Reversal of efflux mediated antifungal resistance underlies synergistic activity of two monoterpenes with fluconazole

European Journal of Pharmaceutical Sciences

Volumn 48, Issue 1-2, 2013, Pages 80-86

  Ahmad, Aijaz ^a   Khan, Amber ^a   Manzoor, Nikhat ^a  

^a JAMIA MILLIA ISLAMIA CENTRAL UNIVERSITY   (India)

Author keywords

Candida; Carvacrol; Drug resistance; Fluconazole; Synergy; Thymol

Indexed keywords

CARVACROL; CDR1 PROTEIN; CDR2 PROTEIN; ERG11 PROTEIN; FLUCONAZOLE; MULTIDRUG RESISTANCE PROTEIN 1; TERPENE; THYMOL; UNCLASSIFIED DRUG;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BROTH DILUTION; CANDIDA ALBICANS; CANDIDA GLABRATA; CANDIDA KRUSEI; CANDIDA TROPICALIS; FUNGUS ISOLATION; GENE OVEREXPRESSION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL;

ANTIFUNGAL AGENTS; BENZIMIDAZOLES; CANDIDA; DRUG SYNERGISM; FLUCONAZOLE; FLUORESCENT DYES; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MONOTERPENES; P-GLYCOPROTEIN; THYMOL;

EID: 84869882182     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2012.09.016     Document Type: Article

References (35)

1. A. Ahmad, A. Khan, L.A. Khan, and N. Manzoor In vitro synergy of eugenol and methyleugenol with fluconazole against clinical Candida isolates J. Med. Microbiol. 59 2010 1178 1184
2. A. Ahmad, A. Khan, F. Akhtar, S. Yousuf, I. Xess, L.A. Khan, and N. Manzoor Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida Eur. J. Clin. Microbiol. Infect. Dis. 30 2011 41 50
3. X. Bi, N. Guo, J. Jin, J. Liu, H. Feng, J. Shi, H. Xiang, X. Wu, J. Dong, H. Hu, S. Yan, C. Yu, X. Wang, X. Deng, and L. Yu The global gene expression profile of the model fungus Saccharomyces cerevisiae induced by thymol J. Appl. Microbiol. 108 2 2010 712 722
4. M.C. Berenbaum What is synergy? Pharmacol. Rev. 41 1989 93 141
5. J.M. Blair, R.M. La Ragione, M.J. Woodward, and L.J. Piddock The membrane fusion protein AcrA has a distinct role in antibiotic resistance and virulence of Salmonella enterica serovar Typhimurium J. Antimicrob. Chemother. 64 2009 965 972
6. A. Chakrabarti, S.S. Chatterjee, K.L. Rao, M.M. Zameer, M.R. Shivaprakash, S. Singhi, R. Singh, and S.C. Varma Recent experience with fungaemia: change in species distribution and azole resistance Scand. J. Infect. Dis. 41 2009 275 284
7. Clinical and Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved Standard M27-A3.CLSI. third ed. PA, USA.
8. P. Eggimann, J. Garbino, and D. Pitte Epidemiology of Candida species infections in critically ill non-immunosuppressed patients Lancet. Infect. Dis. 3 2003 685 702
9. S.G. Filler, and D.C. Sheppard Fungal invasion of normally non-phagocytic host cells PLoS Pathog. 2 2006 e129
10. M.I. Garvey, M.M. Rahman, S. Gibbons, and L.J. Piddock Medicinal plant extracts with efflux inhibitory activity against Gram-negative bacteria Int. J. Antimicrob. Agents. 37 2011 145 151
11. M.A. Ghannoum, Y. Fu, A.S. Ibrahim, L.A. Mortara, M.C. Shafiq, J.E. Edwards, and R.S. Criddle Jr. In vitro determination of optimal antifungal combinations against Cryptococcus neoformans and Candida albicans Antimicrob. Agents. Chemother. 39 1995 2459 2465
12. J. Guinea, M. Sánchez-Somolinos, O. Cuevas, T. Peláez, and E. Bouza Fluconazole resistance mechanisms in Candida krusei: the contribution of efflux-pumps Med. Mycol. 44 6 2006 575 578
13. S. Hemaiswarya, A.K. Kruthiventi, and M. Doble Synergism between natural products and antibiotics against infectious diseases Phytomedicine 15 2008 639 652
14. D. Hiller, D. Sanglard, and J. Morschhauser Overexpression of the MDR1 gene is sufficient to confer increased resistance to toxic compounds in Candida albicans Antimicrob. Agents. Chemother. 50 2006 1365 1371
15. C.A. Kauffman Role of azoles in antifungal therapy Clin. Infect. Dis. 22 Suppl 2 1996 S148 S153
16. A. Khan, A. Ahmad, I. Xess, L.A. Khan, and N. Manzoor Anticandidal effect of Ocimum sanctum essential oil and its synergy with fluconazole and ketoconazole Phytomedicine 17 2010 921 925
17. A. Khan, A. Ahmad, L.A. Khan, and N. Manzoor Antifungal activities of Ocimum sanctum Essential Oil and its Lead Molecules Nat. Prod. Commun. 5 2010 345 349
18. A.P. Koehler, K.C. Chu, E.T. Houang, and A.F. Cheng Simple, reliable and cost effective yeast identification scheme for clinical laboratory J. Clin. Microbiol. 37 1999 422 426
19. O. Lortholary, and B. Dupont Antifungal prophylaxis during neutropenia and immunodeficiency Clin. Microbiol. Rev. 10 3 1997 477 504
20. S. Maesaki, P. Marichal, H. Vanden Bossche, D. Sanglard, and S. Kohno Rhodamine 6G efflux for the detection of CDR1-overexpressing azole-resistant Candida albicans strains J. Antimicrob. Chemother. 44 1999 27 31
21. P.K. Mukherjee, D.J. Sheehan, C.A. Hitchcock, and M.A. Ghannoum Combination treatment of invasive fungal infections Clin. Microbiol. Rev. 18 2005 163 194
22. A. Murzyn, A. Krasowska, P. Stefanowicz, D. Dziadkowiec, and M. Łukaszewicz Capric acid secreted by S. boulardii inhibits C. albicans filamentous growth, adhesion and biofilm formation PLoS One 5 2010 e12050
23. S. Perea, J.L. López-Ribot, W.R. Kirkpatrick, R.K. McAtee, R.A. Santillán, M. Martínez, D. Calabrese, D. Sanglard, and T.F. Patterson Prevalence of molecular mechanisms of resistance to azole antifungal agents in Candida albicans strains displaying high-level fluconazole resistance isolated from human immunodeficiency virus-infected patients Antimicrob. Agents. Chemother. 45 2001 2676 2684
24. E. Pinto, L. Vale-Silva, C. Cavaleiro, and L. Salgueiro Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species J. Med. Microbiol. 58 2009 1454 1462
25. R. Prasad, and K. Kapoor Multidrug resistance in yeast Candida Int. Rev. Cytol. 242 2005 215 248
26. A. Rao, Y. Zhang, S. Muend, and R. Rao Mechanism of antifungal activity of terpenoid phenols resembles calcium stress and inhibition of the TOR pathway Antimicrob. Agents. Chemother. 54 2010 5062 5069
27. D. Sanglard, F. Ischer, T. Parkinson, D. Falconer, and J. Bille Candida albicans mutations in the ergosterol biosynthetic pathway and resistance to several antifungal agents Antimicrob. Agents. Chemother. 47 2003 2404 2412
28. D. Sanglard, F. Ischer, M. Monod, and J. Bille 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
29. D. Sanglard, K. Kuchler, F. Ischer, J.L. Pagani, M. Monod, and J. Bille 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
30. S. Shapiro, and B. Guggenheim The action of thymol on oral bacteria Oral Microbiol. Immunol. 10 1995 241 246
31. M. Sharma, R. Manoharlal, S. Shukla, N. Puri, T. Prasad, S.V. Ambudkar, and R. Prasad Curcumin modulates efflux mediated by yeast ABC multidrug transporters and is synergistic with antifungals Antimicrob. Agents. Chemother. 53 2009 3256 3265
32. V.N. Tariq, E.M. Scott, and N.E. McCain Use of decimal assay for additivity to demonstrate synergy in pair combinations of econazole, nikkomycin Z, and ibuprofen against C. albicans in vitro Antimicrob. Agents. Chemother. 39 1995 2615 2619
33. P. Uppuluri, J. Nett, J. Heitman, and D. Andes Synergistic effect of calcineurin inhibitors and fluconazole against Candida albicans biofilms Antimicrob. Agents. Chemother. 52 2008 1127 1132
34. H.W. van Veen, and W.N. Konings Multidrug transporters from bacteria to man: similarities in structure and function Semin Cancer Biol. 8 3 1997 183 191
35. S. Wada, M. Niimi, K. Niimi, A.R. Holmes, B.C. Monk, R.D. Cannon, and Y. Uehara 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 2002 46809 46821