A Histone Deacetylase Adjusts Transcription Kinetics at Coding Sequences during Candida albicans Morphogenesis

PLoS Genetics

Volumn 8, Issue 12, 2012, Pages

  Hnisz, Denes ^a   Bardet, Anaïs F ^b   Nobile, Clarissa J ^c   Petryshyn, Andriy ^a   Glaser, Walter ^a   Schöck, Ulrike ^d,e   Stark, Alexander ^b   Kuchler, Karl ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GATC Biotech AG   (Germany)

^e MLL MUNICH LEUKEMIA LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE; SET3 COMPLEX; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BRG1; TRANSCRIPTION FACTOR EFG1; TRANSCRIPTION FACTOR NRG1; TRANSCRIPTION FACTOR TEC1; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FUNGAL STRUCTURES; FUNGUS GROWTH; FUNGUS HYPHAE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLYCOLYSIS; MORPHOGENESIS; NONHUMAN; RNA SEQUENCE;

CANDIDA ALBICANS; CHROMATIN; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; HYPHAE; KINETICS; MORPHOGENESIS; OPEN READING FRAMES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

CANDIDA ALBICANS;

EID: 84872007065     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003118     Document Type: Article

References (50)

1. Sudbery P, Gow N, Berman J, (2004) The distinct morphogenic states of Candida albicans. Trends Microbiol 12: 317-324.
2. Thompson DS, Carlisle PL, Kadosh D, (2011) Coevolution of morphology and virulence in Candida species. Eukaryot Cell 10: 1173-1182.
3. Gow NA, Brown AJ, Odds FC, (2002) Fungal morphogenesis and host invasion. Curr Opin Microbiol 5: 366-371.
4. Saville SP, Lazzell AL, Bryant AP, Fretzen A, Monreal A, et al. (2006) Inhibition of filamentation can be used to treat disseminated candidiasis. Antimicrob Agents Chemother 50: 3312-3316.
5. Whiteway M, Bachewich C, (2007) Morphogenesis in Candida albicans. Annu Rev Microbiol 61: 529-553.
6. Shapiro RS, Robbins N, Cowen LE, (2011) Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol Mol Biol Rev 75: 213-267.
7. 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.
8. Homann OR, Dea J, Noble SM, Johnson AD, (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 5: e1000783.
9. Lu Y, Su C, Mao X, Raniga PP, Liu H, et al. (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.
10. Lu Y, Su C, Wang A, Liu H, (2011) Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance. PLoS Biol 9: e1001105.
11. Kadosh D, Johnson AD, (2005) Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol Biol Cell 16: 2903-2912.
12. 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.
13. Raman SB, Nguyen MH, Zhang Z, Cheng S, Jia HY, et al. (2006) Candida albicans SET1 encodes a histone 3 lysine 4 methyltransferase that contributes to the pathogenesis of invasive candidiasis. Mol Microbiol 60: 697-709.
14. 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.
15. 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.
16. Pijnappel WW, Schaft D, Roguev A, Shevchenko A, Tekotte H, et al. (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.
17. Wang A, Kurdistani SK, Grunstein M, (2002) Requirement of Hos2 histone deacetylase for gene activity in yeast. Science 298: 1412-1414.
18. Kim T, Buratowski S, (2009) Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5′ transcribed regions. Cell 137: 259-272.
19. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, et al. (2008) Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135: 174-188.
20. Ding SL, Liu W, Iliuk A, Ribot C, Vallet J, et al. (2010) The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2495-2508.
21. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.
22. Nantel A, Dignard D, Bachewich C, Harcus D, Marcil A, et al. (2002) Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell 13: 3452-3465.
23. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, et al. (2012) A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138.
24. Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, et al. (2009) Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7: e1000133.
25. Askew C, Sellam A, Epp E, Hogues H, Mullick A, et al. (2009) Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog 5: e1000612.
26. Lavoie H, Hogues H, Mallick J, Sellam A, Nantel A, et al. (2010) Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol 8: e1000329.
27. Lassak T, Schneider E, Bussmann M, Kurtz D, Manak JR, et al. (2011) Target specificity of the Candida albicans Efg1 regulator. Mol Microbiol 82: 602-618.
28. Uhl MA, Biery M, Craig N, Johnson AD, (2003) Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C.albicans. EMBO J 22: 2668-2678.
29. Mou Z, Kenny AE, Curcio MJ, (2006) Hos2 and Set3 promote integration of Ty1 retrotransposons at tRNA genes in Saccharomyces cerevisiae. Genetics 172: 2157-2167.
30. Lenstra TL, Benschop JJ, Kim T, Schulze JM, Brabers NA, et al. (2011) The specificity and topology of chromatin interaction pathways in yeast. Mol Cell 42: 536-549.
31. Weiner A, Chen HV, Liu CL, Rahat A, Klien A, et al. (2012) Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10: e1001369.
32. Lee JS, Smith E, Shilatifard A, (2010) The language of histone crosstalk. Cell 142: 682-685.
33. Henikoff S, Shilatifard A, (2011) Histone modification: cause or cog? Trends Genet 27: 389-396.
34. Alejandro-Osorio AL, Huebert DJ, Porcaro DT, Sonntag ME, Nillasithanukroh S, et al. (2009) The histone deacetylase Rpd3p is required for transient changes in genomic expression in response to stress. Genome Biol 10: R57.
35. Lohse MB, Johnson AD, (2010) Temporal anatomy of an epigenetic switch in cell programming: the white-opaque transition of C. albicans. Mol Microbiol 78: 331-343.
36. Sellam A, Hogues H, Askew C, Tebbji F, van Het Hoog M, et al. (2010) Experimental annotation of the human pathogen Candida albicans coding and noncoding transcribed regions using high-resolution tiling arrays. Genome Biol 11: R71.
37. Buratowski S, (2009) Progression through the RNA polymerase II CTD cycle. Mol Cell 36: 541-546.
38. Egloff S, Murphy S, (2008) Cracking the RNA polymerase II CTD code. Trends Genet 24: 280-288.
39. Egloff S, Dienstbier M, Murphy S, (2012) Updating the RNA polymerase CTD code: adding gene-specific layers. Trends Genet.
40. Kim T, Xu Z, Clauder-Münster S, Steinmetz L, Buratowski S, (2012) Set3 HDAC mediates effects of overlapping noncoding transcription on gene induction kinetics. Cell doi:10.1016/j.cell.2012.08.016.
41. Noble SM, Johnson AD, (2005) Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot Cell 4: 298-309.
42. Frohner IE, Bourgeois C, Yatsyk K, Majer O, Kuchler K, (2009) Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol Microbiol 71: 240-252.
43. Reuss O, Vik A, Kolter R, Morschhauser J, (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119-127.
44. Hernday AD, Noble SM, Mitrovich QM, Johnson AD, (2010) Genetics and molecular biology in Candida albicans. Methods Enzymol 470: 737-758.
45. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
46. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
47. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
48. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
49. Li H, Fischle W, Wang W, Duncan EM, Liang L, et al. (2007) Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger. Mol Cell 28: 677-691.
50. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.