Eaf5/7/3 form a functionally independent NuA4 submodule linked to RNA polymerase II-coupled nucleosome recycling

EMBO Journal

Volumn 33, Issue 12, 2014, Pages 1397-1415

  Rossetto, Dorine ^a   Cramet, Myriam ^a   Wang, Alice Y ^b,d   Steunou, Anne Lise ^a   Lacoste, Nicolas ^a,c   Schulze, Julia M ^b,e   Côté, Valérie ^a   Monnet Saksouk, Julie ^a   Piquet, Sandra ^a   Nourani, Amine ^a   Kobor, Michael S ^b   Côté, Jacques ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c INSTITUT CURIE   (France)

^d UNIVERSITY OF CALGARY   (Canada)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

histone acetylation; NuA4; nucleosome dynamics; transcription elongation

Indexed keywords

CHAPERONE; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE NUA4; HISTONE DEACETYLASE; HISTONE H3; HISTONE H3K36; HISTONE METHYLTRANSFERASE; PROTEIN; PROTEIN EAF 3; PROTEIN EAF 5; PROTEIN EAF 7; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL MUTANT; CHROMATIN; CONTROLLED STUDY; DELETION MUTANT; ENZYME PHOSPHORYLATION; FRACTIONATION; GENE ACTIVATION; GENE EXPRESSION; GENE INTERACTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; LETHALITY; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOSOME; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION; TATA BOX; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; YEAST CELL;

HISTONE ACETYLATION; NUA4; NUCLEOSOME DYNAMICS; TRANSCRIPTION ELONGATION;

ACETYLTRANSFERASES; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, FUNGAL; HISTONE ACETYLTRANSFERASES; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; NUCLEOSOMES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84903268527     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201386433     Document Type: Article

References (99)

1. Albulescu LO, Sabet N, Gudipati M, Stepankiw N, Bergman ZJ, Huffaker TC, Pleiss JA, (2012) A quantitative, high-throughput reverse genetic screen reveals novel connections between Pre-mRNA splicing and 5' and 3' end transcript determinants. PLoS Genet 8: e1002530
2. Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, Pillus L, Workman JL, Cote J, (1999) NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 18: 5108-5119
3. Altaf M, Auger A, Covic M, Cote J, (2009) Connection between histone H2A variants and chromatin remodeling complexes. Biochem Cell Biol 87: 35-50
4. Altaf M, Auger A, Monnet-Saksouk J, Brodeur J, Piquet S, Cramet M, Bouchard N, Lacoste N, Utley RT, Gaudreau L, Cote J, (2010) NuA4-dependent acetylation of nucleosomal histones H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex. J Biol Chem 285: 15966-15977
5. Auger A, Galarneau L, Altaf M, Nourani A, Doyon Y, Utley RT, Cronier D, Allard S, Cote J, (2008) Eaf1 is the platform for NuA4 molecular assembly that evolutionarily links chromatin acetylation to ATP-dependent exchange of histone H2A variants. Mol Cell Biol 28: 2257-2270
6. Avvakumov N, Nourani A, Cote J, (2011) Histone chaperones: modulators of chromatin marks. Mol Cell 41: 502-514
7. Avvakumov N, Lalonde ME, Saksouk N, Paquet E, Glass KC, Landry AJ, Doyon Y, Cayrou C, Robitaille GA, Richard DE, Yang XJ, Kutateladze TG, Cote J, (2012) Conserved molecular interactions within the HBO1 acetyltransferase complexes regulate cell proliferation. Mol Cell Biol 32: 689-703
8. Babiarz JE, Halley JE, Rine J, (2006) Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev 20: 700-710
9. Bandyopadhyay S, Mehta M, Kuo D, Sung MK, Chuang R, Jaehnig EJ, Bodenmiller B, Licon K, Copeland W, Shales M, Fiedler D, Dutkowski J, Guenole A, van Attikum H, Shokat KM, Kolodner RD, Huh WK, Aebersold R, Keogh MC, Krogan NJ, et al, (2010) Rewiring of genetic networks in response to DNA damage. Science 330: 1385-1389
10. Bannister AJ, Kouzarides T, (2011) Regulation of chromatin by histone modifications. Cell Res 21: 381-395
11. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF, (2002) Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419: 411-415
12. Biswas D, Takahata S, Stillman DJ, (2008) Different genetic functions for the Rpd3(L) and Rpd3(S) complexes suggest competition between NuA4 and Rpd3(S). Mol Cell Biol 28: 4445-4458
13. Boudreault AA, Cronier D, Selleck W, Lacoste N, Utley RT, Allard S, Savard J, Lane WS, Tan S, Cote J, (2003) Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin. Genes Dev 17: 1415-1428
14. Brown CE, Howe L, Sousa K, Alley SC, Carrozza MJ, Tan S, Workman JL, (2001) Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science 292: 2333-2337
15. Cai Y, Jin J, Tomomori-Sato C, Sato S, Sorokina I, Parmely TJ, Conaway RC, Conaway JW, (2003) Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex. J Biol Chem 278: 42733-42736
16. Carey M, Li B, Workman JL, (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24: 481-487
17. Carroll KL, Pradhan DA, Granek JA, Clarke ND, Corden JL, (2004) Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol Cell Biol 24: 6241-6252
18. 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
19. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR, Winston F, (2008) Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6: e277
20. Choy JS, Kron SJ, (2002) NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol Cell Biol 22: 8215-8225
21. Clarke AS, Lowell JE, Jacobson SJ, Pillus L, (1999) Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol Cell Biol 19: 2515-2526
22. Downs JA, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, Bouchard N, Kron SJ, Jackson SP, Cote J, (2004) Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 16: 979-990
23. Doyon Y, Cote J, (2004) The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev 14: 147-154
24. Doyon Y, Selleck W, Lane WS, Tan S, Cote J, (2004) Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol 24: 1884-1896
25. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, Lane WS, Tan S, Yang XJ, Cote J, (2006) ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 21: 51-64
26. Drouin S, Laramee L, Jacques PE, Forest A, Bergeron M, Robert F, (2010) DSIF and RNA polymerase II CTD phosphorylation coordinate the recruitment of Rpd3S to actively transcribed genes. PLoS Genet 6: e1001173
27. Durant M, Pugh BF, (2007) NuA4-directed chromatin transactions throughout the Saccharomyces cerevisiae genome. Mol Cell Biol 27: 5327-5335
28. Eisen A, Utley RT, Nourani A, Allard S, Schmidt P, Lane WS, Lucchesi JC, Cote J, (2001) The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation. J Biol Chem 276: 3484-3491
29. Friis RM, Wu BP, Reinke SN, Hockman DJ, Sykes BD, Schultz MC, (2009) A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Res 37: 3969-3980
30. Galarneau L, Nourani A, Boudreault AA, Zhang Y, Heliot L, Allard S, Savard J, Lane WS, Stillman DJ, Cote J, (2000) Multiple links between the NuA4 histone acetyltransferase complex and epigenetic control of transcription. Mol Cell 5: 927-937
31. Ginsburg DS, Govind CK, Hinnebusch AG, (2009) NuA4 lysine acetyltransferase Esa1 is targeted to coding regions and stimulates transcription elongation with Gcn5. Mol Cell Biol 29: 6473-6487
32. Govind CK, Qiu H, Ginsburg DS, Ruan C, Hofmeyer K, Hu C, Swaminathan V, Workman JL, Li B, Hinnebusch AG, (2010) Phosphorylated Pol II CTD recruits multiple HDACs, including Rpd3C(S), for methylation-dependent deacetylation of ORF nucleosomes. Mol Cell 39: 234-246
33. Gowher H, Brick K, Camerini-Otero RD, Felsenfeld G, (2012) Vezf1 protein binding sites genome-wide are associated with pausing of elongating RNA polymerase II. Proc Natl Acad Sci USA 109: 2370-2375
34. Hentrich T, Schulze JM, Emberly E, Kobor MS, (2012) CHROMATRA: a Galaxy tool for visualizing genome-wide chromatin signatures. Bioinformatics 28: 717-718
35. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA, (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717-728
36. Jamai A, Puglisi A, Strubin M, (2009) Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol Cell 35: 377-383
37. Joo YJ, Kim JH, Kang UB, Yu MH, Kim J, (2011) Gcn4p-mediated transcriptional repression of ribosomal protein genes under amino-acid starvation. EMBO J 30: 859-872
38. Joshi AA, Struhl K, (2005) Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol Cell 20: 971-978
39. 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
40. Keogh MC, Mennella TA, Sawa C, Berthelet S, Krogan NJ, Wolek A, Podolny V, Carpenter LR, Greenblatt JF, Baetz K, Buratowski S, (2006) The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev 20: 660-665
41. 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
42. Kirkwood KJ, Ahmad Y, Larance M, Lamond AI, (2013) Characterization of Native Protein Complexes and Protein Isoform Variation Using Size-fractionation-based Quantitative Proteomics. Mol Cell Proteomics 12: 3851-3873
43. Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL, Link AJ, Madhani HD, Rine J, (2004) A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2: E131
44. Krogan NJ, Keogh MC, Datta N, Sawa C, Ryan OW, Ding H, Haw RA, Pootoolal J, Tong A, Canadien V, Richards DP, Wu X, Emili A, Hughes TR, Buratowski S, Greenblatt JF, (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12: 1565-1576
45. Krogan NJ, Baetz K, Keogh MC, Datta N, Sawa C, Kwok TC, Thompson NJ, Davey MG, Pootoolal J, Hughes TR, Emili A, Buratowski S, Hieter P, Greenblatt JF, (2004) Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc Natl Acad Sci USA 101: 13513-13518
46. Le Masson I, Yu DY, Jensen K, Chevalier A, Courbeyrette R, Boulard Y, Smith MM, Mann C, (2003) Yaf9, a novel NuA4 histone acetyltransferase subunit, is required for the cellular response to spindle stress in yeast. Mol Cell Biol 23: 6086-6102
47. Li B, Carey M, Workman JL, (2007a) The role of chromatin during transcription. Cell 128: 707-719
48. Li B, Gogol M, Carey M, Lee D, Seidel C, Workman JL, (2007b) Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316: 1050-1054
49. Li B, Gogol M, Carey M, Pattenden SG, Seidel C, Workman JL, (2007c) Infrequently transcribed long genes depend on the Set2/Rpd3S pathway for accurate transcription. Genes Dev 21: 1422-1430
50. Lin YY, Qi Y, Lu JY, Pan X, Yuan DS, Zhao Y, Bader JS, Boeke JD, (2008) A comprehensive synthetic genetic interaction network governing yeast histone acetylation and deacetylation. Genes Dev 22: 2062-2074
51. Lin YY, Lu JY, Zhang J, Walter W, Dang W, Wan J, Tao SC, Qian J, Zhao Y, Boeke JD, Berger SL, Zhu H, (2009) Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136: 1073-1084
52. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR, (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961
53. Lu JY, Lin YY, Sheu JC, Wu JT, Lee FJ, Chen Y, Lin MI, Chiang FT, Tai TY, Berger SL, Zhao Y, Tsai KS, Zhu H, Chuang LM, Boeke JD, (2011) Acetylation of yeast AMPK controls intrinsic aging independently of caloric restriction. Cell 146: 969-979
54. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T, (2011) Epigenetics in alternative pre-mRNA splicing. Cell 144: 16-26
55. Marston AL, Tham WH, Shah H, Amon A, (2004) A genome-wide screen identifies genes required for centromeric cohesion. Science 303: 1367-1370
56. Mason PB, Struhl K, (2005) Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol Cell 17: 831-840
57. Millar CB, Xu F, Zhang K, Grunstein M, (2006) Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev 20: 711-722
58. Mitchell L, Lambert JP, Gerdes M, Al-Madhoun AS, Skerjanc IS, Figeys D, Baetz K, (2008) Functional dissection of the NuA4 histone acetyltransferase reveals its role as a genetic hub and that Eaf1 is essential for complex integrity. Mol Cell Biol 28: 2244-2256
59. Mitchell L, Lau A, Lambert JP, Zhou H, Fong Y, Couture JF, Figeys D, Baetz K, (2011) Regulation of septin dynamics by the Saccharomyces cerevisiae lysine acetyltransferase NuA4. PLoS ONE 6: e25336
60. Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C, (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303: 343-348
61. Morillon A, Karabetsou N, Nair A, Mellor J, (2005) Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 18: 723-734
62. Musselman CA, Lalonde ME, Cote J, Kutateladze TG, (2012) Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 19: 1218-1227
63. Nourani A, Doyon Y, Utley RT, Allard S, Lane WS, Cote J, (2001) Role of an ING1 growth regulator in transcriptional activation and targeted histone acetylation by the NuA4 complex. Mol Cell Biol 21: 7629-7640
64. Nourani A, Utley RT, Allard S, Cote J, (2004) Recruitment of the NuA4 complex poises the PHO5 promoter for chromatin remodeling and activation. EMBO J 23: 2597-2607
65. Nourani A, Robert F, Winston F, (2006) Evidence that Spt2/Sin1, an HMG-like factor, plays roles in transcription elongation, chromatin structure, and genome stability in Saccharomyces cerevisiae. Mol Cell Biol 26: 1496-1509
66. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA, (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527
67. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Seraphin B, (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229
68. Reid JL, Iyer VR, Brown PO, Struhl K, (2000) Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase. Mol Cell 6: 1297-1307
69. Reid JL, Moqtaderi Z, Struhl K, (2004) Eaf3 regulates the global pattern of histone acetylation in Saccharomyces cerevisiae. Mol Cell Biol 24: 757-764
70. Reines D, (2003) Use of RNA yeast polymerase II mutants in studying transcription elongation. Methods Enzymol 371: 284-292
71. Riles L, Shaw RJ, Johnston M, Reines D, (2004) Large-scale screening of yeast mutants for sensitivity to the IMP dehydrogenase inhibitor 6-azauracil. Yeast 21: 241-248
72. 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
73. Rohde JR, Cardenas ME, (2003) The tor pathway regulates gene expression by linking nutrient sensing to histone acetylation. Mol Cell Biol 23: 629-635
74. Rufiange A, Jacques PE, Bhat W, Robert F, Nourani A, (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27: 393-405
75. Santisteban MS, Hang M, Smith MM, (2011) Histone variant H2A.Z and RNA polymerase II transcription elongation. Mol Cell Biol 31: 1848-1860
76. Schulze JM, Jackson J, Nakanishi S, Gardner JM, Hentrich T, Haug J, Johnston M, Jaspersen SL, Kobor MS, Shilatifard A, (2009) Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol Cell 35: 626-641
77. Schulze JM, Hentrich T, Nakanishi S, Gupta A, Emberly E, Shilatifard A, Kobor MS, (2011) Splitting the task: Ubp8 and Ubp10 deubiquitinate different cellular pools of H2BK123. Genes Dev 25: 2242-2247
78. Shen X, Mizuguchi G, Hamiche A, Wu C, (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406: 541-544
79. Shilatifard A, (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269
80. Smith ER, Eisen A, Gu W, Sattah M, Pannuti A, Zhou J, Cook RG, Lucchesi JC, Allis CD, (1998) ESA1 is a histone acetyltransferase that is essential for growth in yeast. Proc Natl Acad Sci USA 95: 3561-3565
81. Smolle M, Workman JL, Venkatesh S, (2013) reSETting chromatin during transcription elongation. Epigenetics 8: 10-15.
82. Suganuma T, Workman JL, (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80: 473-499
83. Sun B, Hong J, Zhang P, Dong X, Shen X, Lin D, Ding J, (2008) Molecular basis of the interaction of Saccharomyces cerevisiae Eaf3 chromo domain with methylated H3K36. J Biol Chem 283: 36504-36512
84. Synowsky SA, van Wijk M, Raijmakers R, Heck AJ, (2009) Comparative multiplexed mass spectrometric analyses of endogenously expressed yeast nuclear and cytoplasmic exosomes. J Mol Biol 385: 1300-1313
85. Teem JL, Rosbash M, (1983) Expression of a beta-galactosidase gene containing the ribosomal protein 51 intron is sensitive to the rna2 mutation of yeast. Proc Natl Acad Sci USA 80: 4403-4407
86. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, Andrews B, Tyers M, Boone C, (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368
87. Uprety B, Lahudkar S, Malik S, Bhaumik SR, (2012) The 19S proteasome subcomplex promotes the targeting of NuA4 HAT to the promoters of ribosomal protein genes to facilitate the recruitment of TFIID for transcriptional initiation in vivo. Nucleic Acids Res 40: 1969-1983
88. Utley RT, Ikeda K, Grant PA, Cote J, Steger DJ, Eberharter A, John S, Workman JL, (1998) Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394: 498-502
89. Utley RT, Lacoste N, Jobin-Robitaille O, Allard S, Cote J, (2005) Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol Cell Biol 25: 8179-8190
90. Venkatesh S, Smolle M, Li H, Gogol MM, Saint M, Kumar S, Natarajan K, Workman JL, (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489: 452-455
91. Venters BJ, Wachi S, Mavrich TN, Andersen BE, Jena P, Sinnamon AJ, Jain P, Rolleri NS, Jiang C, Hemeryck-Walsh C, Pugh BF, (2011) A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 41: 480-492
92. Wilmes GM, Bergkessel M, Bandyopadhyay S, Shales M, Braberg H, Cagney G, Collins SR, Whitworth GB, Kress TL, Weissman JS, Ideker T, Guthrie C, Krogan NJ, (2008) A genetic interaction map of RNA-processing factors reveals links between Sem1/Dss1-containing complexes and mRNA export and splicing. Mol Cell 32: 735-746
93. Xiao T, Hall H, Kizer KO, Shibata Y, Hall MC, Borchers CH, Strahl BD, (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev 17: 654-663
94. Xu C, Cui G, Botuyan MV, Mer G, (2008) Structural basis for the recognition of methylated histone H3K36 by the Eaf3 subunit of histone deacetylase complex Rpd3S. Structure 16: 1740-1750
95. Yi C, Ma M, Ran L, Zheng J, Tong J, Zhu J, Ma C, Sun Y, Zhang S, Feng W, Zhu L, Le Y, Gong X, Yan X, Hong B, Jiang FJ, Xie Z, Miao D, Deng H, Yu L, (2012) Function and molecular mechanism of acetylation in autophagy regulation. Science 336: 474-477
96. Yun M, Wu J, Workman JL, Li B, (2011) Readers of histone modifications. Cell Res 21: 564-578
97. Zentner GE, Henikoff S, (2013) Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20: 259-266
98. Zhang H, Richardson DO, Roberts DN, Utley R, Erdjument-Bromage H, Tempst P, Cote J, Cairns BR, (2004) The Yaf9 component of the SWR1 and NuA4 complexes is required for proper gene expression, histone H4 acetylation, and Htz1 replacement near telomeres. Mol Cell Biol 24: 9424-9436
99. Zhou BO, Wang SS, Xu LX, Meng FL, Xuan YJ, Duan YM, Wang JY, Hu H, Dong X, Ding J, Zhou JQ, (2010) SWR1 complex poises heterochromatin boundaries for antisilencing activity propagation. Mol Cell Biol 30: 2391-2400