Ibuprofen reverts antifungal resistance on Candida albicans showing overexpression of CDR genes

FEMS Yeast Research

Volumn 9, Issue 4, 2009, Pages 618-625

  Ricardo, Elisabete ^a,b   Costa De Oliveira, Sofia ^a,b   Silva Dias, Ana ^a   Guerra, José ^a   Rodrigues, Acácio Gonçalves ^a,b   Pina Vaz, Cidália ^a,b,c  

^a University of Porto   (Portugal)

^b Unit of Cardiovascular Diseases   (Portugal)

^c HOSPITAL DE SÃO JOÃO   (Portugal)

Author keywords

Antifungal resistance; Azoles resistance genes; Candida albicans; Ibuprofen; Real time PCR

Indexed keywords

FLUCONAZOLE; IBUPROFEN; ITRACONAZOLE; MEMBRANE PROTEIN; MEMBRANE PROTEIN CDR1; MEMBRANE PROTEIN CDR2; MULTIDRUG RESISTANCE PROTEIN 1; TACROLIMUS; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR ERG 11; UNCLASSIFIED DRUG; VORICONAZOLE;

ANTIFUNGAL RESISTANCE; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; DRUG POTENTIATION; DRUG SENSITIVITY; GENE EXPRESSION; GENE OVEREXPRESSION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE;

ANTIFUNGAL AGENTS; AZOLES; CANDIDA ALBICANS; CANDIDIASIS; DRUG RESISTANCE, FUNGAL; DRUG SYNERGISM; ENZYME INHIBITORS; FLUCONAZOLE; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; HUMANS; IBUPROFEN; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; TACROLIMUS;

CANDIDA; CANDIDA ALBICANS;

EID: 65549122922     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2009.00504.x     Document Type: Article

References (33)

1. Arceci RJ, Stieglitz K Bierer BE (1992) Immunosuppressants FK506 and rapamycin function as reversal agents of the multidrug resistance phenotype. Blood 80 : 1528 1536.
2. Carrillo-Munoz AJ, Giusano G, Ezkurra PA Quindós G (2006) Antifungal agents: mode of action in yeast cells. Rev Esp Quimioterap 19 : 130 139. (Pubitemid 44186630)
3. Clinical Laboratory Standards Institute (2002) Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Approved Standard. CLSI Document M27-A2. National Committee for Clinical Laboratory Standards, Wayne, PA.
4. Coste A, Turner V, Ischer F, Morschhäuser J, Forche A, Selmecki A, Berman J, Bille J Sanglard D (2006) A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at chromosome 5 to mediate antifungal resistance in Candida albicans. Genetics 172 : 2139 2156.
5. Coste A, Selmecki A, Forche A, Diogo D, Bougnoux M-E, d'Enfert C, Berman J Sanglard D (2007) Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 6 : 1889 1904. (Pubitemid 47585577)
6. Coste AT, Karababa M, Ischer F, Bille J 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. (Pubitemid 40025121)
7. Cowen LE, Sanglard D, Calabrese D, Sirjusingh C, Anderson JB Kohn LM (2000) Evolution of drug resistance in experimental populations of Candida albicans. J Bacteriol 182 : 1515 1522. (Pubitemid 30121114)
8. De Micheli M, Bille J, Schueller C Sanglard D (2002) 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 : 1197 1214. (Pubitemid 34304537)
9. Fling ME, Kopf J, Tamarkin A, Gorman JA, Smith HA 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.
10. Franz R, Kelly SL, Lamb DC, Kelly DE, Ruhnke M Morschhäuser J (1998) Multiple molecular mechanisms contribute to a stepwise development of fluconazole resistance in clinical Candida albicans strains. Antimicrob Agents Ch 42 : 3065 3072. (Pubitemid 28553719)
11. Harry JB, Oliver BG, Song JL, Silver PM, Little JT, Choiniere J White TC (2005) Drug-induced regulation of the MDR1 promoter in Candida albicans. Antimicrob Agents Ch 49 : 2785 2792. (Pubitemid 40917592)
12. Karababa M, Coste AT, Rognon B, Bille J Sanglard D (2004) Comparison of gene expression profiles of Candida albicans azole-resistant clinical isolates and laboratory strains exposed to drugs inducing multidrug transporters. Antimicrob Agents Ch 48 : 3064 3079. (Pubitemid 38989176)
13. Köhrer K Domdey H (1991) Preparation of high molecular weight RNA. Method Enzymol 194 : 398 405.
14. Lai MH Kirsch DR (1989) Nucleotide sequence of cytochrome P450 L1A1 (lanosterol 14 alpha-demethylase) from Candida albicans. Nucleic Acids Res 17 : 804. (Pubitemid 19042313)
15. Losberger C Ernst JF (1989) Sequence of the Candida albicans gene encoding actin. Nucleic Acids Res 17 : 9488. (Pubitemid 20003223)
16. Lyons CN White TC (2000) Transcriptional analyses of antifungal drug resistance in Candida albicans. Antimicrob Agents Ch 44 : 2296 2303. (Pubitemid 30650871)
17. Maesaki S, Marichal P, Hossain MA, Sanglard D, Vanden Bossche H Kohno S (1998) Synergic effects of tactolimus and azole antifungal agents against azole-resistant Candida albican strains. J Antimicrob Chemoth 42 : 747 753. (Pubitemid 29008076)
18. Marchetti O, Moreillon P, Glauser MP, Bille J Sanglard D (2000) Potent synergism of the combination of fluconazole and cyclosporine in Candida albicans. Antimicrob Agents Ch 44 : 2373 2381. (Pubitemid 30650882)
19. Marichal P, Koymans L, Willemsens S, Bellens D, Verhasselt P, Luyten W, Borgers M, Ramaekers FC, Odds FC Bossche HV (1999) Contribution of mutations in the cytochrome P450 14a-demethylase (Erg11p, Cyp51p) to azole resistance in Candida albicans. Microbiology 145 : 2701 2713. (Pubitemid 29485885)
20. Morschhauser J, Barker KS, Liu TT, Blaß-Warmuth J, Homayouni R Rogers PD (2007) The transcription factor Mrr1p controls expression of the MDR1 efflux pump and mediates multidrug resistance in Candida albicans. PLoS Pathog 3 : e164. (Pubitemid 350291598)
21. Onyewu C, Blankenship JR, Del Poeta M Heitman J (2003) Ergosterol biosynthesis inhibitors become fungicidal when combined with calcineurin inhibitors against Candida albicans, Candida glabrata, and Candida krusei. Antimicrob Agents Ch 47 : 956 964. (Pubitemid 36254221)
22. Pasrija R, Banerjee D Prasad R (2007) Structure and function analysis of CaMdr1p, a major facilitator superfamily antifungal efflux transporter protein of Candida albicans: identification of amino acid residues critical for drug/H+ transport. Eukaryot Cell 6 : 443 453. (Pubitemid 46492332)
23. Pina-Vaz C, Rodrigues AG, Costa-de-Oliveira S, Ricardo E Mrdh 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 Chemoth 56 : 678 685. (Pubitemid 41487768)
24. Prasad R, de Wergifosse P, Goffeau A 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.
25. Redding S, Smith J, Farinacci G, Rinaldi M, Fothergill A, Rhine-Chalberg J Pfaller M (1994) Resistance of Candida albicans to fluconazole during treatment of oropharyngeal candidiasis in a patient with AIDS: documentation by in vitro susceptibility testing and DNA subtype analysis. Clin Infect Dis 18 : 240 242. (Pubitemid 24055265)
26. Sanglard D Odds FC (2002) Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis 2 : 73 85. (Pubitemid 36114141)
27. 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. (Pubitemid 27092176)
28. Schuetzer-Muehlbauer M, Willinger B, Egner R, Ecker G Kuchler K (2003) Reversal of antifungal resistance mediated by ABC efflux pumps from Candida albicans functionally expressed in yeast. Int J Antimicrob Ag 22 : 291 300. (Pubitemid 37103216)
29. Silver PM, Oliver BG White TC (2004) Role of Candida albicans transcription factor Upc2p in drug resistance and sterol metabolism. Eukaryot Cell 3 : 1391 1397. (Pubitemid 40025098)
30. Sun S, Li Y, Guo Q, Shi C, Yu J Ma L (2008) In vitro interactions between Tacrolimus and Azoles against Candida albicans determined by different methods. Antimicrob Agents Ch 52 : 409 417.
31. White TC (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 Ch 41 : 1482 1487. (Pubitemid 27289672)
32. White TC, Marr KA Bowden RA (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11 : 382 402. (Pubitemid 28197359)
33. White TC, Holleman S, Dy F, Mirels LF Stevens DA (2002) Resistance mechanisms in clinical isolates of Candida albicans. Antimicrob Agents Ch 46 : 1704 1713. (Pubitemid 34535186)