Functional analysis of fungal drug efflux transporters by heterologous expression in Saccharomyces cerevisiae

Japanese Journal of Infectious Diseases

Volumn 58, Issue 1, 2005, Pages 1-7

  Niimi, Masakazu ^b   Wada, Shun Ichi ^b   Tanabe, Koichi ^b   Kaneko, Aki ^b   Takano, Yukie ^b   Umeyama, Takashi ^b   Hanoka, Nozomu ^b   Uehara, Yoshimasa ^b   Lamping, Erwin ^a   Niimi, Kyoko ^a   Tsao, Sarah ^a   Holmes, Ann R ^a   Monk, Brian C ^a   Cannon, Richard D ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; AMPHOTERICIN B; ANTIFUNGAL AGENT; CARRIER PROTEIN; CASPOFUNGIN; CYCLOHEXIMIDE; CYCLOSPORIN; ECHINOCANDIN; FLUCONAZOLE; GLYCOPROTEIN P; ITRACONAZOLE; KETOCONAZOLE; MEMBRANE PROTEIN; MICAFUNGIN; MILBEMYCIN; MULTIDRUG RESISTANCE PROTEIN 1; NYSTATIN; PYRROLE DERIVATIVE; RHODAMINE 6G; TACROLIMUS;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIFUNGAL ACTIVITY; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; CANDIDA ALBICANS; CANDIDA DUBLINIENSIS; CANDIDA GLABRATA; CANDIDA KRUSEI; CRYPTOCOCCUS NEOFORMANS; DRUG POTENTIATION; DRUG TRANSPORT; ENZYME ACTIVITY; FUNCTIONAL ASSESSMENT; FUNGAL VIRULENCE; GENE DELETION; GENE OVEREXPRESSION; GENETIC ENGINEERING; HOMOLOGOUS RECOMBINATION; HOST; HUMAN; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; MYCOSIS; NONHUMAN; PLASMID; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; UBIQUITINATION;

ANTIFUNGAL AGENTS; DRUG RESISTANCE, FUNGAL; GENE EXPRESSION; MEMBRANE TRANSPORT PROTEINS; SACCHAROMYCES CEREVISIAE;

EID: 20144365880     PISSN: 13446304     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (54)

1. Berman, J. and Sudbery, P. E. (2002): Candida albicans: a molecular revolution built on lessons from budding yeast. Nature Rev. Genet., 3, 918-930.
2. Magee, P. T., Gale, C., Berman, J. and Davis, D. (2003): Molecular genetics and genomic approaches to the study of medically important fungi. Infect. Immun., 71, 2299-2309.
3. Bruno, V. E. and Mitchell, A. P. (2004): Large-scale gene function analysis in Candida albicans. Trends Microbiol., 12, 157-161.
4. Niimi, M., Cannon, R. D. and Monk, B. C. (1999): Candida albicans pathogenicity: a proteomic perspective. Electrophoresis, 20, 2299-2308.
5. Kaneko, A., Umeyama, T., Hanaoka, N., Monk, B. C., Uehara, Y. and Niimi, M. (2004): Tandem affinity purification of the Candida albicans septin protein complex. Yeast, 21, 1025-1033.
6. Jones, T., Federspiel, N. A., Chibana, H., Dungan, J., Kalman, S., Magee, B. B., Newport, G., Thorstenson, Y. R., Agabian, N., Magee, P. T., Davis, R. W. and Scherer, S. (2004): The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA, 101, 7329-7334.
7. Sherman, D., Durrens, P., Beyne, E., Nikolski, M. and Jean-Luc Souciet for the Génolevures Consortium. (2004): Génolevures: comparative genomics and molecular evolution of hemiascomycetous yeasts. Nucleic Acids Res., 32, D315-D318.
8. Richardson, M. D. and Kokki, M. (2001): Therapeutic guidelines in systemic fungal infections. 2nd ed. Current Medical Literature, London.
9. Albertson, G. D., Niimi, M., Cannon, R. D. and Jenkinson, H. F. (1996): Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrob. Agents Chemother., 40, 2835-2841.
10. Maebashi, K., Niimi, M., Kudoh, M., Fischer, F. J., Makimura, K., Niimi, K., Piper, R. J., Uchida, K., Arisawa, M., Cannon, R. D. and Yamaguchi, H. (2001): Mechanisms of fluconazole resistance in Candida albicans isolates from Japanese AIDS patients. J. Antimicrob. Chemother., 47, 527-536.
11. Takakura, S., Fujihara, N., Saito, T., Kudo, T., Iinuma, Y. and Ichiyama, S. (2004): Japan Invasive Mycosis Surveillance Study Group. Clinical factors associated with fluconazole resistance and short-term survival in patients with Candida bloodstream infection. Eur. J. Clin. Microbiol. Infect., 23, 380-388.
12. White, T., Marr, K. A. and Bowden, R. A. (1998): Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev., 11, 382-402.
13. Sanglard, D. and Bille, J. (2002): Current understanding of the modes of action of and resistance mechanisms to conventional and emerging antifungal agents for treatment of Candida infections. p.349-383. In R. A. Calderone (ed.), Candida and Candidiasis. ASM Press, Washington, D.C.
14. Lupetti, A., Danesi, R., Campa, M., Del Tacca, M. and Kelly, S. (2002): Molecular basis of resistance to azole antifungals. Trends Mol. Med., 8, 76-81.
15. Kontoyiannis, D. P. and Lewis, R. E. (2002): Antifungal drug resistance of pathogenic fungi. Lancet, 359, 1135-1144.
16. Chau, A. S., Mendrick, C. A., Sabatelli, F. J., Loebenberg, D. and McNicholas, P. M. (2004): Application of realtime quantitative PCR to molecular analysis of Candida albicans strains exhibiting reduced susceptibility to azoles. Antimicrob. Agents Chemother., 48, 2124-2131.
17. White, T. C., Holleman, S., Dy, F., Mirels, L. F. and Stevens, D. A. (2002): Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob. Agents Chemother., 46, 1704-1713.
18. Rogers, P. D. and Barker, K. S. (2003): Genome-wide expression profile analysis reveals coordinately regulated genes associated with stepwise acquisition of azole resistance in Candida albicans clinical isolates. Antimicrob. Agents Chemother., 47, 1220-1227.
19. White, T. C. (1997): Increased mRNA levels of ERG16, CDR and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob. Agents Chemother., 41, 1482-1487.
20. Prasad, R., De Wergifosse, P., Goffeau, A. and Balzi, E. (1995): Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr. Genet., 27, 320-329.
21. Sanglard, D., Ischer, F., Monod, M. and Bille, J. (1997): Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology, 143, 405-416.
22. Fling, M. E., Kopf, J., Tamarkin, A., Gorman, J. A., Smith, H. A. and Koltin, Y. (1991): Analysis of a Candida albicans gene that encodes a novel mechanism for resistance to benomyl and methotrexate. Mol. Gen. Genet., 227, 318-329.
23. Calabrese, D., Bille, J. and Sanglard, D. (2000): A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology, 146, 2743-2754.
24. Sanglard, D., Ischer, F., Calabrese, D., Majcherczyk, P. A. and Bille, J. (1999): The ABC 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.
25. Miyazaki, H., Miyazaki, Y., Geber, A., Parkinson, T., Hitchcock, C., Falconer, D. J., Ward, D. J., Marsden, K. and Bennett, J. E. (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.
26. Moran, G. P., Sanglard, D., Donnelly, S. M., Shanley, D. B., Sullivan, D. J. and Coleman, D. C. (1998): Identification and expression of multidrug transporters responsible for fluconazole resistance in Candida dubliniensis. Antimicrob. Agents Chemother., 42, 1819-1830.
27. Katiyar, S. K. and Edlind, T. D. (2001): Identification and expression of multidrug resistance-related ABC transporter genes in Candida krusei. Med. Mycol., 39, 109-116.
28. Thornewell, S. J., Peery, R. B. and Skatrud, P. L. (1997): Cloning and characterization of CneMDR1: a Cryptococcus neoformans gene encoding a protein related to multidrug resistance proteins. Gene, 201, 21-29.
29. Posteraro, B., Sanguinetti, M., Sanglard, D., La Sorda, M., Boccia, S., Romano, L., Morace, G. and Fadda, G. (2003): Identification and characterization of a Cryptococcus neoformans ATP binding cassette (ABC) transporter-encoding gene, CnAFR1, involved in the resistance to fluconazole. Mol. Microbiol., 47, 357-371.
30. Tobin, M. B., Peery, R. B. and Skatrud, P. L. (1997): Genes encoding multiple drug resistance-like proteins in Aspergillus fumigatus and Aspergillus flavus. Gene, 200, 11-23.
31. Nascimento, A. M., Goldman, G. H., Park, S., Marras, S. A. E., Delmas, G., Oza, U., Lolans, K., Dudley, M. N., Mann, P. A. and Perlin, D. S. (2003): Multiple resistance mechanisms among Aspergillus fumigatus mutants with high-level resistance to itraconazole. Antimicrob. Agents Chemother., 47, 1719-1726.
32. Del Sorbo, G., Andrade, A. C., Van Nistelrooy, J. G. M., Van Kan, J. A. L., Balzi, E. and De Waard, M. A. (1997): Multidrug resistance in Aspergillus nidulans involves novel ATP-binding cassette transporters. Mol. Gen. Genet., 245, 417-426.
33. Angermayr, K., Parson, W., Stoffler, G. and Haas, H. (1999): Expression of atrC - encoding a novel member of the ATP binding cassette transporter family in Aspergillus nidulans - is sensitive to cycloheximide. Biochem. Biophys. Acta, 1453, 304-310.
34. Andrade, A. C., Van Nistelrooy, J. G. M., Peery, R. B., Skatrud, P. I. and De Waard, M. A. (2000): The role of ABC transporters from Aspergillus nidulans in protection against cytotoxic agents and in antibiotic production. Mol. Gen. Genet., 263, 966-977.
35. Krcmery, V. and Barnes, A. J. (2002): Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance. J. Hosp. Infect., 50, 243-260.
36. Niimi, M., Nagai, Y., Niimi, K., Wada, S., Cannon R. D., Uehara, Y. and Monk, B. C. (2002): Identification of two proteins induced by exposure of the pathogenic fungus Candida glabrata to fluconazole. J. Chromatogr. B, 782, 245-252.
37. Vermitsky, J. P. and Edlind, T. D. (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.
38. Decottignies, A., Grant, A. M., Nichols, J. W., de Wet, H., McIntosh, D. B. and Goffeau, A. (1998): ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem., 273, 12612-12622.
39. Nakamura, K., Niimi, M., Niimi, K., Holmes, A. R., Yates, J. E., Decottignies, A., Monk, B. C., Goffeau, A. and Cannon, R. D. (2001): Functional expression of Candida albicans drug efflux pump Cdr1p in a Saccharomyces cerevisiae strain deficient in membrane transporters. Antimicrob. Agents Chemother., 45, 3366-3374.
40. Wada, S., Niimi, M., Niimi, K., Monk, B. C., Holmes, A. R., Cannon, R. D. and Uehara, Y. (2002): Candida glabrata ATP-binding cassette transporters Cdr1p and Pdh1p expressed in a Saccharomyces cerevisiae strain deficient in membrane transporters show phosphorylation-dependent pumping properties. J. Biol. Chem., 277, 46809-46821.
41. Shukla, S., Saini, P., Smriti Jha, S., Ambudkar, S. V. and Prasad, R. (2003): Functional characterization of Candida albicans ABC Transporter Cdr1p. Eukaryotic Cell, 2, 1361-1375.
42. Kohli, A., Gupta, V., Krishnamurthy, S., Hasnain, S. E. and Prasad, R. (2001): Specificity of drug transport mediated by CaMDR1 a major facilitator of Candida albicans. J. Biosci., 26, 333-339.
43. Kolaczkowski, M., van der Rest, M., Cybularz-Kolaczkowska, A., Soumillion, J.-P., Konings, W. N. and Goffeau, A. (1996): Anticancer drugs, ionophoric peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p. J. Biol. Chem., 271, 31543-31548.
44. Wolfger, H., Mamnun, Y. M. and Kuchler, K. (2001): Fungal ABC proteins: pleiotropic drug resistance, stress response and cellular detoxification. Res. Microbiol., 152, 375-389.
45. Sa-Correia, I. and Tenreiro, S. (2002): The multidrug resistance transporters of the major facilitator superfamily, 6 years after disclosure of Saccharomyces cerevisiae genome sequence. J. Biotechnol., 98, 215-226.
46. Szczypka, M. S., Wemmie, J. A., Moye-Rowley, W. S. and Thiele, D. J. (1994): A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem., 269, 22853-22857.
47. Chen, X. J., Bauer, B. E., Kuchler, K. and Clark-Walker, G. D. (2000): Positive and negative control of multidrug resistance by the Sit4 protein phosphatase in Kluyveromyces lactis. J. Biol. Chem., 275, 14865-14872.
48. Decottignies, A., Owsianik, G. and Ghislain, M. (1999): Casein kinase I-dependent phosphorylation and stability of the yeast multidrug transporter Pdr5p. J. Biol. Chem., 274, 37139-37146.
49. Wada, S., Tanabe, K., Yamazaki, A., Niimi, M., Uerhara, Y., Niimi, K., Lamping, E., Cannon, R. D. and Monk, B. C. (2005): Phosphorylation of Candida glabrata ATP-binding cassette transporter Cdr1p regulates drug efflux activity and ATPase stability. J. Biol. Chem., 280, 94-103.
50. Denning, D. W. (2003): Echinocandin antifungal drugs. Lancet, 362, 1142-1151.
51. Blankenship, J. R., Steinbach, W. J., Perfect, J. R. and Heitman, J. (2003): Teaching old drugs new tricks: reincarnating immunosuppressants as antifungal drugs. Curr. Opin. Investig. Drugs, 4, 192-199.
52. Maesaki, S., Marichal, P., Hossain, M. A., Sanglard, D., Vanden Bossche, H. and Kohno, S. (1998): Synergic effects of tacrolimus and azole antifungal agents against azole-resistant Candida albicans strains. J. Antimicrob. Chemother., 42, 747-753.
53. Lee, M. D., Galazzo, J. L., Staley, A. L., Lee, J. C., Warren, M. S., Fuernkranz, H., Chamberland, S., Lomovskaya, O. and Miller, G. H. (2001): Microbial fermentation-derived inhibitors of efflux-pump-mediated drug resistance. Farmaco., 56, 81-85.
54. Niimi, K., Harding, D. R. K., Parshot, R., King, A., Lun, D. J., Decottignies, A., Niimi, M., Lin, S., Cannon, R. D., Goffeau, A. and Monk, B. C. (2004): Chemosensitization of fluconazole resistance in S. cerevisiae and pathogenic fungi by a D-octapeptide derivative. Antimicrob. Agents Chemother., 48, 1256-1271.