RNA sequencing revealed novel actors of the acquisition of drug resistance in Candida albicans

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Dhamgaye, Sanjiveeni ^a   Bernard, Maria ^c,d,e   Lelandais, Gaelle ^f   Sismeiro, Odile ^g   Lemoine, Sophie ^c,d,e   Coppée, Jean Yves ^g   Le Crom, Stéphane ^c,d,e   Prasad, Rajendra ^a   Devaux, Frédéric ^b  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b UMR 7238   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d INSERM   (France)

^e CNRS   (France)

^f INSTITUT NATIONAL DE LA TRANSFUSION SANGUINE   (France)

^g INSTITUT PASTEUR   (France)

Author keywords

Candida albicans; CZF1; Multidrug resistance; RNA seq; Yeast

Indexed keywords

AMPHOTERICIN B; ANISOMYCIN; BETA GLUCAN; CASPOFUNGIN; KETOCONAZOLE; RNA; TERBINAFINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CZF1; TRANSCRIPTION FACTOR TAC1; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA ALBICANS; CARBOHYDRATE SYNTHESIS; CELL WALL; CORRELATION ANALYSIS; CZF1 GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; RNA SEQUENCE; RNA TRANSCRIPTION; TAC1 GENE; TRANSCRIPTION REGULATION;

BETA-GLUCANS; CANDIDA ALBICANS; DRUG RESISTANCE, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION FACTORS;

CANDIDA; CANDIDA ALBICANS;

EID: 84866368685     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-396     Document Type: Article

References (60)

1. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Meis JF, Gould IM, Fu W, Colombo AL, Rodriguez-Noriega E. Global Antifungal Surveillance Study: Results from the ARTEMIS DISK Global Antifungal Surveillance study, 1997 to 2005: an 8.5-year analysis of susceptibilities ofCandidaspecies and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol 2007, 45:1735-1745. 10.1128/JCM.00409-07, 1933070, 17442797.
2. Odds FC, Brown AJ, Gow NA. Antifungal agents: mechanisms of action. Trends Microbiol 2003, 11:272-279. 10.1016/S0966-842X(03)00117-3, 12823944.
3. Anderson JB. Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat Rev Microbiol 2005, 3:547-556. 10.1038/nrmicro1179, 15953931.
4. Akins RA. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med Mycol 2005, 43:285-318. 10.1080/13693780500138971, 16110776.
5. Barker KS, Rogers PD. Recent insights into the mechanisms of antifungal resistance. Curr Infect Dis Rep 2006, 8:449-456. 10.1007/s11908-006-0019-3, 17064638.
6. Lopez-Ribot JL, McAtee RK, Lee LN, Kirkpatrick WR, White TC, Sanglard D, Patterson TF. Distinct patterns of gene expression associated with development of fluconazole resistance in serial Candida albicans isolates from human immunodeficiency virus-infected patients with oropharyngeal candidiasis. Antimicrob Agents Chemother 1998, 42:2932-2937. 105968, 9797228.
7. Saidane S, Weber S, De Deken X, St-Germain G, Raymond M. PDR16-mediated azole resistance in Candida albicans. Mol Microbiol 2006, 60:1546-1562. 10.1111/j.1365-2958.2006.05196.x, 16796687.
8. Sanglard D, Kuchler K, Ischer F, Pagani JL, Monod M, Bille J. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob Agents Chemother 1995, 39:2378-2386. 10.1128/AAC.39.11.2378, 162951, 8585712.
9. Schubert S, Barker KS, Znaidi S, Schneider S, Dierolf F, Dunkel N, Aïd M, Boucher G, Rogers PD, Raymond M, Morschhäuser J. Regulation of efflux pump expression and drug resistance by the transcription factors Mrr1, Upc2, and Cap1 in Candida albicans. Antimicrob Agents Chemother 2011, 55:2212-2223. 10.1128/AAC.01343-10, 3088179, 21402859.
10. Ben-Yaacov R, Knoller S, Caldwell GA, Becker JM, Koltin Y. Candida albicans gene encoding resistance to benomyl and methotrexate is a multidrug resistance gene. Antimicrob Agents Chemother 1994, 38:648-652. 10.1128/AAC.38.4.648, 284519, 8031026.
11. Lucau-Danila A, Lelandais G, Kozovska Z, Tanty V, Delaveau T, Devaux F, Jacq C. Early expression of yeast genes affected by chemical stress. Mol Cell Biol 2005, 25:1860-1868. 10.1128/MCB.25.5.1860-1868.2005, 549374, 15713640.
12. Prasad R, De Wergifosse P, Goffeau A, Balzi E. 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. 10.1007/BF00352101, 7614555.
13. Sanglard D, Ischer F, Monod M, Bille J. Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 1997, 143:405-416. 10.1099/00221287-143-2-405, 9043118.
14. Coste AT, Karababa M, Ischer F, Bille J, Sanglard D. 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 2004, 3:1639-1652. 10.1128/EC.3.6.1639-1652.2004, 539021, 15590837.
15. Selmecki A, Gerami-Nejad M, Paulson C, Forche A, Berman J. An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol Microbiol 2008, 68:624-641. 10.1111/j.1365-2958.2008.06176.x, 18363649.
16. Coste A, Selmecki A, Forche A, Diogo D, Bougnoux ME, d'Enfert C, Berman J, Sanglard D. Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 2007, 6:1889-1904. 10.1128/EC.00151-07, 2043391, 17693596.
17. Hoehamer CF, Cummings ED, Hilliard GM, Morschhäuser J, Rogers PD. Proteomic analysis of Mrr1p- and Tac1p-associated differential protein expression in azole-resistant clinical isolates of Candida albicans. Proteomics Clin Appl 2009, 3:968-978. 10.1002/prca.200800252, 21136999.
18. Liu TT, Znaidi S, Barker KS, Xu L, Homayouni R, Saidane S, Morschhäuser J, Nantel A, Raymond M, Rogers PD. Genome-wide expression and location analyses of the Candida albicans Tac1p regulon. Eukaryot Cell 2007, 6:2122-2138. 10.1128/EC.00327-07, 2168409, 17905926.
19. Znaidi S, De Deken X, Weber S, Rigby T, Nantel A, Raymond M. The zinc cluster transcription factor Tac1p regulates PDR16 expression in Candida albicans. Mol Microbiol 2006, 66:440-452.
20. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10:57-63. 10.1038/nrg2484, 2949280, 19015660.
21. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320:1344-1349. 10.1126/science.1158441, 2951732, 18451266.
22. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, Schmidt D, O'Keeffe S, Haas S, Vingron M, Lehrach H, Yaspo ML. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 2008, 321:956-960. 10.1126/science.1160342, 18599741.
23. Xiong Y, Chen X, Chen Z, Wang X, Shi S, Wang X, Zhang J, He X. RNA sequencing shows no dosage compensation of the active X-chromosome. Nat Genet 2010, 42:1043-1047. 10.1038/ng.711, 21102464.
24. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010, 28:503-510. 10.1038/nbt.1633, 2868100, 20436462.
25. Bruno VM, Wang Z, Marjani SL, Euskirchen GM, Martin J, Sherlock G, Snyder M. Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res 2010, 20:1451-1458. 10.1101/gr.109553.110, 2945194, 20810668.
26. Tuch BB, Mitrovich QM, Homann OR, Hernday AD, Monighetti CK, De La Vega FM, Johnson AD. The transcriptomes of two heritable cell types illuminate the circuit governing their differentiation. PLoS Genet 2010, 6:e1001070. 10.1371/journal.pgen.1001070, 2924316, 20808890.
27. Sellam A, Hogues H, Askew C, Tebbji F, van Het Hoog M, Lavoie H, Kumamoto CA, Whiteway M, Nantel A. Experimental annotation of the human pathogen Candida albicans coding and noncoding transcribed regions using high-resolution tiling arrays. Genome Biol 2010, 11:R71. 10.1186/gb-2010-11-7-r71, 2926782, 20618945.
28. Franz R, Ruhnke M, Morschhäuser J. Molecular aspects of fluconazole resistance development in Candida albicans. Mycoses 1999, 42:453-458. 10.1046/j.1439-0507.1999.00498.x, 10546486.
29. Banerjee D, Lelandais G, Shukla S, Mukhopadhyay G, Jacq C, Devaux F, Prasad R. Responses of pathogenic and nonpathogenic yeast species to steroids reveal the functioning and evolution of multidrug resistance transcriptional networks. Eukaryot Cell 2008, 7:68-77. 10.1128/EC.00256-07, 2224153, 17993571.
30. Cruz MC, Goldstein AL, Blankenship JR, Del Poeta M, Davis D, Cardenas ME, Perfect JR, McCusker JH, Heitman J. Calcineurin is essential for survival during membrane stress in Candida albicans. EMBO J 2002, 21:546-559. 10.1093/emboj/21.4.546, 125859, 11847103.
31. Sanglard D, Ischer F, Marchetti O, Entenza J, Bille J. Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 2003, 48:959-976. 10.1046/j.1365-2958.2003.03495.x, 12753189.
32. Klis FM, Sosinska GJ, de Groot PW, Brul S. Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEMS Yeast Res 2009, 9:1013-1028. 10.1111/j.1567-1364.2009.00541.x, 19624749.
33. Cantón E, Pemán J, Gobernado M, Alvarez E, Baquero F, Cisterna R, Gil J, Martín-Mazuelos E, Rubio C, Sánchez-Sousa A, Serrano C. Sensititre YeastOne caspofungin susceptibility testing of Candida clinical isolates: correlation with results of NCCLS M27-A2 multicenter study. Antimicrob Agents Chemother 2005, 49:1604-1607. 10.1128/AAC.49.4.1604-1607.2005, 1068645, 15793151.
34. White TC. 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 Chemother 1997, 41:1482-1487. 163944, 9210670.
35. Guida A, Lindstädt C, Maguire SL, Ding C, Higgins DG, Corton NJ, Berriman M, Butler G. Using RNA-seq to determine the transcriptional landscape and the hypoxic response of the pathogenic yeast Candida parapsilosis. BMC Genomics 2011, 12:628. 10.1186/1471-2164-12-628, 3287387, 22192698.
36. Vinces MD, Haas C, Kumamoto CA. Expression of the Candida albicans morphogenesis regulator gene CZF1 and its regulation by Efg1p and Czf1p. Eukaryot Cell 2006, 5:825-835. 10.1128/EC.5.5.825-835.2006, 1459686, 16682460.
37. Pickering BM, Willis AE. The implications of structured 5' untranslated regions on translation and disease. Semin Cell Dev Biol 2005, 16:39-47. 10.1016/j.semcdb.2004.11.006, 15659338.
38. Vilela C, McCarthy JE. Regulation of fungal gene expression via short open reading frames in the mRNA 5'untranslated region. Mol Microbiol 2003, 49:859-867. 10.1046/j.1365-2958.2003.03622.x, 12890013.
39. Lachke SA, Srikantha T, Soll DR. The regulation of EFG1 in white-opaque switching in Candida albicans involves overlapping promoters. Mol Microbiol 2003, 48:523-536. 10.1046/j.1365-2958.2003.t01-1-03448.x, 12675809.
40. Lohse MB, Johnson AD. White-opaque switching in Candida albicans. Curr Opin Microbiol 2009, 12:650-654. 10.1016/j.mib.2009.09.010, 2812476, 19853498.
41. Brown DH, Giusani AD, Chen X, Kumamoto CA. Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol Microbiol 1999, 34:651-662. 10.1046/j.1365-2958.1999.01619.x, 10564506.
42. Stichternoth C, Fraund A, Setiadi E, Giasson L, Vecchiarelli A, Ernst JF. Sch9 kinase integrates hypoxia and CO2 sensing to suppress hyphal morphogenesis in Candida albicans. Eukaryot Cell 2011, 10:502-511. 10.1128/EC.00289-10, 3127645, 21335533.
43. Giusani AD, Vinces M, Kumamoto CA. Invasive filamentous growth of Candida albicans is promoted by Czf1p-dependent relief of Efg1p-mediated repression. Genetics 2002, 160:1749-1753. 1462044, 11973327.
44. Lassak T, Schneider E, Bussmann M, Kurtz D, Manak JR, Srikantha T, Soll DR, Ernst JF. Target specificity of the Candida albicans Efg1 regulator. Mol Microbiol 2011, 82:602-618. 10.1111/j.1365-2958.2011.07837.x, 21923768.
45. Finkel JS, Xu W, Huang D, Hill EM, Desai JV, Woolford CA, Nett JE, Taff H, Norice CT, Andes DR, Lanni F, Mitchell AP. Portrait of Candida albicans adherence regulators. PLoS Pathog 2012, 8:e1002525. 10.1371/journal.ppat.1002525, 3280983, 22359502.
46. Kopecká M, Gabriel M. The influence of congo red on the cell wall and (1-3)-beta-D-glucan microfibril biogenesis in Saccharomyces cerevisiae. Arch Microbiol 1992, 158:115-126. 10.1007/BF00245214, 1417414.
47. Sohn K, Urban C, Brunner H, Rupp S. EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol Microbiol 2003, 47:89-102.
48. Zavrel M, Majer O, Kuchler K, Rupp S. Transcription factor Efg1 shows a haploinsufficiency phenotype in modulating the cell wall architecture and immunogenicity of Candida albicans. Eukaryot Cell 2012, 11:129-140. 10.1128/EC.05206-11, 3272906, 22140230.
49. Agarwal AK, Rogers PD, Baerson SR, Jacob MR, Barker KS, Cleary JD, Walker LA, Nagle DG, Clark AM. Genome-wide expression profiling of the response to polyene, pyrimidine, azole, and echinocandin antifungal agents in Saccharomyces cerevisiae. J Biol Chem 2003, 278:34998-35015. 10.1074/jbc.M306291200, 12824174.
50. Lagorce A, Hauser NC, Labourdette D, Rodriguez C, Martin-Yken H, Arroyo J, Hoheisel JD, François J. Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J Biol Chem 2003, 278:20345-20357. 10.1074/jbc.M211604200, 12644457.
51. Liu TT, Lee RE, Barker KS, Lee RE, Wei L, Homayouni R, Rogers PD. Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob Agents Chemother 2005, 49:2226-2236. 10.1128/AAC.49.6.2226-2236.2005, 1140538, 15917516.
52. García R, Rodríguez-Peña JM, Bermejo C, Nombela C, Arroyo J. The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J Biol Chem 2009, 284:10901-10911. 10.1074/jbc.M808693200, 2667776, 19234305.
53. Arias P, Díez-Muñiz S, García R, Nombela C, Rodríguez-Peña JM, Arroyo J. Genome-wide survey of yeast mutations leading to activation of the yeast cell integrity MAPK pathway: novel insights into diverse MAPK outcomes. BMC Genomics 2011, 12:390. 10.1186/1471-2164-12-390, 3167797, 21810245.
54. Douglas CM, D'Ippolito JA, Shei GJ, Meinz M, Onishi J, Marrinan JA, Li W, Abruzzo GK, Flattery A, Bartizal K, Mitchell A, Kurtz MB. Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob Agents Chemother 1997, 41:2471-2479. 164147, 9371352.
55. Park S, Kelly R, Kahn JN, Robles J, Hsu MJ, Register E, Li W, Vyas V, Fan H, Abruzzo G, Flattery A, Gill C, Chrebet G, Parent SA, Kurtz M, Teppler H, Douglas CM, Perlin DS. Specific substitutions in the echinocandin target Fks1p account for reduced susceptibility of rare laboratory and clinical Candida sp. isolates. Antimicrob Agents Chemother 2005, 49:3264-3273. 10.1128/AAC.49.8.3264-3273.2005, 1196231, 16048935.
56. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25:1966-1967. 10.1093/bioinformatics/btp336, 19497933.
57. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G. GO:: TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004, 20:3710-3715. 10.1093/bioinformatics/bth456, 3037731, 15297299.
58. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106. 10.1186/gb-2010-11-10-r106, 3218662, 20979621.
59. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140. 10.1093/bioinformatics/btp616, 2796818, 19910308.
60. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2012,