The Rpd3/Hda1 family of histone deacetylases regulates azole resistance in Candida albicans

Journal of Antimicrobial Chemotherapy

Volumn 70, Issue 7, 2015, Pages 1993-2003

  Li, Xiaofang ^a,b   Cai, Qing ^a,b,c   Mei, Huan ^a,b   Zhou, Xiaowei ^a,b   Shen, Yongnian ^a,b   Li, Dongmei ^a,b,d   Liu, Weida ^a,b  

^a INSTITUTE OF DERMATOLOGY   (China)

^b Jiangsu Key Laboratory of Molecular Biology for Skin Diseases and STIs   (China)

^c Shanghai Dermatology Hospital   (China)

^d GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

C. albicans; Histone deacetylase inhibitors; Histone deacetylation; Trichostatin A

Indexed keywords

ANTIFUNGAL AGENT; FLUCONAZOLE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; ITRACONAZOLE; PYRROLE DERIVATIVE; STERILE WATER; TRICHOSTATIN A; VORICONAZOLE;

ADAPTATION; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA ALBICANS; DEACETYLATION; FUNGAL VIRULENCE; GENE EXPRESSION; IN VITRO STUDY; INHIBITORY CONCENTRATION; MORPHOGENESIS; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84936943259     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkv070     Document Type: Article

References (50)

1. Alcazar-Fuoli L, Mellado E. Current status of antifungal resistance and its impact on clinical practice. Br J Haematol 2014; 166: 471-84.
2. Tang HJ, Liu WL, Lin HL et al. Epidemiology and prognostic factors of candidemia in cancer patients. PLoS One 2014; 9: e99103.
3. Guo F, Yang Y, Kang Y et al. Invasive candidiasis in intensive care units in China: a multicentre prospective observational study. J Antimicrob Chemother 2013; 68: 1660-8.
4. Sanglard D, Coste A, Ferrari S. Antifungal drug resistance mechanisms in fungal pathogens from the perspective of transcriptional gene regulation. FEMS Yeast Res 2009; 9: 1029-50.
5. Espinel-Ingroff A. Mechanisms of resistance to antifungal agents: yeasts and filamentous fungi. Rev Iberoam Micol 2008; 25: 101-6.
6. Morio F, Pagniez F, Lacroix C et al. Amino acid substitutions in the Candida albicans sterol Δ5, 6-desaturase (Erg3p) confer azole resistance: characterization of two novel mutants with impaired virulence. J Antimicrob Chemother 2012; 67: 2131-8.
7. Arthington-Skaggs BA, Lee-Yang W, Ciblak MA et al. Comparison of visual and spectrophotometricmethods of brothmicrodilutionMICendpoint determination and evaluation of a sterol quantitationmethod for in vitro susceptibility testing of fluconazole and itraconazole against trailing and nontrailing Candida isolates. Antimicrob Agents Chemother 2002; 46: 2477-81.
8. Lee MK, Kim HR, Kang JO et al. Susceptibility and trailing growth of Candida albicans to fluconazole: results of a Korean multicentre study. Mycoses 2007; 50: 148-9.
9. Lee MK, Williams LE, Warnock DWet al. Drug resistance genes and trailing growth in Candida albicans isolates. J Antimicrob Chemother 2004; 53: 217-24.
10. Wang AH, Bertos NR, Vezmar M et al. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol Cell Biol 1999; 19: 7816-27.
11. Emiliani S, FischleW, Van Lint C et al. Characterization of a human RPD3 ortholog, HDAC3. Proc Natl Acad Sci USA 1998; 95: 2795-800.
12. Grozinger CM, Hassig CA, Schreiber SL. Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc Natl Acad Sci USA 1999; 96: 4868-73.
13. Yang XJ, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 2008; 9: 206-18.
14. Khan SN, Khan AU. Role of histone acetylation in cell physiology and diseases: an update. Clin Chim Acta 2010; 411: 1401-11.
15. Bernstein BE, Tong JK, Schreiber SL. Genomewide studies of histone deacetylase function in yeast. Proc Natl Acad Sci USA 2000; 97: 13708-13.
16. Pontiki E, Hadjipavlou-Litina D. Histone deacetylase inhibitors (HDACIs). Structure-activity relationships: history and new QSAR perspectives. Med Res Rev 2012; 32: 1-165.
17. Carmen AA, Rundlett SE, Grunstein M. HDA1 and HDA3 are components of a yeast histone deacetylase (HDA) complex. J Biol Chem 1996; 271: 15837-44.
18. Liu L, Chen B, Qin S et al. A novel histone deacetylase inhibitor chidamide induces apoptosis of human colon cancer cells. Biochem Biophys Res Commun 2010; 392: 190-5.
19. Wagner JM, Hackanson B, Lübbert M et al. Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy. Clin Epigenetics 2010; 1: 117-36.
20. Beumer JH, Tawbi H. Role of histone deacetylases and their inhibitors in cancer biology and treatment. Curr Clin Pharmacol 2010; 5: 196-208.
21. Bolden JE, Peart MJ, Johnstone RW et al. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Disc 2006; 5: 769-84.
22. Sharma SV, Lee DY, Li B et al. A chromatin-mediated reversible drugtolerant state in cancer cell subpopulations. Cell 2010; 141: 69-80.
23. Rebecca VW, Smalley KS. Tumor heterogeneity and strategies to overcome kinase inhibitor resistance in cancer: lessons from melanoma. Expert Opin Investig Drugs 2011; 20: 137-40.
24. Wurtele H, Tsao S, Lépine G et al. Modulation of histone H3 lysine 56 acetylation as an antifungal therapeutic strategy. NatMed 2010; 16: 774-80.
25. Smith WL, Edlind TD. Histone deacetylase inhibitors enhance Candida albicans susceptibility to azoles and related antifungals: correlation with reduction in CDR and ERG upregulation. Antimicrob Agents Chemother 2002; 46: 3532-9.
26. Pfaller MA, Messer SA, Georgopapadakou N et al. Activity of MGCD290, a Hos2 histone deacetylase inhibitor, in combination with azole antifungals against opportunistic fungal pathogens. J ClinMicrobiol 2009; 47: 3797-804.
27. Mai A, Rotili D, Massa S et al. Discovery of uracil-based histone deacetylase inhibitors able to reduce acquired antifungal resistance and trailing growth in Candida albicans. Bioorg Med Chem Lett 2007; 17: 1221-5.
28. Morschhäuser J. Regulation of multidrug resistance in pathogenic fungi. Fungal Genet Biol 2010; 47: 94-106.
29. Srikantha T, Tsai L, Daniels K et al. The histone deacetylase genes HDA1 and RPD3 play distinct roles in regulation of high-frequency phenotypic switching in Candida albicans. J Bacteriol 2001; 183: 4614-25.
30. White TC, Pfaller MA, Rinaldi MG et al. Stable azole drug resistance associated with a substrain of Candida albicans from an HIV-infected patient. Oral Dis 1997; 3 Suppl 1: S102-9.
31. White TC. The presence of an R467 K amino acid substitution and loss of allelic variation correlate with an azole-resistant lanosterol 14alpha demethylase in Candida albicans. Antimicrob Agents Chemother 1997; 41: 1488-94.
32. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: Approved Standard M27-A3. CLSI, Wayne, PA, USA, 2008.
33. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: Fourth Informational Supplement M27-S4. CLSI, Wayne, PA, USA, 2012.
34. Yan L, Zhang JD, Cao YB, Gao PH, Jiang YY. Proteomic analysis reveals a metabolism shift in a laboratory fluconazole-resistant Candida albicans strain. J Proteome Res 2007; 6: 2248-56.
35. 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: 1482-7.
36. Riddihough G, Zahn LM. Epigenetics. What is epigenetics? Introduction. Science 2010; 330: 611.
37. Bonasio R, Tu S, Reinberg D. Molecular signals of epigenetic states. Science 2010; 330: 612-6.
38. Kaminsky ZA, Tang T, Wang SC et al. DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet 2009; 41: 240-5.
39. Hnisz D, Majer O, Frohner IE et al. The Set3/Hos2 histone deacetylase complex attenuates cAMP/PKA signaling to regulate morphogenesis and virulence of Candida albicans. PLoS Pathog 2010; 6: e1000889.
40. Klar AJ, Srikantha T, Soll DR. A histone deacetylation inhibitor and mutant promote colony-type switching of the human pathogen Candida albicans. Genetics 2001; 158: 919-24.
41. Simonetti G, Passariello C, Rotili D et al. Histone deacetylase inhibitors may reduce pathogenicity and virulence in Candida albicans. FEMS Yeast Res 2007; 7: 1371-80.
42. Hnisz D, Schwarzmüller T, Kuchler K. Transcriptional loops meet chromatin: a dual-layer network controls white-opaque switching in Candida albicans. Mol Microbiol 2009; 74: 1-15.
43. Hnisz D, Bardet AF, Nobile CJ et al. A histone deacetylase adjusts transcription kinetics at coding sequences during Candida albicans morphogenesis. PLoS Genet 2012; 8: e1003118.
44. Zacchi LF, Schulz WL, Davis DA. HOS2 and HDA1 encode histone deacetylases with opposing roles in Candida albicans morphogenesis. PLoS One 2010; 5: e12171.
45. Tebarth B, Doedt T, Krishnamurthy S et al. Adaptation of the Efg1p morphogenetic pathway in Candida albicans by negative autoregulation and PKA-dependent repression of the EFG1 gene. J Mol Biol 2003; 329: 949-62.
46. Shen H, An MM, Wang DJ et al. Fcr1p inhibits development of fluconazole resistance in Candida albicans by abolishing CDR1 induction. Biol Pharm Bull 2007; 30: 68-73.
47. Morio F, Pagniez F, Besse M et al. Deciphering azole resistance mechanisms with a focus on transcription factor-encoding genes TAC1, MRR1 and UPC2 in a set of fluconazole-resistant clinical isolates of Candida albicans. Int J Antimicrob Agents 2013; 42: 410-5.
48. Robbins N, Leach MD, Cowen LE. Lysine deacetylases Hda1 and Rpd3 regulate Hsp90 function thereby governing fungal drug resistance. Cell Rep 2012; 2: 878-88.
49. Cowen LE. The fungal Achilles' heel: targeting Hsp90 to cripple fungal pathogens. Curr Opin Microbiol 2013; 16: 377-84.
50. Yu LH, Wei X, Ma M et al. Possible inhibitory molecular mechanism of farnesol on the development of fluconazole resistance in Candida albicans biofilm. Antimicrob Agents Chemother 2012; 56: 770-5.