Molecular mechanisms of fluconazole resistance in Candida parapsilosis isolates from a U.S. surveillance system

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 2, 2015, Pages 1030-1037

  Grossman, Nina T ^a   Pham, Cau D ^a   Cleveland, Angela A ^a   Lockhart, Shawn R ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FLUCONAZOLE; RNA; STEROL 14ALPHA DEMETHYLASE; TRANSCRIPTION FACTOR; VORICONAZOLE; ANTIFUNGAL AGENT;

AMINO ACID SUBSTITUTION; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA PARAPSILOSIS; CANDIDEMIA; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SURVEILLANCE; DOSE RESPONSE; ERG11 GENE; FUNGAL GENE; FUNGAL STRAIN; GENE OVEREXPRESSION; GENE SEQUENCE; HOSPITAL; HUMAN; MDR1 GENE; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR BIOLOGY; MRR1 GENE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; CANDIDA; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MICROBIAL SENSITIVITY TEST;

ANTIFUNGAL AGENTS; CANDIDA; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; GENE EXPRESSION REGULATION, FUNGAL; MICROBIAL SENSITIVITY TESTS;

EID: 84921711253     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.04613-14     Document Type: Article

References (29)

1. Romeo O, Delfino D, Cascio A, Lo Passo C, Amorini M, Romeo D, Pernice I. 2013. Microsatellite-based genotyping of Candida parapsilosis sensu stricto isolates reveals dominance and persistence of a particular epidemiological clone among neonatal intensive care unit patients. Infect Genet Evol 13:105-108. http://dx.doi.org/10.1016/j.meegid.2012.09.006.
2. Diab-Elschahawi M, Forstner C, Hagen F, Meis JF, Lassnig AM, Presterl E, Klaassen CH. 2012. Microsatellite genotyping clarified conspicuous accumulation of Candida parapsilosis at a cardiothoracic surgery intensive care unit. J Clin Microbiol 50:3422-3426. http://dx.doi.org/10.1128/JCM .01179-12.
3. Pfaller MA, Diekema DJ. 2007. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133-163. http: //dx.doi.org/10.1128/CMR.00029-06.
4. Lockhart SR, Iqbal N, Cleveland AA, Farley MM, Harrison LH, Bolden CB, Baughman W, Stein B, Hollick R, Park BJ, Chiller T. 2012. Species identification and antifungal susceptibility testing of Candida bloodstream isolates from population-based surveillance studies in two U.S. cities from 2008 to 2011. J Clin Microbiol 50:3435-3442. http://dx.doi.org /10.1128/JCM.01283-12.
5. Pfaller MA, Jones RN, Castanheira M. 2014. Regional data analysis of Candida non-albicans strains collected in United States medical sites over a 6-year period, 2006-2011. Mycoses 57:602-611. http://dx.doi.org/10 .1111/myc.12206.
6. Pfaller MA, Andes DR, Diekema DJ, Horn DL, Reboli AC, Rotstein C, Franks B, Azie NE. 2014. Epidemiology and outcomes of invasive candidiasis due to non-albicans species of Candida in 2,496 patients: data from the Prospective Antifungal Therapy (PATH) registry 2004-2008. PLoS One 9:e101510. http://dx.doi.org/10.1371/journal.pone.0101510.
7. Trofa D, Gacser A, Nosanchuk JD. 2008. Candida parapsilosis, an emerging fungal pathogen. Clin Microbiol Rev 21:606-625. http://dx.doi.org /10.1128/CMR.00013-08.
8. Pammi M, Holland L, Butler G, Gacser A, Bliss JM. 2013. Candida parapsilosis is a significant neonatal pathogen: a systematic review and meta-analysis. Pediatr Infect Dis J 32:e206-e216. http://dx.doi.org/10 .1097/INF.0b013e3182863a1c.
9. Pappas PG, Kauffman CA, Andes D, Benjamin DK, Jr, Calandra TF, Edwards JE, Jr, Filler SG, Fisher JF, Kullberg BJ, Ostrosky-Zeichner L, Reboli AC, Rex JH, Walsh TJ, Sobel JD. 2009. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 48:503-535. http://dx.doi.org /10.1086/596757.
10. Raghuram A, Restrepo A, Safadjou S, Cooley J, Orloff M, Hardy D, Butler S, Koval CE. 2012. Invasive fungal infections following liver transplantation: incidence, risk factors, survival, and impact of fluconazoleresistant Candida parapsilosis (2003-2007). Liver Transplant 18:1100-1109. http://dx.doi.org/10.1002/lt.23467.
11. Cleveland AA, Farley MM, Harrison LH, Stein B, Hollick R, Lockhart SR, Magill SS, Derado G, Park BJ, Chiller TM. 2012. Changes in incidence and antifungal drug resistance in candidemia: results from popula-tion- based laboratory surveillance in Atlanta and Baltimore, 2008-2011. Clin Infect Dis 55:1352-1361. http://dx.doi.org/10.1093/cid/cis697.
12. Sanglard D, Odds FC. 2002. Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis 2:73-85. http://dx.doi.org/10.1016/S1473-3099(02)00181-0.
13. Silva AP, Miranda IM, Guida A, Synnott J, Rocha R, Silva R, Amorim A, Pina-Vaz C, Butler G, Rodrigues AG. 2011. Transcriptional profiling of azole-resistant Candida parapsilosis strains. Antimicrob Agents Chemother 55:3546-3556. http://dx.doi.org/10.1128/AAC.01127-10.
14. Reiss E, Lasker BA, Lott TJ, Bendel CM, Kaufman DA, Hazen KC, Wade KC, McGowan KL, Lockhart SR. 2012. Genotyping of Candida parapsilosis from three neonatal intensive care units (NICUs) using a panel of five multilocus microsatellite markers: broad genetic diversity and a cluster of related strains in one NICU. Infect Genet Evol 12:1654-1660. http://dx.doi.org/10.1016/j.meegid.2012.06.012.
15. Dieringer D, Schlötterer C. 2003. Microsatellite Analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167-169. http://dx.doi.org/10.1046/j.1471-8286.2003.00351.x.
16. Nei M, Tajima F, Tateno Y. 1983. Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19:153-170.
17. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. http://dx.doi.org/10.1186/gb-2007-8-2-r19.
18. Perea S, Lopez-Ribot JL, Kirkpatrick WR, McAtee RK, Santillan RA, Martinez M, Calabrese D, Sanglard D, Patterson TF. 2001. 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 45:2676-2684. http://dx.doi.org/10.1128/AAC.45.10.2676 -2684.2001.
19. Xiang MJ, Liu JY, Ni PH, Wang S, Shi C, Wei B, Ni YX, Ge HL. 2013. Erg11 mutations associated with azole resistance in clinical isolates of Candida albicans. FEMS Yeast Res 13:386-393. http://dx.doi.org/10.1111 /1567-1364.12042.
20. Morio F, Loge C, Besse B, Hennequin C, Le Pape P. 2010. Screening for amino acid substitutions in the Candida albicans Erg11 protein of azolesusceptible and azole-resistant clinical isolates: new substitutions and a review of the literature. Diagn Microbiol Infect Dis 66:373-384. http://dx .doi.org/10.1016/j.diagmicrobio.2009.11.006.
21. Forastiero A, Mesa-Arango AC, Alastruey-Izquierdo A, Alcazar-Fuoli L, Bernal-Martinez L, Pelaez T, Lopez JF, Grimalt JO, Gomez-Lopez A, Cuesta I, Zaragoza O, Mellado E. 2013. Candida tropicalis antifungal cross-resistance is related to different azole target (Erg11p) modifications. Antimicrob Agents Chemother 57:4769-4781. http://dx.doi.org/10.1128 /AAC.00477-13.
22. Kelly SL, Lamb DC, Kelly DE. 1999. Y132H substitution in Candida albicans sterol 14alpha-demethylase confers fluconazole resistance by preventing binding to haem.FEMSMicrobiol Lett 180:171-175. http://dx.doi .org/10.1016/S0378-1097(99)00478-4.
23. Pfaller MA, Andes D, Diekema DJ, Espinel-Ingroff A, Sheehan D. 2010. Wild-type MIC distributions, epidemiological cutoff values and speciesspecific clinical breakpoints for fluconazole and Candida: time for harmonization of CLSI and EUCAST broth microdilution methods. Drug Resist Updat 13:180-195. http://dx.doi.org/10.1016/j.drup.2010.09.002.
24. Clinical and Laboratory Standards Institute. 2012. M27-S4 reference method for broth dilution antifungal susceptibility testing of yeasts; fourth informational supplement. Clinical and Laboratory Standards Institute, Wayne, PA.
25. Dunkel N, Blass J, Rogers PD, Morschhauser J. 2008. Mutations in the multi-drug resistance regulator MRR1, followed by loss of heterozygosity, are the main cause of MDR1 overexpression in fluconazole-resistant Candida albicans strains. Mol Microbiol 69:827-840. http://dx.doi.org/10 .1111/j.1365-2958.2008.06309.x.
26. Eddouzi J, Parker JE, Vale-Silva LA, Coste A, Ischer F, Kelly S, Manai M, Sanglard D. 2013. Molecular mechanisms of drug resistance in clinical Candida species isolated from Tunisian hospitals. Antimicrob Agents Chemother 57:3182-3193. http://dx.doi.org/10.1128/AAC.00555-13.
27. Morio F, Pagniez F, Besse M, Gay-andrieu F, Miegeville M, Le Pape P. 2013. Deciphering azole resistance mechanisms with a focus on transcription factor-encoding genes TAC1, MRR1 and UPC2 in a set of flucona-zole- resistant clinical isolates of Candida albicans. Int J Antimicrob Agents 42:410-415. http://dx.doi.org/10.1016/j.ijantimicag.2013.07.013.
28. Schubert S, Rogers PD, Morschhauser J. 2008. Gain-of-function mutations in the transcription factor MRR1 are responsible for overexpression of the MDR1 efflux pump in fluconazole-resistant Candida dubliniensis strains. Antimicrob Agents Chemother 52:4274-4280. http://dx.doi.org /10.1128/AAC.00740-08.
29. Schubert S, Barker KS, Znaidi S, Schneider S, Dierolf F, Dunkel N, Aid M, Boucher G, Rogers PD, Raymond M, Morschhauser J. 2011. Regulation of efflux pump expression and drug resistance by the transcription factors Mrr1, Upc2, and Cap1 in Candida albicans. Antimicrob Agents Chemother 55:2212-2223. http://dx.doi.org/10.1128/AAC.01343-10.