Reversal of antifungal resistance mediated by ABC efflux pumps from Candida albicans functionally expressed in yeast

International Journal of Antimicrobial Agents

Volumn 22, Issue 3, 2003, Pages 291-300

  Schuetzer Muehlbauer, Manuela ^a   Willinger, Birgit ^b   Egner, Ralf ^a   Ecker, Gerhard ^b   Kuchler, Karl ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

ABC pumps; Candida albicans; Clinical isolates; Multidrug resistance reversal; Saccharomyces cerevisiae

Indexed keywords

ABC TRANSPORTER; FLUCONAZOLE; ITRACONAZOLE; KETOCONAZOLE; PROPAFENONE; PYRROLE DERIVATIVE; TACROLIMUS; TERBINAFINE; VORICONAZOLE;

ANTIBIOTIC SENSITIVITY; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; FUNGAL STRAIN; FUNGUS GROWTH; GROWTH INHIBITION; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

EID: 0041833313     PISSN: 09248579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0924-8579(03)00213-9     Document Type: Article

References (63)

1. Schüller C., Bauer B.E., Kuchler K. Inventory and evolution of fungal ABC protein genes. Holland S.M., Coole S., Kuchler K., Higgins C. ABC proteins from bacteria to man. 2002;279-293 Academic Press, Elsevier Science, London.
2. Bauer B.E., Schüller C., Kuchler K. Fungal ABC proteins in clinical drug resistance and cellular detoxification. Holland S.M., Coole S., Kuchler K., Higgins C. ABC proteins from bacteria to man. 2003;295-316 Academic Press, Elsevier Science, London.
3. Bauer B.E., Wolfger H., Kuchler K. Inventory and function of yeast ABC proteins: about sex, stress, pleiotropic drug and heavy metal resistance. Biochim. Biophys. Acta. 1461:1999;217-236.
4. Decottignies A., Goffeau A. Complete inventory of the yeast ABC proteins. Nat. Genet. 15:1997;137-145.
5. Bastert J., Schaller M., Korting H.C., Evans E.G. Current and future approaches to antimycotic treatment in the era of resistant fungi and immunocompromised hosts. Int. J. Antimicrob. Agents. 17:2001;81-91.
6. Garber G. An overview of fungal infections. Drugs. 61:2001;1-12.
7. Powderly W.G. Resistant candidiasis. AIDS Res. Hum. Retroviruses. 10:1994;925-929.
8. Kontoyiannis D.P., Lewis R.E. Antifungal drug resistance of pathogenic fungi. Lancet. 359:2002;1135-1144.
9. White T.C., Holleman S., Dy F., Mirels L.F., Stevens D.A. Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob. Agents Chemother. 46:2002;1704-1713.
10. Sanglard D., Odds F.C. Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect. Dis. 2:2002;73-85.
11. Prasad R., Dewergifosse P., Goffeau A., Balzi E. Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr. Genet. 27:1995;320-329.
12. Sanglard D., Kuchler K., Ischer F., Pagani J.L., Monod M., Bille J. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob. Agents Chemother. 39:1995;2378-2386.
13. Sanglard D., Ischer F., Monod M., Bille J. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology. 143:1997;405-416.
14. Fling M.E., Kopf J., Tamarkin A., Gorman J.A., Smith H.A., Koltin Y. Analysis of a Candida albicans gene that encodes a novel mechanism for resistance to benomyl and methotrexate. Mol. Gen. Genet. 227:1991;318-329.
15. Balan I., Alarco A.M., Raymond M. The Candida albicans CDR3 gene codes for an opaque-phase ABC transporter. J. Bacteriol. 179:1997;7210-7218.
16. Franz R., Michel S., Morschhauser J. A fourth gene from the Candida albicans CDR family of ABC transporters. Gene. 220:1998;91-98.
17. Smriti, Krishnamurthy S., Dixit B.L., Gupta C.M., Milewski S., Prasad R. ABC transporters Cdr1p, Cdr2p and Cdr3p of a human pathogen Candida albicans are general phospholipid translocators. Yeast. 19:2002;303-318.
18. Balzi E., Wang M., Leterme S., Van D.L., Goffeau A. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269:1994;2206-2214.
19. Bissinger P.H., Kuchler K. Molecular cloning and expression of the Saccharomyces cerevisiae STS1 gene product. A yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem. 269:1994;4180-4186.
20. Egner R., Mahé Y., Pandjaitan R., Huter V., Lamprecht A., Kuchler K. ATP binding cassette transporters in yeast: from mating to multidrug resistance. Rothman S. Membrane protein transport. 2:1995;57-96 JAI Press, Greenwich.
21. Delaveau T., Delahodde A., Carvajal E., Subik J., Jacq C. PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls the multidrug resistance phenomenon. Mol. Gen. Genet. 244:1994;501-511.
22. Mamnun Y.M., Pandjaitan R., Mahé Y., Delahodde A., Kuchler K. The yeast zinc finger regulators Pdr1p and Pdr3p control pleiotropic drug resistance (PDR) as homo- and heterodimers in vivo. Mol. Microbiol. 46:2002;1429-1440.
23. Wolfger H., Mamnun Y.M., Kuchler K. Fungal ABC proteins: pleiotropic drug resistance, stress response and cellular detoxification. Res. Microbiol. 152:2001;375-389.
24. Krishnamurthy S., Gupta V., Prasad R., Panwar S.L. Expression of CDR1, a multidrug resistance gene of Candida albicans: transcriptional activation by heat shock, drugs and human steroid hormones. FEMS Microbiol. Lett. 160:1998;191-197.
25. Micheli M., Bille J., Schüller C., Sanglard D. 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. 43:2002;1197-1214.
26. Sanglard D. Resistance of human fungal pathogens to antifungal drugs. Curr. Opin. Microbiol. 5:2002;379-385.
27. Demeule M., Wenger R.M., Beliveau R. Molecular interactions of cyclosporin A with P-glycoprotein. Photolabeling with cyclosporin derivatives. J. Biol. Chem. 272:1997;6647-6652.
28. Jachez B., Boesch D., Grassberger M.A., Loor F. Reversion of the P-glycoprotein-mediated multidrug resistance of cancer cells by FK-506 derivatives. Anticancer Drugs. 4:1993;223-229.
29. Egashira M., Kawamata N., Sugimoto K., Kaneko T., Oshimi K. P-glycoprotein expression on normal and abnormally expanded natural killer cells and inhibition of P-glycoprotein function by cyclosporin A and its analogue, PSC833. Blood. 93:1999;599-606.
30. Marchetti O., Moreillon P., Glauser M.P., Bille J., Sanglard D. Potent synergism of the combination of fluconazole and cyclosporine in Candida albicans. Antimicrob. Agents Chemother. 44:2000;2373-2381.
31. Perea S., Gonzalez G., Fothergill A.W., Sutton D.A., Rinaldi M.G. in vitro activities of terbinafine in combination with fluconazole, itraconazole, voriconazole, and posaconazole against clinical isolates of Candida glabrata with decreased susceptibility to azoles. J. Clin. Microbiol. 40:2002;1831-1833.
32. Ryder N.S., Leitner I. Synergistic interaction of terbinafine with triazoles or amphotericin B against Aspergillus species. Med. Mycol. 39:2001;91-95.
33. Cruz M.C., Goldstein A.L., Blankenship J.R., et al. Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J. 21:2002;546-559.
34. Petranyi G., Ryder N.S., Stütz A. Allylamine derivatives: new class of synthetic antifungal agents inhibiting fungal squalene epoxidase. Science. 224:1984;1239-1241.
35. Chiba P., Ecker G., Schmid D., et al. Structural requirements for activity of propafenone-type modulators in P-glycoprotein-mediated multidrug resistance. Mol. Pharmacol. 49:1996;1122-1130.
36. Kaiser C., Michaelis S., Mitchell A. Methods in yeast genetics. A laboratory course manual. 1994;Cold Spring Harbor Laboratory Press, New York.
37. Sikorski R.S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:1989;19-27.
38. Egner R., Rosenthal F.E., Kralli A., Sanglard D., Kuchler K. Genetic separation of FK506 susceptibility and drug transport in the yeast Pdr5 ATP-binding cassette multidrug resistance transporter. Mol. Biol. Cell. 9:1998;523-543.
39. Auger P., Dumas C., Joly J. Interactions of serotypes A and B of Candida albicans in mice. Sabouraudia. 21:1983;173-178.
40. Auger P., Dumas C., Joly J. A study of 666 strains of Candida albicans: correlation between serotype and susceptibility to 5-fluorocytosine. J. Infect. Dis. 139:1979;590-594.
41. Rippon J.W. Medical mycology. 1988;W.B. Saunders.
42. Sanglard D., Ischer F., Monod M., Bille J. Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob. Agents Chemother. 40:1996;2300-2305.
43. Grey M., Brendel M. A ten-minute protocol for transforming Saccharomyces cerevisiae by electroporation. Curr. Genet. 22:1992;335-336.
44. Wach A., Brachat A., Alberti-Segui C., Rebischung C., Philippsen P. Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast. 13:1997;1065-1075.
45. Egner R., Bauer B.E., Kuchler K. The transmembrane domain 10 of the yeast Pdr5p ABC antifungal efflux pump determines both substrate specificity and inhibitor susceptibility. Mol. Microbiol. 35:2000;1255-1263.
46. Ecker G., Chiba P., Hitzler M., et al. Structure-activity relationship studies on benzofuran analogs of propafenone-type modulators of tumor cell multidrug resistance. J. Med. Chem. 39:1996;4767-4774.
47. Nakamura K., Niimi M., Niimi K., et al. Functional expression of Candida albicans drug efflux pump Cdr1p in a Saccharomyces cerevisiae strain deficient in membrane transporters. Antimicrob. Agents Chemother. 45:2001;3366-3374.
48. Schuetzer-Muehlbauer M., Willinger B., Krapf G., Enzinger S., Presterl E., Kuchler K. The Candida albicans Cdr2p ATP-binding cassette (ABC) transporter confers resistance to caspofungin. Mol. Microbiol. 48:2003;225-235.
49. Rao U.S., Scarborough G.A. Direct demonstration of high affinity interactions of immunosuppressant drugs with the drug binding site of the human P-glycoprotein. Mol. Pharmacol. 45:1994;773-776.
50. Leber R., Zenz R., Schrottner K., Fuchsbichler S., Puhringer B., Turnowsky F. A novel sequence element is involved in the transcriptional regulation of expression of the ERG1 (squalene epoxidase) gene in Saccharomyces cerevisiae. Eur. J. Biochem. 268:2001;914-924.
51. Favre B., Didmon M., Ryder N.S. Multiple amino acid substitutions in lanosterol 14alpha-demethylase contribute to azole resistance in Candida albicans. Microbiology. 145:1999;2715-2725.
52. Favre B., Ryder N.S. Cloning and expression of squalene epoxidase from the pathogenic yeast Candida albicans. Gene. 189:1997;119-126.
53. Ryder N.S. Activity of terbinafine against serious fungal pathogens. Mycoses. 42:1999;115-119.
54. Weig M., Muller F.M. Synergism of voriconazole and terbinafine against Candida albicans isolates from human immunodeficiency virus-infected patients with oropharyngeal candidiasis. Antimicrob. Agents Chemother. 45:2001;966-968.
55. Del Poeta M., Cruz M.C., Cardenas M.E., Perfect J.R., Heitman J. Synergistic antifungal activities of bafilomycin A(1), fluconazole, and the pneumocandin MK-0991/caspofungin acetate (L-743,873) with calcineurin inhibitors FK506 and L-685,818 against Cryptococcus neoformans. Antimicrob. Agents Chemother. 44:2000;739-746.
56. Henry K.W., Cruz M.C., Katiyar S.K., Edlind T.D. Antagonism of azole activity against Candida albicans following induction of multidrug resistance genes by selected antimicrobial agents. Antimicrob. Agents Chemother. 43:1999;1968-1974.
57. Maesaki S., Hossain M.A., Miyazaki Y., Tomono K., Tashiro T., Kohno S. Efficacy of FK463, a (1,3)-beta-D-glucan synthase inhibitor, in disseminated azole-resistant Candida albicans infection in mice. Antimicrob. Agents Chemother. 44:2000;1728-1730.
58. Chiba P., Rebitzer S., Richter E., Hitzler M., Ecker G. Synthesis and pharmacological activity of the stereoisomers of GP-88, a propafenone-type modulator of multidrug resistance. Bioorg. Med. Chem. Lett. 8:1998;829-832.
59. Chiba P., Burghofer S., Richter E., Tell B., Moser A., Ecker G. Synthesis, pharmacologic activity, and structure-activity relationships of a series of propafenone-related modulators of multidrug resistance. J. Med. Chem. 38:1995;2789-2793.
60. Leonard G.D., Polgar O., Bates S.E. ABC transporters and inhibitors: new targets, new agents. Curr. Opin. Invest. Drugs. 3:2002;1652-1659.
61. Sikic B.I., Fisher G.A., Lum B.L., Halsey J., Beketic-Oreskovic L., Chen G. Modulation and prevention of multidrug resistance by inhibitors of P-glycoprotein. Cancer Chemother. Pharmacol. 40:(Suppl.):1997;S13-S19.
62. Maesaki S., Marichal P., Hossain M.A., Sanglard D., Vanden Bossche H., Kohno S. Synergic effects of tactolimus and azole antifungal agents against azole-resistant Candida albicans strains. J. Antimicrob. Chemother. 42:1998;747-753.
63. Lee M.D., Galazzo J.L., Staley A.L., et al. Microbial fermentation-derived inhibitors of efflux-pump-mediated drug resistance. Farmaco. 56:2001;81-85.