A histone deacetylase complex mediates biofilm dispersal and drug resistance in Candida albicans

mBio

Volumn 5, Issue 3, 2014, Pages

  Nobile, Clarissa J ^a,b   Fox, Emily P ^a   Hartooni, Nairi ^a   Mitchell, Kaitlin F ^c   Hnisz, Denes ^d,e   Andes, David R ^c   Kuchler, Karl ^d   Johnson, Alexander D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,10 PHENANTHROLINE; 4 NITROQUINOLINE 1 OXIDE; AMPHOTERICIN B; ANTIFUNGAL AGENT; CASPOFUNGIN; FLUCONAZOLE; HISTONE DEACETYLASE; PROTEIN HOS2; PROTEIN SET3; PROTEIN SIF2; PROTEIN SNT1; UNCLASSIFIED DRUG; FUNGAL PROTEIN;

ANTIFUNGAL RESISTANCE; ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL SUSPENSION; CELL VIABILITY; COMPLEX FORMATION; FUNGAL CELL; FUNGAL STRAIN; MINIMUM INHIBITORY CONCENTRATION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; CANDIDIASIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHYSIOLOGY;

ANTIFUNGAL AGENTS; BIOFILMS; CANDIDA ALBICANS; CANDIDIASIS; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; HUMANS; MICROBIAL SENSITIVITY TESTS;

EID: 84903954203     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01201-14     Document Type: Article

References (55)

1. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15: 167-193. http://dx. doi. org/10. 1128/CMR. 15. 2. 167-193. 2002.
2. Kojic EM, Darouiche RO. 2004. Candida infections of medical devices. Clin. Microbiol. Rev. 17: 255-267. http://dx. doi. org/10. 1128/CMR. 17. 2. 255-267. 2004.
3. Donlan RM. 2001. Biofilm formation: a clinically relevant microbiologi-cal process. Clin. Infect. Dis. 33: 1387-1392. http://dx. doi. org/10. 1086/322972.
4. Douglas LJ. 2002. Medical importance of biofilms in Candida infections. Rev. Iberoam. Micol. 19: 139-143. http://www. reviberoammicol. com/2002-19/139143. pdf.
5. Douglas LJ. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11: 30-36. http://dx. doi. org/10. 1016/S0966-842X(02)00002-1.
6. Wenzel RP. 1995. Nosocomial candidemia: risk factors and attributable mortality. Clin. Infect. Dis. 20: 1531-1534. http://dx. doi. org/10. 1093/clinids/20. 6. 1531.
7. Akins RA. 2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43: 285-318. http://dx. doi. org/10. 1080/13693780500138971.
8. Mathé L, Van Dijck P. 2013. Recent insights into Candida albicans biofilm resistance mechanisms. Curr. Genet. 59: 251-264. http://dx. doi. org/10. 1007/s00294-013-0400-3.
9. Ramage G, Rajendran R, Sherry L, Williams C. 2012. Fungal biofilm resistance. Int. J. Microbiol. 2012: 528521. http://dx. doi. org/10. 1155/2012/528521.
10. Taff HT, Mitchell KF, Edward JA, Andes DR. 2013. Mechanisms of Candida biofilm drug resistance. Future Microbiol. 8: 1325-1337. http://dx. doi. org/10. 2217/fmb. 13. 101.
11. Hawser SP, Douglas LJ. 1994. Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect. Immun. 62: 915-921.
12. Baillie GS, Douglas LJ. 1999. Role of dimorphism in the development of Candida albicans biofilms. J. Med. Microbiol. 48: 671-679. http://dx. doi. org/10. 1099/00222615-48-7-671.
13. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183: 5385-5394. http://dx. doi. org/10. 1128/JB. 183. 18. 5385-5394. 2001.
14. Nobile CJ, Mitchell AP. 2005. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15: 1150-1155. http://dx. doi. org/10. 1016/j. cub. 2005. 05. 047.
15. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, Köhler JR, Kadosh D, Lopez-Ribot JL. 2010. Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog. 6: e1000828. http://dx. doi. org/10. 1371/journal. ppat. 1000828.
16. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138. http://dx. doi. org/10. 1016/j. cell. 2011. 10. 048.
17. Fox EP, Nobile CJ. 2012. A sticky situation: untangling the transcriptional network controlling biofilm development in Candida albicans. Transcription 3: 315-322. http://dx. doi. org/10. 4161/trns. 22281.
18. Chen C, Pande K, French SD, Tuch BB, Noble SM. 2011. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe 10: 118-135. http://dx. doi. org/10. 1016/j. chom. 2011. 07. 005.
19. Finkel JS, Xu W, Huang D, Hill EM, Desai JV, Woolford CA, Nett JE, Taff H, Norice CT, Andes DR, Lanni F, Mitchell AP. 2012. Portrait of Candida albicans adherence regulators. PLoS Pathog. 8: e1002525. http://dx. doi. org/10. 1371/journal. ppat. 1002525.
20. Uppuluri P, Pierce CG, Thomas DP, Bubeck SS, Saville SP, Lopez-Ribot JL. 2010. The transcriptional regulator Nrg1p controls Candida albicans biofilm formation and dispersion. Eukaryot. Cell 9: 1531-1537. http://dx. doi. org/10. 1128/EC. 00111-10.
21. Lu Y, Su C, Liu H. 2012. A GATA transcription factor recruits Hda1 in response to reduced Tor1 signaling to establish a hyphal chromatin state in Candida albicans. PLoS Pathog. 8: e1002663. http://dx. doi. org/10. 1371/journal. ppat. 1002663.
22. Lu Y, Su C, Mao X, Raniga PP, Liu H, Chen J. 2008. Efg1-mediated recruitment of NuA4 to promoters is required for hypha-specific Swi/Snf binding and activation in Candida albicans. Mol. Biol. Cell 19: 4260-4272. http://dx. doi. org/10. 1091/mbc. E08-02-0173.
23. Hnisz D, Bardet AF, Nobile CJ, Petryshyn A, Glaser W, Schöck U, Stark A, Kuchler K. 2012. A histone deacetylase adjusts transcription kinetics at coding sequences during Candida albicans morphogenesis. PLoS Genet. 8: e1003118. http://dx. doi. org/10. 1371/journal. pgen. 1003118.
24. Hnisz D, Majer O, Frohner IE, Komnenovic V, Kuchler K. 2010. The Set3/Hos2 histone deacetylase complex attenuates cAMP/PKA signaling to regulate morphogenesis and virulence of Candida albicans. PLoS Pathog. 6: e1000889. http://dx. doi. org/10. 1371/journal. ppat. 1000889.
25. Lopes da Rosa J, Boyartchuk VL, Zhu LJ, Kaufman PD. 2010. Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 107: 1594-1599. http://dx. doi. org/10. 1073/pnas. 0912427107.
26. Raman SB, Nguyen MH, Zhang Z, Cheng S, Jia HY, Weisner N, Iczkowski K, Clancy CJ. 2006. Candida albicans SET1 encodes a histone 3 lysine 4 methyltransferase that contributes to the pathogenesis of invasive candidiasis. Mol. Microbiol. 60: 697-709. http://dx. doi. org/10. 1111/j. 1365-2958. 2006. 05121. x.
27. Pijnappel WW, Schaft D, Roguev A, Shevchenko A, Tekotte H, Wilm M, Rigaut G, Séraphin B, Aasland R, Stewart AF. 2001. The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev. 15: 2991-3004. http://dx. doi. org/10. 1101/gad. 207401.
28. Homann OR, Dea J, Noble SM, Johnson AD. 2009. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5: e1000783. http://dx. doi. org/10. 1371/journal. pgen. 1000783.
29. Noble SM, French S, Kohn LA, Chen V, Johnson AD. 2010. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42: 590-598. http://dx. doi. org/10. 1038/ng. 605.
30. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2: e63. http://dx. doi. org/10. 1371/journal. ppat. 0020063.
31. Nett J, Andes D. 2006. Candida albicans biofilm development, modeling a host-pathogen interaction. Curr. Opin. Microbiol. 9: 340-345. http://dx. doi. org/10. 1016/j. mib. 2006. 06. 007.
32. Andes D, Nett J, Oschel P, Albrecht R, Marchillo K, Pitula A. 2004. Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect. Immun. 72: 6023-6031. http://dx. doi. org/10. 1128/IAI. 72. 10. 6023-6031. 2004.
33. Singh SD, Robbins N, Zaas AK, Schell WA, Perfect JR, Cowen LE. 2009. Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog. 5: e1000532. http://dx. doi. org/10. 1371/journal. ppat. 1000532.
34. Breeuwer P, Drocourt JL, Bunschoten N, Zwietering MH, Rombouts FM, Abee T. 1995. Characterization of uptake and hydrolysis of fluorescein diacetate and carboxyfluorescein diacetate by intracellular esterases in Saccharomyces cerevisiae, which result in accumulation of fluorescent product. Appl. Environ. Microbiol. 61: 1614-1619.
35. Nett J, Lincoln L, Marchillo K, Massey R, Holoyda K, Hoff B, Van-Handel M, Andes D. 2007. Putative role of beta-1, 3-glucans in Candida albicans biofilm resistance. Antimicrob. Agents Chemother. 51: 510-520. http://dx. doi. org/10. 1128/AAC. 01056-06.
36. Kaplan JB. 2010. Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J. Dent. Res. 89: 205-218. http://dx. doi. org/10. 1177/0022034509359403.
37. Karatan E, Watnick P. 2009. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol. Mol. Biol. Rev. 73: 310-347. http://dx. doi. org/10. 1128/MMBR. 00041-08.
38. Kim SM, Park JH, Lee HS, Kim WB, Ryu JM, Han HJ, Choi SH. 2013. LuxR homologue SmcR is essential for Vibrio vulnificus pathogenesis and biofilm detachment, and its expression is induced by host cells. Infect. Immun. 81: 3721-3730. http://dx. doi. org/10. 1128/IAI. 00561-13.
39. Connolly KL, Braden AK, Holder RC, Reid SD. 2011. Srv mediated dispersal of streptococcal biofilms through SpeB is observed in CovRS s t r a i n s. PLoS One 6: e28640. http://dx. doi. org/10. 1371/journal. pone. 0028640.
40. Connolly KL, Roberts AL, Holder RC, Reid SD. 2011. Dispersal of group A streptococcal biofilms by the cysteine protease SpeB leads to increased disease severity in a murine model. PLoS One 6: e18984. http://dx. doi. org/10. 1371/journal. pone. 0018984.
41. Bieber D, Ramer SW, Wu CY, Murray WJ, Tobe T, Fernandez R, Schoolnik GK. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280: 2114-2118. http://dx. doi. org/10. 1126/science. 280. 5372. 2114.
42. Murad AM, Leng P, Straffon M, Wishart J, Macaskill S, MacCallum D, Schnell N, Talibi D, Marechal D, Tekaia F, d'Enfert C, Gaillardin C, Odds FC, Brown AJ. 2001. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20: 4742-4752. http://dx. doi. org/10. 1093/emboj/20. 17. 4742.
43. Wightman R, Bates S, Amornrrattanapan P, Sudbery P. 2004. In Can-dida albicans, the Nim1 kinases Gin4 and Hsl1 negatively regulate pseudohypha formation and Gin4 also controls septin organization. J. Cell Biol. 164: 581-591. http://dx. doi. org/10. 1083/jcb. 200307176.
44. Sinha I, Wang YM, Philp R, Li CR, Yap WH, Wang Y. 2007. Cyclindependent kinases control septin phosphorylation in Candida albicans hyphal development. Dev. Cell 13: 421-432. http://dx. doi. org/10. 1016/j. devcel. 2007. 06. 011.
45. Clarke DJ, Giménez-Abián JF. 2000. Checkpoints controlling mitosis. Bioessays 22: 351-363. http://dx. doi. org/10. 1002/(SICI)1521-1878(200004)22: 4_351:: AID-BIES5 3. 0. CO; 2-W.
46. González-Novo A, Correa-Bordes J, Labrador L, Sánchez M, Vázquez de Aldana CR, Jiménez J. 2008. Sep7 is essential to modify septin ring dynamics and inhibit cell separation during Candida albicans hyphal growth. Mol. Biol. Cell 19: 1509-1518. http://dx. doi. org/10. 1091/mbc. E07-09-0876.
47. Whiteway M, Dignard D, Thomas DY. 1992. Dominant negative selection of heterologous genes: isolation of Candida albicans genes that interfere with Saccharomyces cerevisiae mating factor-induced cell cycle arrest. Proc. Natl. Acad. Sci. U. S. A. 89: 9410-9414. http://dx. doi. org/10. 1073/pnas. 89. 20. 9410.
48. Côte P, Hogues H, Whiteway M. 2009. Transcriptional analysis of the Candida albicans cell cycle. Mol. Biol. Cell 20: 3363-3373. http://dx. doi. org/10. 1091/mbc. E09-03-0210.
49. Simonetti G, Passariello C, Rotili D, Mai A, Garaci E, Palamara AT. 2007. Histone deacetylase inhibitors may reduce pathogenicity and virulence in Candida albicans. FEMS Yeast Res. 7: 1371-1380. http://dx. doi. org/10. 1111/j. 1567-1364. 2007. 00276. x.
50. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, Noble SM. 2008. Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135: 174-188. http://dx. doi. org/10. 1016/j. cell. 2008. 07. 046.
51. Liu H, Köhler J, Fink GR. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726. http://dx. doi. org/10. 1126/science. 7992058.
52. Jin Y, Yip HK, Samaranayake YH, Yau JY, Samaranayake LP. 2003. Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage in cases of human immunodeficiency virus infection. J. Clin. Microbiol. 41: 2961-2967. http://dx. doi. org/10. 1128/JCM. 41. 7. 2961-2967. 2003.
53. Nett JE, Cain MT, Crawford K, Andes DR. 2011. Optimizing a Candida biofilm microtiter plate model for measurement of antifungal susceptibility by tetrazolium salt assay. J. Clin. Microbiol. 49: 1426-1433. http://dx. doi. org/10. 1128/JCM. 02273-10.
54. Taff HT, Nett JE, Andes DR. 2012. Comparative analysis of Candida biofilm quantitation assays. Med. Mycol. 50: 214-218. http://dx. doi. org/10. 3109/13693786. 2011. 580016.
55. Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, Nantel A, Andes DR, Johnson AD, Mitchell AP. 2009. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol. 7: e1000133. http://dx. doi. org/10. 1371/journal. pbio. 1000133.