Identification of aspergillus fumigates multidrug transporter genes and their potential involvement in antifungal resistance

Medical Mycology

Volumn 54, Issue 6, 2016, Pages 616-627

  Meneau, Isabelle ^a,b   Coste, Alix T ^a   Sanglard, Dominique ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITÄTSSPITAL ZÜRICH   (Switzerland)

Author keywords

Aspergillus; Azole resistance; Cyp51A; Multidrug transporters

Indexed keywords

ABC TRANSPORTER PDR5; ANTIFUNGAL AGENT; ATRF PROTEIN; ATRI PROTEIN; COMPLEMENTARY DNA; GENOMIC DNA; ITRACONAZOLE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN A; PYRROLE; UNCLASSIFIED DRUG; VORICONAZOLE; CARRIER PROTEIN; PYRROLE DERIVATIVE;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ASPERGILLUS FUMIGATUS; FUNGUS GROWTH; GENE DISRUPTION; GENE INACTIVATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; WILD TYPE; DRUG EFFECTS; ENZYMOLOGY; FUNGAL GENE; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; SACCHAROMYCES CEREVISIAE;

ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; AZOLES; DRUG RESISTANCE, FUNGAL; ENVIRONMENTAL MICROBIOLOGY; GENE EXPRESSION; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; HUMANS; MEMBRANE TRANSPORT PROTEINS; SACCHAROMYCES CEREVISIAE;

EID: 84981742378     PISSN: 13693786     EISSN: 14602709     Source Type: Journal    
DOI: 10.1093/mmy/myw005     Document Type: Article

References (62)

1. Latge JP. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 1999; 12: 310-350.
2. Groll AH, Shah PM, Mentzel C et al. Trends in the postmortem epidemiology of invasive fungal infections at a university hospital. J Infect 1996; 33: 23-32.
3. Cowen LE, Sanglard D, Howard SJ et al. Mechanisms of antifungal drug resistance. Cold Spring Harb Perspect Med 2014:a019752.
4. Pfaller MA. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am. J. Med 2012; 125 (1 Suppl): S3-S13.
5. Bowyer P, Moore CB, Rautemaa R et al. azole antifungal resistance today: focus on Aspergillus. Curr Infect Dis Rep 2011; 13: 485-491.
6. Denning DW. Invasive aspergillosis. Clin Infect Dis 1998; 26: 781-803; quiz 804-785.
7. Diaz-Guerra TM, Mellado E, Cuenca-Estrella M et al. A point mutation in the 14alpha-sterol demethylase gene cyp51A contributes to itraconazole resistance in Aspergillus fumigatus. Antimicrob Agents Chemother 2003; 47: 1120-1124.
8. Mellado E, Garcia-Effron G, Alcazar-Fuoli L et al. Substitutions at methionine 220 in the 14alpha-sterol demethylase (Cyp51A) of Aspergillus fumigatus are responsible for resistance in vitro to azole antifungal drugs. Antimicrob Agents Chemother 2004; 48: 2747-2750.
9. Mosquera J, Denning DW. Azole cross-resistance in Aspergillus fumigatus. Antimicrob Agents Chemother 2002; 46: 556-557.
10. Snelders E, Huis I’nt Veld RA, Rijs AJ et al. Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Appl Environ Microbiol 2009; 75: 4053-4057.
11. Snelders E, van der Lee HAL, Kuijpers J et al. Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med 2008; 5: e219.
12. van Ingen J, van der Lee HAL, Rijs AJMM et al. High-level panazole-resistant aspergillosis. J Clin Microbiol 2015: JCM.00502-00515-00510.
13. Kidd SE, Goeman E, Meis JF et al. Multi-triazole-resistant Aspergillus fumigatus infections in Australia. Mycoses 2015; 58: 350-355.
14. Snelders E, Melchers WJ, Verweij PE. Azole resistance in Aspergillus fumigatus: a new challenge in the management of invasive aspergillosis? Future Microbiol 2011; 6: 335-347.
15. Perlin DS, Shor E, Zhao Y. Update on antifungal drug resistance. Curr Clin Microbiol Reports 2015; 2: 84-95.
16. Chowdhary A, Kathuria S, Xu J et al. Emergence of azole-resistant Aspergillus fumigatus strains due to agricultural azole use creates an increasing threat to human health. PLoS Pathog 2013; 9: e1003633.
17. Verweij PE, Snelders E, Kema GHJ et al. Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use? Lancet Infect Dis 2009; 9: 789-795.
18. Nascimento AM, Goldman GH, Park S et al. Multiple resistance mechanisms among Aspergillus fumigatus mutants with high-level resistance to itraconazole. Antimicrob Agents Chemother 2003; 47: 1719-1726.
19. da Silva Ferreira ME, Capellaro JL, dos Reis Marques E et al. In vitro evolution of itraconazole resistance in Aspergillus fumigatus involves multiple mechanisms of resistance. Antimicrob Agents Chemother 2004; 48: 4405-4413.
20. Slaven JW, Anderson MJ, Sanglard D et al. Increased expression of a novel Aspergillus fumigatus ABC transporter gene, atrF, in the presence of itraconazole in an itraconazole resistant clinical isolate. Fungal Genet Biol 2002; 36: 199-206.
21. Fraczek MG, Bromley M, Buied A et al. The cdr1B efflux transporter is associated with non-cyp51a-mediated itraconazole resistance in Aspergillus fumigatus. J Antimicrob Chemother 2013; 68: 1486-1496.
22. Paul S, Diekema D, Moye-Rowley WS. Contributions of As-pergillus fumigatus ATP-binding cassette transporter proteins to drug resistance and virulence. Eukaryot. Cell. 2013; 12: 1619-1628.
23. Paul S, Moye-Rowley WS. Functional analysis of an ATP-binding cassette transporter protein from Aspergillus fumigates by heterologous expression in Saccharomyces cerevisiae. Fungal Genet Biol 2013; 57(C): 85-91.
24. Balzi E, Wang M, Leterme S et al. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J Biol Chem 1994; 269: 2206-2214
25. Cove DJ. The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochim Biophys Acta 1966; 113: 51-56.
26. Minet M, Dufour ME, Lacroute F. Complementation of Saccha-romyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J 1992; 2: 417-422.
27. Punt PJ, Oliver RP, Dingemanse MA et al. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 1987; 56: 117-124.
28. Malardier L, Daboussi MJ, Julien J et al. Cloning of the nitrate reductase gene (niaD) of Aspergillus nidulans and its use for transformation of Fusarium oxysporum. Gene 1989; 78: 147-156.
29. Girardin H, Latge JP, Srikantha T et al. Development of DNA probes for fingerprinting Aspergillus fumigatus. J Clin Microbiol 1993; 31: 1547-1554.
30. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard-Second Edition. CLSI document M38-A2. Wayne, Pa: CLSI; 2008.
31. Mahe Y, Parle-McDermott A, Nourani A et al. The ATP-binding cassette multidrug transporter Snq2 of Saccharomyces cerevisiae: a novel target for the transcription factors Pdr1 and Pdr3. Mol Microbiol 1996; 20: 109-117.
32. Schrettl M, Kim HS, Eisendle M et al. SreA-mediated iron regulation in Aspergillus fumigatus. Mol Microbiol 2008; 70: 27-43.
33. Kovalchuk A, Driessen AJM. Phylogenetic analysis of fungal ABC transporters. BMC Genomics 2010; 11: 177.
34. Walker JE, Saraste M, Runswick MJ et al. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. Embo J 1982; 1: 945-951.
35. Pain A, Woodward J, Quail MA et al. Insight into the genome of Aspergillus fumigatus: analysis of a 922 kb region encompassing the nitrate assimilation gene cluster. Fungal Genet Biol 2004; 41: 443-453.
36. Costa C, Dias PJ, Sa-Correia I. et al. MFS multidrug transporters in pathogenic fungi: do they have real clinical impact? Front Physiol 2014; 5: 197.
37. Calabrese D, Bille J, Sanglard D. A novel multidrug efflux transporter gene of the major facilitator superfamily from Candida albicans (FLU1) conferring resistance to fluconazole. Microbiology (Reading, Engl) 2000; 146 (Pt 11): 2743-2754.
38. Cheeseman K, Ropars J, Renault P et al. Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nature Communications 2014; 5: 1-9.
39. Lessing F, Kniemeyer O, Wozniok I et al. The Aspergillus fu-migatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot Cell 2007; 6: 2290-2302.
40. Del Sorbo G, Andrade AC, Van Nistelrooy JG et al. Multidrug resistance in Aspergillus nidulans involves novel ATP-binding cassette transporters. Mol Gen Genet 1997; 254: 417-426.
41. Prasad R, De Wergifosse P, Goffeau A et al. Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr Genet 1995; 27: 320-329.
42. Tobin MB, Peery RB, Skatrud PL. Genes encoding multiple drug resistance-like proteins in Aspergillus fumigatus and Aspergillus flavus. Gene 1997; 200: 11-23.
43. Meneau I, Sanglard D. Azole and fungicide resistance in clinical and environmental Aspergillus fumigatus isolates. Med. Mycol 2005; 43 Suppl 1: S307-311.
44. Howard SJ, Cerar D, Anderson MJ et al. Frequency and evolution of azole resistance in Aspergillus fumigatus associated with treatment failure. Emerging Infect Dis 2009; 15: 1068-1076.
45. Snelders E, Karawajczyk A, Schaftenaar G et al. Azole resistance profile of amino acid changes in Aspergillus fumigatus CYP51A based on protein homology modeling. Antimicrob Agents Chemother 2010; 54: 2425-2430.
46. Escribano P, Recio S, Pel áez T et al. Aspergillus fumigates strains with mutations in the cyp51A gene do not always show phenotypic resistance to itraconazole, voriconazole, or posaconazole. Antimicrob Agents Chemother 2011; 55: 2460-2462.
47. Semighini CP, Marins M, Goldman MH et al. Quantitative analysis of the relative transcript levels of ABC transporter Atr genes in Aspergillus nidulans by real-time reverse transcription-PCR assay. Appl Environ Microbiol 2002; 68: 1351-1357.
48. Kretschmer M, Leroch M, Mosbach A et al. fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 2009; 5: e1000696.
49. Moye-Rowley WS. Multidrug resistance in fungi: regulation of transporter-encoding gene expression. Front Physiol 2014; 5: 1-14.
50. Denning DW, Perlin DS. Azole resistance in Aspergillus: a growing public health menace. Future Microbiol 2011; 6: 1229-1232.
51. Rajendran R, Mowat E, McCulloch E et al. Azole resistance of Aspergillus fumigatus biofilms is partly associated with efflux pump activity. Antimicrob. Agents Chemother 2011; 55: 2092-2097.
52. Pham CD, Lockhart SR. An Invisible Threat: mutation-mediated resistance to triazole drugs in Aspergillus. Curr Fungal Infect Rep 2012; 6: 288-295.
53. Abdolrasouli A, Rhodes J, Beale MA et al. genomic context of azole resistance mutations in Aspergillus fumigatus determined using whole-genome sequencing. mBio 2015; 6: e00536-00515-00512.
54. Losada L, Sugui JA, Eckhaus MA et al. genetic analysis using an isogenic mating pair of Aspergillus fumigatus identifies azole resistance genes and lack of MAT locus’s role in virulence. PLoS Pathog 2015; 11: e1004834-1004823.
55. Sanglard D, Kuchler K, Ischer F et al. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. An-timicrob Agents Chemother 1995; 39: 2378-2386.
56. Alarco AM, Balan I, Talibi D et al. AP1-mediated multidrug resistance in Saccharomyces cerevisiae requires FLR1 encoding a transporter of the major facilitator superfamily. J Biol Chem 1997; 272: 19304-19313
57. Qiao J, Kontoyiannis DP, Calderone R et al. Afyap1, encoding a bZip transcriptional factor of Aspergillus fumigatus, contributes to oxidative stress response but is not essential to the virulence of this pathogen in mice immunosuppressed by cyclophosphamide and triamcinolone. Med Mycol 2008; 46: 773-782.
58. Meneau I, Sanglard D. Azole and fungicide resistance in clinical and environmental Aspergillus fumigatus isolates. Med Mycol 2005; 43 Suppl 1: S307-311.
59. d’Enfert C. Selection of multiple disruption events in Aspergillus fumigatus using the orotidine-5′-decarboxylase gene, pyrG, as a unique transformation marker. Curr Genet 1996; 30: 76-82.
60. Denning DW, Clemons KV, Hanson LH et al. Restriction endonuclease analysis of total cellular DNA of Aspergillus fumigatus isolates of geographically and epidemiologically diverse origin. J Infect Dis 1990; 162: 1151-1158.
61. Denning DW, Venkateswarlu K, Oakley KL et al. Itraconazole resistance in Aspergillus fumigatus. Antimicrob Agents Chemother 1997; 41: 1364-1368.
62. Diaz-Guerra TM, Mellado E, Cuenca-Estrella M et al. A point mutation in the 14alpha-sterol demethylase gene cyp51A contributes to itraconazole resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother 2003; 47: 1120-1124