Synergistic effect of fluconazole and doxycycline against Candida albicans biofilms resulting from calcium fluctuation and downregulation of fluconazole-inducible efflux pump gene overexpression

Journal of Medical Microbiology

Volumn 63, Issue PART 7, 2014, Pages 956-961

  Gao, Yuan ^a,b   Li, Hui ^a   Liu, Shuyuan ^a   Zhang, Xiang ^c   Sun, Shujuan ^d  

^a SHANDONG UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^c JINAN CENTRAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^d THE FIRST AFFILIATED HOSPITAL OF SHANDONG FIRST MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CDR1 PROTEIN; CDR2 PROTEIN; DOXYCYCLINE; FLUCONAZOLE; FLUO 3; FLUO 3 AM; FLUORESCENT DYE; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIFUNGAL ACTIVITY; ARTICLE; BIOFILM; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CANDIDA ALBICANS; CELL CYCLE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG POTENTIATION; FLOW CYTOMETRY; FLUORESCENCE SPECTROSCOPY; FUNGAL CELL; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE OVEREXPRESSION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION;

ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; BIOFILMS; CALCIUM; CANDIDA ALBICANS; CARRIER PROTEINS; DOWN-REGULATION; DOXYCYCLINE; DRUG SYNERGISM; FLUCONAZOLE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL;

EID: 84903128821     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.072421-0     Document Type: Article

References (32)

1. Albertson, G. D., Niimi, M., Cannon, R. D. & Jenkinson, H. F. (1996). Multiple efflux mechanisms are involved in Candida albicans fluconazole resistance. Antimicrob Agents Chemother 40, 2835-2841.
2. Bader, T., Schröppel, K., Bentink, S., Agabian, N., Köhler, G. & Morschhäuser, J. (2006). Role of calcineurin in stress resistance, morphogenesis, and virulence of a Candida albicans wild-type strain. Infect Immun 74, 4366-4369.
3. Bink, A., Pellens, K., Cammue, B. P. A. & Thevissen, K. (2011). Antibiofilm strategies: how to eradicate Candida biofilms? The Open Mycology Journal 5, 29-38.
4. Cruz, M. C., Goldstein, A. L., Blankenship, J. R., Del Poeta, M., Davis, D., Cardenas, M. E., Perfect, J. R., McCusker, J. H. & Heitman, J. (2002). Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J 21, 546-559.
5. Fiori, A. & Van Dijck, P. (2012). Potent synergistic effect of doxycycline with fluconazole against Candida albicans is mediated by interference with iron homeostasis. Antimicrob Agents Chemother 56, 3785-3796.
6. Foland, T. B., Dentler, W. L., Suprenant, K. A., Gupta, M. L., Jr & Himes, R. H. (2005). Paclitaxel-induced microtubule stabilization causes mitotic block and apoptotic-like cell death in a paclitaxelsensitive strain of Saccharomyces cerevisiae. Yeast 22, 971-978.
7. Ford, J. M. & Hait, W. N. (1990). Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol Rev 42, 155-199.
8. Gao, Y., Zhang, C., Lu, C., Liu, P., Li, Y., Li, H. & Sun, S. (2013). Synergistic effect of doxycycline and fluconazole against Candida albicans biofilms and the impact of calcium channel blockers. FEMS Yeast Res 13, 453-462.
9. Gupta, S. S., Ton, V. K., Beaudry, V., Rulli, S., Cunningham, K. & Rao, R. (2003). Antifungal activity of amiodarone is mediated by disruption of calcium homeostasis. J Biol Chem 278, 28831-28839.
10. Hawser, S. P. & Douglas, L. J. (1995). Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother 39, 2128-2131.
11. Jacks, T. & Weinberg, R. A. (1996). Cell-cycle control and its watchman. Nature 381, 643-644.
12. Jung, H. J., Park, K., Lee, I. S., Kim, H. S., Yeo, S. H., Woo, E. R. & Lee, D. G. (2007). S-phase accumulation of Candida albicans by anticandidal effect of amentoflavone isolated from Selaginella tamariscina. Biol Pharm Bull 30, 1969-1971.
13. Kauh, E. A. & Bjornsti, M. A. (1995). SCT1 mutants suppress the camptothecin sensitivity of yeast cells expressing wild-type DNA topoisomerase I. Proc Natl Acad Sci U S A 92, 6299-6303.
14. 2+ signaling pathway and caspase activity. PLoS ONE 6, e15808.
15. McConkey, D. J. & Orrenius, S. (1997). The role of calcium in the regulation of apoptosis. Biochem Biophys Res Commun 239, 357-366.
16. Miceli, M. H., Bernardo, S.M. & Lee, S. A. (2009). In vitro analyses of the combination of high-dose doxycycline and antifungal agents against Candida albicans biofilms. Int J Antimicrob Agents 34, 326-332.
17. Oliver, B. G., Silver, P. M., Marie, C., Hoot, S. J., Leyde, S. E. & White, T. C. (2008). Tetracycline alters drug susceptibility in Candida albicans and other pathogenic fungi. Microbiology 154, 960-970.
18. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.
19. Phillips, A. J., Sudbery, I. & Ramsdale, M. (2003). Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc Natl Acad Sci U S A 100, 14327-14332.
20. Pina-Vaz, C., Rodrigues, A. G., Costa-de-Oliveira, S., Ricardo, E. & Mårdh, P. A. (2005). Potent synergic effect between ibuprofen and azoles on Candida resulting from blockade of efflux pumps as determined by FUN-1 staining and flow cytometry. J Antimicrob Chemother 56, 678-685.
21. Pozniakovsky, A. I., Knorre, D. A., Markova, O. V., Hyman, A. A., Skulachev, V. P. & Severin, F. F. (2005). Role of mitochondria in the pheromone-and amiodarone-induced programmed death of yeast. J Cell Biol 168, 257-269.
22. Ramage, G., Bachmann, S., Patterson, T. F., Wickes, B. L. & López-Ribot, J. L. (2002). Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J Antimicrob Chemother 49, 973-980.
23. Reedy, J. L., Filler, S. G. & Heitman, J. (2010). Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence. Fungal Genet Biol 47, 107-116.
24. Sabourin, M., Nitiss, J. L., Nitiss, K. C., Tatebayashi, K., Ikeda, H. & Osheroff, N. (2003). Yeast recombination pathways triggered by topoisomerase II-mediated DNA breaks. Nucleic Acids Res 31, 4373-4384.
25. Sanglard, D., Ischer, F., Monod, M. & 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.
26. Schmitt, M. E., Brown, T. A. & Trumpower, B. L. (1990). A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18, 3091-3092.
27. Shi, W., Chen, Z., Chen, X., Cao, L., Liu, P. & Sun, S. (2010). The combination of minocycline and fluconazole causes synergistic growth inhibition against Candida albicans: an in vitro interaction of antifungal and antibacterial agents. FEMS Yeast Res 10, 885-893.
28. Wang, H., Liang, Y., Zhang, B., Zheng, W., Xing, L. & Li, M. (2011). Alkaline stress triggers an immediate calcium fluctuation in Candida albicans mediated by Rim101p and Crz1p transcription factors. FEMS Yeast Res 11, 430-439.
29. Watamoto, T., Samaranayake, L. P., Egusa, H., Yatani, H. & Seneviratne, C. J. (2011). Transcriptional regulation of drugresistance genes in Candida albicans biofilms in response to antifungals. J Med Microbiol 60, 1241-1247.
30. Wu, X. Z., Chang, W. Q., Cheng, A. X., Sun, L. M. & Lou, H. X. (2010). Plagiochin E, an antifungal active macrocyclic bis(bibenzyl), induced apoptosis in Candida albicans through a metacaspase-dependent apoptotic pathway. Biochim Biophys Acta 1800, 439-447.
31. Zhang, Y. Q. & Rao, R. (2007). Global disruption of cell cycle progression and nutrient response by the antifungal agent amiodarone. J Biol Chem 282, 37844-37853.
32. Zore, G. B., Thakre, A. D., Jadhav, S. & Karuppayil, S. M. (2011). Terpenoids inhibit Candida albicans growth by affecting membrane integrity and arrest of cell cycle. Phytomedicine 18, 1181-1190.