Detection of inhibitors of Candida albicans Cdr transporters using a diS-C3(3) fluorescence

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Szczepaniak, Joanna ^a   Lukaszewicz, Marcin ^a   Krasowska, Anna ^a  

^a UNIVERSITY OF WROC AW   (Poland)

Author keywords

ABC transporters; Beauvericin; Candida albicans; DiS C3(3); Enniatin A; Inhibitors

Indexed keywords

ABC TRANSPORTER; BEAUVERICIN; CDR1 TRANSPORTER INHIBITOR; CDR2 TRANSPORTER INHIBITOR; ENNIATIN; FLUORESCENT DYE; MICONAZOLE; MULTIDRUG RESISTANCE PROTEIN; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA ALBICANS; CONFOCAL MICROSCOPY; DISK DIFFUSION; DRUG ACTIVITY; DRUG INHIBITION; FLUORESCENCE; FUNGAL STRAIN; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; POTENTIOMETRY;

CANDIDA ALBICANS;

EID: 84927137089     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00176     Document Type: Article

References (32)

1. Calahorra, M., Sánchez, N., and Peña, A. (2012). Characterization of glycolytic metabolism and ion transport of Candida albicans. Yeast 29, 357-370. doi: 10.1002/yea.2915.
2. Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Baret, P. V., Keniya, M. V., et al. (2009). Efflux-mediated antifungal drug resistance. Clin. Microbiol. Rev. 22, 291-321, Table of Contents. doi: 10.1128/CMR.00051-08.
3. Clark, F., Parkinson, T., Hitchcock, C., and Gow, N. (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.
4. Coste, A. T., Crittin, J., Bauser, C., Rohde, B., and Sanglard, D. (2009). Functional analysis of cis-and trans-acting elements of the Candida albicans CDR2 promoter with a novel promoter reporter system. Eukaryot. Cell 8, 1250-1267. doi: 10.1128/EC.00069-09.
5. Coste, A. T., Karababa, M., Ischer, F., Bille, J., and Sanglard, D. (2004). TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2. Eukaryot. Cell 3, 1639-1652. doi: 10.1128/EC.3.6.1639-1652.2004.
6. Fonzi, W., and Irwin, M. (1993). Isogenic strain construction and gene mapping in Candida albicans. Genetics 134, 717-728.
7. Fukuda, T., Arai, M., Yamaguchi, Y., Masuma, R., Tomoda, H., and Omura, S. (2004). New beauvericins, potentiators of antifungal miconazole activity, Produced by Beauveria sp. FKI-1366: I. Taxonomy, fermentation, isolation and biological properties. J. Antibiot. (Tokyo) 57, 110-116. doi: 10.7164/antibiotics.57.110.
8. Gásková, D., Brodská, B., Herman, P., Vecer, J., Malínskỳ, J., Sigler, K., et al. (1998). Fluorescent probing of membrane potential in walled cells: diS-C3(3) assay in Saccharomyces cerevisiae. Yeast 14, 1189-1197. doi: 10.1002/(SICI)1097-0061(19980930)14:13<1189::AID-YEA320>3.0.CO;2-K.
9. Gášková, D., Brodská, B., Holoubek, A., and Sigler, K. (1999). Factors and processes involved in membrane potential build-up in yeast: diS-C3(3) assay. Int. J. Biochem. Cell Biol. 31, 575-584. doi: 10.1016/S1357-2725(99)00002-3.
10. Hendrych, T., Kodedová, M., Sigler, K., and Gásková, D. (2009). Characterization of the kinetics and mechanisms of inhibition of drugs interacting with the S. cerevisiae multidrug resistance pumps Pdr5p and Snq2p. Biochim. Biophys. Acta 1788, 717-723. doi: 10.1016/j.bbamem.2008.12.001.
11. Hiraga, K., Yamamoto, S., Fukuda, H., Hamanaka, N., and Oda, K. (2005). Enniatin has a new function as an inhibitor of Pdr5p, one of the ABC transporters in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 328, 1119-1125. doi: 10.1016/j.bbrc.2005.01.075.
12. Holmes, A. R., Lin, Y.-H., Niimi, K., Lamping, E., Keniya, M., Niimi, M., et al. (2008). ABC transporter Cdr1p contributes more than Cdr2p does to fluconazole efflux in fluconazole-resistant Candida albicans clinical isolates. Antimicrob. Agents Chemother. 52, 3851-3862. doi: 10.1128/AAC.00463-08.
13. Ivnitski-Steele, I., Holmes, A. R., Lamping, E., Monk, B. C., Richard, D., and Sklar, L. A. (2010). Identification of Nile Red as a fluorescent substrate of the Candida albicans ABC transporters Cdr1p and Cdr2p and the MFS transporter Mdr1p. Anal. Biochem. 394, 87-91. doi: 10.1016/j.ab.2009.07.001.
14. Kolaczkowska, A., and Goffeau, A. (1999). Regulation of pleiotropic drug resistance in yeast. Drug Resist. Updat. 2, 403-414. doi: 10.1054/drup.1999.0113.
15. Krasowska, A., Lukaszewicz, M., Bartosiewicz, D., and Sigler, K. (2010). Cell ATP level of Saccharomyces cerevisiae sensitively responds to culture growth and drug-inflicted variations in membrane integrity and PDR pump activity. Biochem. Biophys. Res. Commun. 395, 51-55. doi: 10.1016/j.bbrc.2010.03.133.
16. Morschhäuser, J. (2010). Regulation of multidrug resistance in pathogenic fungi. Fungal Genet. Biol. 47, 94-106. doi: 10.1016/j.fgb.2009.08.002.
17. Mukherjee, P., and Chandra, J. (2003). Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect. Immun. 71, 4333-4340. doi: 10.1128/IAI.71.8.4333-4340.2003.
18. Niimi, K., Harding, D. R. K., Parshot, R., King, A., Lun, D. J., Decottignies, A., et al. (2004). Chemosensitization of fluconazole resistance in Saccharomyces cerevisiae and pathogenic fungi by a D-octapeptide derivative. Antimicrob. Agents Chemother. 48, 1256-1271. doi: 10.1128/AAC.48.4.1256-1271.2004.
19. Puri, N., Prakash, O., Manoharlal, R., Sharma, M., Ghosh, I., and Prasad, R. (2010). Analysis of physico-chemical properties of substrates of ABC and MFS multidrug transporters of pathogenic Candida albicans. Eur. J. Med. Chem. 45, 4813-4826. doi: 10.1016/j.ejmech.2010.07.050.
20. Rodaki, A., Bohovych, I. M., Enjalbert, B., Young, T., Odds, F. C., Gow, N. A. R., et al. (2009). Glucose promotes stress resistance in the fungal pathogen Candida albicans. Mol. Biol. Cell 20, 4845-4855. doi: 10.1091/mbc.E09-01-0002.
21. Rogers, B., Decottignies, A., Kolaczkowski, M., Carvajal, E., Balzi, E., and Goffeau, A. (2001). The pleitropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 3, 207-214.
22. Sanglard, D., Coste, A., and Ferrari, S. (2009). Antifungal drug resistance mechanisms in fungal pathogens from the perspective of transcriptional gene regulation. FEMS Yeast Res. 9, 1029-1050. doi: 10.1111/j.1567-1364.2009.00578.x.
23. Sanglard, D., and Ischer, F. (1996). Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob. Agents Chemother. 40, 2300-2305.
24. 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(Pt 2), 405-416. doi: 10.1099/00221287-143-2-405.
25. Sanglard, D., Kuchler, K., Ischer, F., Pagani, J. L., Monod, M., and Bille, J. (1995). Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob. Agents Chemother. 39, 2378-2386. doi: 10.1128/AAC.39.11.2378.
26. Sharma, M., Manoharlal, R., Shukla, S., Puri, N., Prasad, T., Ambudkar, S. V., et al. (2009). Curcumin modulates efflux mediated by yeast ABC multidrug transporters and is synergistic with antifungals. Antimicrob. Agents Chemother. 53, 3256-3265. doi: 10.1128/AAC.01497-08.
27. Sharma, M., and Prasad, R. (2011). The quorum-sensing molecule farnesol is a modulator of drug efflux mediated by ABC multidrug transporters and synergizes with drugs in Candida albicans. Antimicrob. Agents Chemother. 55, 4834-4843. doi: 10.1128/AAC.00344-11.
28. Spampinato, C., and Leonardi, D. (2013). Candida infections, causes, targets, and resistance mechanisms: traditional and alternative antifungal agents. Biomed Res. Int. 2013, 204237. doi: 10.1155/2013/204237.
29. Tanabe, K., Lamping, E., Nagi, M., Okawada, A., Holmes, A. R., Miyazaki, Y., et al. (2011). Chimeras of Candida albicans Cdr1p and Cdr2p reveal features of pleiotropic drug resistance transporter structure and function. Mol. Microbiol. 82, 416-433. doi: 10.1111/j.1365-2958.2011.07820.x.
30. Tonshin, A. A., Teplova, V. V., Andersson, M. A., and Salkinoja-Salonen, M. S. (2010). The Fusarium mycotoxins enniatins and beauvericin cause mitochondrial dysfunction by affecting the mitochondrial volume regulation, oxidative phosphorylation and ion homeostasis. Toxicology 276, 49-57. doi: 10.1016/j.tox.2010.07.001.
31. Zhang, H., Gao, A., Li, F., Zhang, G., Ho, H. I., and Liao, W. (2009). Mechanism of action of tetrandrine, a natural inhibitor of Candida albicans drug efflux pumps. Yakugaku Zasshi 129, 623-630. doi: 10.1248/yakushi.129.623.
32. Zhang, L., Yan, K., Zhang, Y., Huang, R., Bian, J., Zheng, C., et al. (2007). High-throughput synergy screening identifies microbial metabolites as combination agents for the treatment of fungal infections. Proc. Natl. Acad. Sci. U.S.A. 104, 4606-4611. doi: 10.1073/pnas.0609370104.