sheehan, C. A. Hitchcock, and M. A. Ghannoum. 2005. Combination treatment of invasive fungal infections. Clin. Microbiol. Rev. 18:163-194.
27. Nakayama, H., K. Tanabe, M. Bard, W. Hodgson, S. Wu, D. Takemori, T. Aoyama, N. S. Kumaraswami, L. Metzler, Y. Takano, H. Chibana, and M. Niimi. 2007. The Candida glabrata putative sterol transporter gene CgAUS1 protects cells against azoles in the presence of serum. J. Antimicrob. Chemother. 60:1264-1272.
28. Niimi, K., D. R. Harding, R. Parshot, A. King, D. J. Lun, A. Decottignies, M. Niimi, S. Lin, R. D. Cannon, A. Goffeau, and B. C. Monk. 2004. Chemosensitization of fluconazole resistance in Saccharomyces cerevisiae and pathogenic fungi by a D-octapeptide derivative. Antimicrob. Agents Chemother. 48:1256-1271.
29. Niimi, M., Y. Nagai, K. Niimi, S. Wada, R. D. Cannon, Y. Uehara, and B. C. Monk. 2002. Identification of two proteins induced by exposure of the pathogenic fungus Candida glabrata to fluconazole. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 782:245-252.
30. Odds, F. C. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1.
31. Oliver, B. G., J. L. Song, J. H. Choiniere, and T. C. White. 2007. cis-Acting elements within the Candida albicans ERG11 promoter mediate the azole response through transcription factor Upc2p. Eukaryot. Cell 6:2231-2239.
32. Orozco, A. S., L. M. Higginbotham, C. A. Hitchcock, T. Parkinson, D. Falconer, A. S. Ibrahim, M. A. Ghannoum, and S. G. Filler. 1998. Mechanism of fluconazole resistance in Candida krusei. Antimicrob. Agents Chemother. 42:2645-2649.
33. Pfaller, M. A., and D. J. Diekema. 2002. Role of sentinel surveillance of candidemia: trends in species distribution and antifungal susceptibility. J. Clin. Microbiol. 40:3551-3557.
34. Pfaller, M. A., D. J. Diekema, D. L. Gibbs, V. A. Newell, E. Nagy, S. Dobiasova, M. Rinaldi, R. Barton, and A. Veselov. 2008. Candida krusei, a multidrug-resistant opportunistic fungal pathogen: geographic and temporal trends from the ARTEMIS DISK Antifungal Surveillance Program, 2001 to 2005. J. Clin. Microbiol. 46:515-521.
35. Pfaller, M. A., S. A. Messer, L. Boyken, S. Tendolkar, R. J. Hollis, and D. J. Diekema. 2008. Selection of a surrogate agent (fluconazole or voriconazole) for initial susceptibility testing of posaconazole against Candida spp.: results from a global antifungal surveillance program. J. Clin. Microbiol. 46:551-559.
36. Podust, L. M., T. L. Poulos, and M. R. Waterman. 2001. Crystal structure of cytochrome P450 14α-sterol demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors. Proc. Natl. Acad. Sci. USA 98:3068-3073.
37. Reuss, O., A. Vik, R. Kolter, and J. Morschhauser. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119-127.
38. Rex, J. H., M. G. Rinaldi, and M. A. Pfaller. 1995. Resistance of Candida species to fluconazole. Antimicrob. Agents Chemother. 39:1-8.
39. Rost, B., G. Yachdav, and J. Liu. 2004. The PredictProtein server. Nucleic Acids Res. 32:W321-W326.
40. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. 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.
42. Sanglard, D., F. Ischer, L. Koymans, and J. Bille. 1998. Amino acid substitutions in the cytochrome P-450 lanosterol 14α-demethylase (CYP51A1) from azole-resistant Candida albicans clinical isolates contribute to resistance to azole antifungal agents. Antimicrob. Agents Chemother. 42:241-253.
43. Shemer, R., Z. Weissman, N. Hashman, and D. Kornitzer. 2001. A highly polymorphic degenerate microsatellite for molecular strain typing of Candida krusei. Microbiology 147:2021-2028.
44. Song, J. L., J. B. Harry, R. T. Eastman, B. G. Oliver, and T. C. White. 2004. The Candida albicans lanosterol 14-α-demethylase (ERG11) gene promoter is maximally induced after prolonged growth with antifungal drugs. Antimicrob. Agents Chemother. 48:1136-1144.
45. Tanabe, K., E. Lamping, K. Adachi, Y. Takano, K. Kawabata, Y. Shizuri, M. Niimi, and Y. Uehara. 2007. Inhibition of fungal ABC transporters by unnarmicin A and unnarmicin C, novel cyclic peptides from marine bacterium. Biochem. Biophys. Res. Commun. 364:990-995.
46. Thakur, J. K., H. Arthanari, F. Yang, S. J. Pan, X. Fan, J. Breger, D. P. Frueh, K. Gulshan, D. K. Li, E. Mylonakis, K. Struhl, W. S. Moye-Rowley, B. P. Cormack, G. Wagner, and A. M. Naar. 2008. A nuclear receptor-like pathway regulating multidrug resistance in fungi. Nature 452:604-609.
47. Torres, E. M., T. Sokolsky, C. M. Tucker, L. Y. Chan, M. Boselli, M. J. Dunham, and A. Amon. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317:916-924.
48. 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.
49. Venkateswarlu, K., D. W. Denning, and S. L. Kelly. 1997. Inhibition and interaction of cytochrome P450 of Candida krusei with azole antifungal drugs. J. Med. Vet. Mycol. 35:19-25.
50. Venkateswarlu, K., D. W. Denning, N. J. Manning, and S. L. Kelly. 1996. Reduced accumulation of drug in Candida krusei accounts for itraconazole resistance. Antimicrob. Agents Chemother. 40:2443-2446.
51. Vermitsky, J. P., and T. D. Edlind. 2004. Azole resistance in Candida glabrata: coordinate upregulation of multidrug transporters and evidence for a Pdr1-like transcription factor. Antimicrob. Agents Chemother. 48:3773-3781.
52. Wada, S., K. Tanabe, A. Yamazaki, M. Niimi, Y. Uehara, K. Niimi, E. Lamping, R. D. Cannon, and B. C. Monk. 2005. Phosphorylation of candida glabrata ATP-binding cassette transporter Cdr1p regulates drug efflux activity and ATPase stability. J. Biol. Chem. 280:94-103.
53. Wang, H. P., Y. F. Yen, W. S. Chen, Y. L. Chou, C. Y. Tsai, H. N. Chang, and C. T. Chou. 2007. An unusual case of Candida tropicalis and Candida krusei arthritis in a patient with acute myelogenous leukemia before chemotherapy. Clin. Rheumatol. 26:1195-1197.
54. Whelan, W. L., and K. J. Kwon-Chung. 1988. Auxotrophic heterozygosities and the ploidy of Candida parapsilosis and Candida krusei. J. Med. Vet. Mycol. 26:163-171.
55. White, T. C., K. A. Marr, and R. A. Bowden. 1998. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev. 11:382-402.
56. Xiong, Q., S. A. Hassan, W. K. Wilson, X. Y. Han, G. S. May, J. J. Tarrand, and S. P. Matsuda. 2005. Cholesterol import by Aspergillus fumigatus and its influence on antifungal potency of sterol biosynthesis inhibitors. Antimicrob. Agents Chemother. 49:518-524.