A novel histone deacetylase complex in the control of transcription and genome stability

Molecular and Cellular Biology

Volumn 34, Issue 18, 2014, Pages 3500-3514

  Zilio, Nicola ^a   Codlin, Sandra ^b   Vashisht, Ajay A ^c   Bitton, Danny A ^b   Head, Steven R ^a   Wohlschlegel, James A ^c   Bähler, Jürg ^b   Boddy, Michael N ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; LONG UNTRANSLATED RNA; MUG165 PROTEIN; NTS1 PROTEIN; NUCLEAR PROTEIN; PNG3 PROTEIN; PROTEIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TRANSCRIPTION FACTOR II; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ARTICLE; CHROMATIN; CONTROLLED STUDY; GENE EXPRESSION; GENOMIC INSTABILITY; MEIOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCHIZOSACCHAROMYCES POMBE; TELOMERE;

CELL CYCLE PROTEINS; CHROMATIN; CHROMOSOMES, FUNGAL; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; GENOMIC INSTABILITY; HISTONE DEACETYLASES; MEIOSIS; PHENOTYPE; RNA, FUNGAL; RNA, LONG NONCODING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84906070143     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00519-14     Document Type: Article

References (54)

1. Dawson MA, Kouzarides T. 2012. Cancer epigenetics: from mechanism to therapy. Cell 150:12-27. http://dx.doi.org/10.1016/j.cell.2012.06.013.
2. Haberland M, Montgomery RL, Olson EN. 2009. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10:32-42. http://dx.doi.org/10.1038/nrg2485.
3. Lee KK, Workman JL. 2007. Histone acetyltransferase complexes: one size doesn't fit all. Nat. Rev. Mol. Cell Biol. 8:284-295. http://dx.doi.org/10.1038/nrm2145.
4. Grewal SI, Bonaduce MJ, Klar AJ. 1998. Histone deacetylase homologs regulate epigenetic inheritance of transcriptional silencing and chromosome segregation in fission yeast. Genetics 150:563-576.
5. Nicolas E, Yamada T, Cam HP, Fitzgerald PC, Kobayashi R, Grewal SI. Distinct roles of HDAC complexes in promoter silencing, antisense suppression and DNA damage protection. Nat. Struct. Mol. Biol. 14:372-380. http://dx.doi.org/10.1038/nsmb1239.
6. Sinha I, Wiren M, Ekwall K. 2006. Genome-wide patterns of histone modifications in fission yeast. Chromosome Res. 14:95-105. http://dx.doi .org/10.1007/s10577-005-1023-4.
7. Grewal SI, Jia S. 2007. Heterochromatin revisited. Nat. Rev. Genet. 8:35-46. http://dx.doi.org/10.1038/nrg2008.
8. Cam HP, Noma K, Ebina H, Levin HL, Grewal SI. 2008. Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451:431-436. http://dx.doi.org/10.1038/nature06499.
9. Hansen KR, Burns G, Mata J, Volpe TA, Martienssen RA, Bahler J, Thon G. 2005. Global effects on gene expression in fission yeast by silencing and RNA interference machineries. Mol. Cell. Biol. 25:590-601. http://dx.doi.org/10.1128/MCB.25.2.590-601.2005.
10. Anderson HE, Kagansky A, Wardle J, Rappsilber J, Allshire RC, Whitehall SK. 2010. Silencing mediated by the Schizosaccharomyces pombe HIRA complex is dependent upon the Hpc2-like protein, Hip4. PLoS One 5:e13488. http://dx.doi.org/10.1371/journal.pone.0013488.
11. Anderson HE, Wardle J, Korkut SV, Murton HE, Lopez-Maury L, Bahler J, Whitehall SK. 2009. The fission yeast HIRA histone chaperone is required for promoter silencing and the suppression of cryptic antisense transcripts. Mol. Cell. Biol. 29:5158-5167. http://dx.doi.org/10.1128/MCB.00698-09.
12. Lorenz DR, Mikheyeva IV, Johansen P, Meyer L, Berg A, Grewal SI, Cam HP. 2012. CENP-B cooperates with Set1 in bidirectional transcriptional silencing and genome organization of retrotransposons. Mol. Cell. Biol. 32:4215-4225. http://dx.doi.org/10.1128/MCB.00395-12.
13. Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823. http://dx.doi.org/10.1016/0076-6879(91)94059-L.
14. Zilio N, Wehrkamp-Richter S, Boddy MN. 2012. A new versatile system for rapid control of gene expression in the fission yeast Schizosaccharomyces pombe. Yeast 29:425-434. http://dx.doi.org/10.1002/yea.2920.
15. Wohlschlegel JA. 2009. Identification of SUMO-conjugated proteins and their SUMO attachment sites using proteomic mass spectrometry. Methods Mol. Biol. 497:33-49. http://dx.doi.org/10.1007/978-1-59745-566 -4_3.
16. Florens L, Washburn MP. 2006. Proteomic analysis by multidimensional protein identification technology. Methods Mol. Biol. 328:159-175. http://dx.doi.org/10.1385/1-59745-026-X:159.
17. Eng JK, McCormack AL, Yates JR. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5:976-989. http://dx.doi .org/10.1016/1044-0305(94)80016-2.
18. Tabb DL, McDonald WH, Yates JR, III. 2002. DTASelect and contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 1:21-26. http://dx.doi.org/10.1021/pr015504q.
19. Cociorva D, D LT, Yates JR. 2007. Validation of tandem mass spectrometry database search results using DTASelect. Curr. Protoc. Bioinform. Chapter 13:Unit 13.14.
20. Elias JE, Gygi SP. 2007. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4:207-214. http://dx.doi.org/10.1038/nmeth1019.
21. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J. 2003. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell 14:214-229. http://dx.doi.org/10 .1091/mbc.E02-08-0499.
22. Lyne R, Burns G, Mata J, Penkett CJ, Rustici G, Chen D, Langford C, Vetrie D, Bahler J. 2003. Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4:27. http://dx.doi.org/10.1186/1471-2164-4-27.
23. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, Gordon L, Hourlier T, Hunt S, Johnson N, Juettemann T, Kahari AK, Keenan S, Kulesha E, Martin FJ, Maurel T, McLaren WM, Murphy DN, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, Ruffier M, Sheppard D, Taylor K, Thormann A, Trevanion SJ, Vullo A, Wilder SP, Wilson M, Zadissa A, Aken BL, Birney E, Cunningham F, Harrow J, Herrero J, Hubbard TJ, Kinsella R, Muffato M, Parker A, Spudich G, Yates A, Zerbino DR, Searle SM. 2014. Ensembl 2014. Nucleic Acids Res. 42:D749-D755. http://dx.doi.org/10.1093/nar/gkt1196.
24. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
25. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576-589. http://dx.doi .org/10.1016/j.molcel.2010.05.004.
26. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137. http://dx.doi.org/10 .1186/gb-2008-9-9-r137.
27. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A, III, Steever AB, Wach A, Philippsen P, Pringle JR. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943-951.
28. Pebernard S, Wohlschlegel J, McDonald WH, Yates JR, III, Boddy MN. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol. Cell. Biol. 26:1617-1630. http://dx.doi.org/10.1128/MCB .26.5.1617-1630.2006.
29. Shevchenko A, Roguev A, Schaft D, Buchanan L, Habermann B, Sakalar C, Thomas H, Krogan NJ, Shevchenko A, Stewart AF. 2008. Chromatin central: towards the comparative proteome by accurate mapping of the yeast proteomic environment. Genome Biol. 9:R167. http://dx.doi.org/10 .1186/gb-2008-9-11-r167.
30. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, Yang L, Wolting C, Donaldson I, Schandorff S, Shewnarane J, Vo M, Taggart J, Goudreault M, Muskat B, Alfarano C, Dewar D, Lin Z, Michalickova K, Willems AR, Sassi H, Nielsen PA, Rasmussen KJ, Andersen JR, Johansen LE, Hansen LH, Jespersen H, Podtelejnikov A, Nielsen E, Crawford J, Poulsen V, Sorensen BD, Matthiesen J, Hendrickson RC, Gleeson F, Pawson T, Moran MF, Durocher D, Mann M, Hogue CW, Figeys D, Tyers M. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183. http://dx.doi.org/10.1038/415180a.
31. Bowen NJ, Jordan IK, Epstein JA, Wood V, Levin HL. 2003. Retrotransposons and their recognition of Pol II promoters: a comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. Genome Res. 13:1984-1997. http://dx.doi .org/10.1101/gr.1191603.
32. Kim HS, Vanoosthuyse V, Fillingham J, Roguev A, Watt S, Kislinger T, Treyer A, Carpenter LR, Bennett CS, Emili A, Greenblatt JF, Hardwick KG, Krogan NJ, Bahler J, Keogh MC. 2009. An acetylated form of histone H2A.Z regulates chromosome architecture in Schizosaccharomyces pombe. Nat. Struct. Mol. Biol. 16:1286-1293. http://dx.doi.org/10.1038/nsmb .1688.
33. Helmlinger D, Marguerat S, Villen J, Gygi SP, Bahler J, Winston F. The S. pombe SAGA complex controls the switch from proliferation to sexual differentiation through the opposing roles of its subunits Gcn5 and Spt8. Genes Dev. 22:3184-3195. http://dx.doi.org/10.1101/gad .1719908.
34. Kurdistani SK, Robyr D, Tavazoie S, Grunstein M. 2002. Genome-wide binding map of the histone deacetylase Rpd3 in yeast. Nat. Genet. 31:248-254. http://dx.doi.org/10.1038/ng907.
35. Robert F, Pokholok DK, Hannett NM, Rinaldi NJ, Chandy M, Rolfe A, Workman JL, Gifford DK, Young RA. 2004. Global position and recruitment of HATs and HDACs in the yeast genome. Mol. Cell 16:199-209. http://dx.doi.org/10.1016/j.molcel.2004.09.021.
36. Chen D, Wilkinson CR, Watt S, Penkett CJ, Toone WM, Jones N, Bahler J. 2008. Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol. Biol. Cell 19:308-317. http://dx.doi .org/10.1091/mbc.E07-08-0735.
37. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, Schubert F, Preiss T, Bahler J. 2007. A network of multiple regulatory layers shapes gene expression in fission yeast. Mol. Cell 26:145-155. http://dx.doi.org/10.1016/j.molcel.2007.03.002.
38. Marguerat S, Jensen TS, de Lichtenberg U, Wilhelm BT, Jensen LJ, Bahler J. 2006. The more the merrier: comparative analysis of microarray studies on cell cycle-regulated genes in fission yeast. Yeast 23:261-277. http://dx.doi.org/10.1002/yea.1351.
39. Mata J, Wilbrey A, Bahler J. 2007. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 8:R217. http://dx.doi .org/10.1186/gb-2007-8-10-r217.
40. McDonald WH, Pavlova Y, Yates JR, III, Boddy MN. 2003. Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J. Biol. Chem. 278:45460-45467. http://dx .doi.org/10.1074/jbc.M308828200.
41. Alper BJ, Job G, Yadav RK, Shanker S, Lowe BR, Partridge JF. 2013. Sir2 is required for Clr4 to initiate centromeric heterochromatin assembly in fission yeast. EMBO J. 32:2321-2335. http://dx.doi.org/10.1038/emboj .2013.143.
42. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ. 2005. Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593-605. http://dx.doi.org/10.1016/j.cell.2005.10.025.
43. Carrozza MJ, Florens L, Swanson SK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL. 2005. Stable incorporation of sequence specific repressors Ash1 and Ume6 into the Rpd3L complex. Biochim. Biophys. Acta 1731:77-87, discussion 75-76. http://dx.doi.org/10.1016/j .bbaexp.2005.09.005.
44. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581-592. http://dx .doi.org/10.1016/j.cell.2005.10.023.
45. Mata J, Lyne R, Burns G, Bahler J. 2002. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32:143-147. http://dx .doi.org/10.1038/ng951.
46. Voth WP, Yu Y, Takahata S, Kretschmann KL, Lieb JD, Parker RL, Milash B, Stillman DJ. 2007. Forkhead proteins control the outcome of transcription factor binding by antiactivation. EMBO J. 26:4324-4334. http://dx.doi.org/10.1038/sj.emboj.7601859.
47. Teytelman L, Thurtle DM, Rine J, van Oudenaarden A. 2013. Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc. Natl. Acad. Sci. U. S. A. 110:18602-18607. http://dx.doi.org/10.1073/pnas.1316064110.
48. Liang J, Lacroix L, Gamot A, Cuddapah S, Queille S, Lhoumaud P, Lepetit P, Martin PG, Vogelmann J, Court F, Hennion M, Micas G, Urbach S, Bouchez O, Nollmann M, Zhao K, Emberly E, Cuvier O. Chromatin immunoprecipitation indirect peaks highlight longrange interactions of insulator proteins and Pol II pausing. Mol. Cell 53: 672-681. http://dx.doi.org/10.1016/j.molcel.2013.12.029.
49. Knott SR, Peace JM, Ostrow AZ, Gan Y, Rex AE, Viggiani CJ, Tavare S, Aparicio OM. 2012. Forkhead transcription factors establish origin timing and long-range clustering in S. cerevisiae. Cell 148:99-111. http://dx .doi.org/10.1016/j.cell.2011.12.012.
50. Chen HM, Rosebrock AP, Khan SR, Futcher B, Leatherwood JK. 2012. Repression of meiotic genes by antisense transcription and by Fkh2 transcription factor in Schizosaccharomyces pombe. PLoS One 7:e29917. http://dx.doi.org/10.1371/journal.pone.0029917.
51. Zaratiegui M, Castel SE, Irvine DV, Kloc A, Ren J, Li F, de Castro E, Marin L, Chang AY, Goto D, Cande WZ, Antequera F, Arcangioli B, Martienssen RA. 2011. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 479:135-138. http://dx.doi.org/10.1038/nature10501.
52. Pebernard S, McDonald WH, Pavlova Y, Yates JR, III, Boddy MN. Nse1, Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a crucial role in meiosis. Mol. Biol. Cell 15:4866-4876. http://dx.doi .org/10.1091/mbc.E04-05-0436.
53. Lee SY, Rozenzhak S, Russell P. 2013. gammaH2A-binding protein Brc1 affects centromere function in fission yeast. Mol. Cell. Biol. 33:1410-1416. http://dx.doi.org/10.1128/MCB.01654-12.
54. Heichinger C, Penkett CJ, Bahler J, Nurse P. 2006. Genome-wide characterization of fission yeast DNA replication origins. EMBO J. 25: 5171-5179. http://dx.doi.org/10.1038/sj.emboj.7601390.