A PWWP domain-containing protein targets the NuA3 acetyltransferase complex via histone H3 lysine 36 trimethylation to coordinate transcriptional elongation at coding regions

Molecular and Cellular Proteomics

Volumn 13, Issue 11, 2014, Pages 2883-2895

  Gilbert, Tonya M ^a   McDaniel, Stephen L ^b   Byrum, Stephanie D ^c   Cades, Jessica A ^a   Dancy, Blair C R ^a   Wade, Herschel ^a   Tackett, Alan J ^c   Strahl, Brian D ^b,d   Taverna, Sean D ^a,d  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE ACETYLTRANSFERASE NUA3; HISTONE ACETYLTRANSFERASE NUA3A; HISTONE ACETYLTRANSFERASE NUA3B; HISTONE H3; LYSINE; PDP3 PROTEIN; PROLINE; PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG; YNG1 PROTEIN; HISTONE; SACCHAROMYCES CEREVISIAE PROTEIN; SAS3 PROTEIN, S CEREVISIAE; YNG1 PROTEIN, S CEREVISIAE;

ARTICLE; BINDING ASSAY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENETIC ANALYSIS; HISTONE ACETYLATION; HISTONE METHYLATION; MASS SPECTROMETRY; NONHUMAN; OPEN READING FRAME; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TARGETING; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; ACETYLATION; AMINO ACID SEQUENCE; GENETICS; METABOLISM; METHYLATION; MOLECULAR GENETICS; PHYSIOLOGY; PLASMID; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; RNA TRANSLATION; SEQUENCE ALIGNMENT;

ACETYLATION; AMINO ACID SEQUENCE; ESCHERICHIA COLI; HISTONE ACETYLTRANSFERASES; HISTONES; MASS SPECTROMETRY; METHYLATION; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PLASMIDS; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 84910679960     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.038224     Document Type: Article

References (110)

1. Kulaeva, O. I., Gaykalova, D. A., Pestov, N. A., Golovastov, V. V., Vassylyev, D. G., Artsimovitch, I., and Studitsky, V. M. (2009) Mechanism of chromatin remodeling and recovery during passage of RNA polymerase II. Nat. Struct. Mol. Biol. 16, 1272-1278
2. Kulaeva, O. I., Hsieh, F. K., and Studitsky, V. M. (2010) RNA polymerase complexes cooperate to relieve the nucleosomal barrier and evict histones. Proc. Natl. Acad. Sci. U. S. A. 107, 11325-11330
3. Smolle, M., Workman, J. L., and Venkatesh, S. (2013) reSETting chromatin during transcription elongation. Epigenetics 8, 10-15
4. Gardner, K. E., Allis, C. D., and Strahl, B. D. (2011) Operating on chromatin, a colorful language where context matters. J. Mol. Biol. 409, 36-46
5. Petesch, S. J., and Lis, J. T. (2012) Overcoming the nucleosome barrier during transcript elongation. Trends Genet. 28, 285-294
6. Strahl, B. D., and Allis, C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45
7. Taverna, S. D., Li, H., Ruthenburg, A. J., Allis, C. D., and Patel, D. J. (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14, 1025-1040
8. Lee, J. S., and Shilatifard, A. (2007) A site to remember: H3K36 methylation a mark for histone deacetylation. Mutat. Res. 618, 130-134
9. Barrera, L. O., and Ren, B. (2006) The transcriptional regulatory code of eukaryotic cells-insights from genome-wide analysis of chromatin organization and transcription factor binding. Curr. Opin. Cell Biol. 18, 291-298
10. Fuchs, S. M., Laribee, R. N., and Strahl, B. D. (2009) Protein modifications in transcription elongation. Biochim. Biophys. Acta 1789, 26-36
11. Heyse, K. S., Weber, S. E., and Lipps, H. J. (2009) Histone modifications are specifically relocated during gene activation and nuclear differentiation. BMC Genomics 10, 554
12. Liang, G., Lin, J. C., Wei, V., Yoo, C., Cheng, J. C., Nguyen, C. T., Weisenberger, D. J., Egger, G., Takai, D., Gonzales, F. A., and Jones, P. A. (2004) Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc. Natl. Acad. Sci. U. S. A. 101, 7357-7362
13. Pokholok, D. K., Harbison, C. T., Levine, S., Cole, M., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, P. A., Herbolsheimer, E., Zeitlinger, J., Lewitter, F., Gifford, D. K., and Young, R. A. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517-527
14. Rando, O. J. (2007) Global patterns of histone modifications. Curr. Opin. Genet. Dev. 17, 94-99
15. Bian, C., Xu, C., Ruan, J., Lee, K. K., Burke, T. L., Tempel, W., Barsyte, D., Li, J., Wu, M., Zhou, B. O., Fleharty, B. E., Paulson, A., Allali-Hassani, A., Zhou, J. Q., Mer, G., Grant, P. A., Workman, J. L., Zang, J., and Min, J. (2011) Sgf29 binds histone H3K4me2/3 and is required for SAGA complex recruitment and histone H3 acetylation. EMBO J. 30, 2829-2842
16. Choy, J. S., Tobe, B. T., Huh, J. H., and Kron, S. J. (2001) Yng2p-dependent NuA4 histone H4 acetylation activity is required for mitotic and meiotic progression. J. Biol. Chem. 276, 43653-43662
17. Klein, B. J., Lalonde, M. E., Cote, J., Yang, X. J., and Kutateladze, T. G. (2013) Crosstalk between epigenetic readers regulates the MOZ/MORF HAT complexes. Epigenetics 9, 186-193
18. Li, B., Gogol, M., Carey, M., Lee, D., Seidel, C., and Workman, J. L. (2007) Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316, 1050-1054
19. Taverna, S. D., Ilin, S., Rogers, R. S., Tanny, J. C., Lavender, H., Li, H., Baker, L., Boyle, J., Blair, L. P., Chait, B. T., Patel, D. J., Aitchison, J. D., Tackett, A. J., and Allis, C. D. (2006) Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 24, 785-796
20. Vermeulen, M., Eberl, H. C., Matarese, F., Marks, H., Denissov, S., Butter, F., Lee, K. K., Olsen, J. V., Hyman, A. A., Stunnenberg, H. G., and Mann, M. (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142, 967-980
21. Eberharter, A., John, S., Grant, P. A., Utley, R. T., and Workman, J. L. (1998) Identification and analysis of yeast nucleosomal histone acetyltransferase complexes. Methods 15, 315-321
22. Briggs, S. D., Bryk, M., Strahl, B. D., Cheung, W. L., Davie, J. K., Dent, S. Y., Winston, F., and Allis, C. D. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15, 3286-3295
23. Doyon, Y., Cayrou, C., Ullah, M., Landry, A. J., Cote, V., Selleck, W., Lane, W. S., Tan, S., Yang, X. J., and Cote, J. (2006) ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 21, 51-64
24. Howe, L., Kusch, T., Muster, N., Chaterji, R., Yates, J. R., 3rd, and Workman, J. L. (2002) Yng1p modulates the activity of Sas3p as a component of the yeast NuA3 Hhistone acetyltransferase complex. Mol. Cell. Biol. 22, 5047-5053
25. John, S., Howe, L., Tafrov, S. T., Grant, P. A., Sternglanz, R., and Workman, J. L. (2000) The something about silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAF(II)30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev. 14, 1196-1208
26. Martin, D. G., Baetz, K., Shi, X., Walter, K. L., MacDonald, V. E., Wlodarski, M. J., Gozani, O., Hieter, P., and Howe, L. (2006) The Yng1p plant homeodomain finger is a methyl-histone binding module that recognizes lysine 4-methylated histone H3. Mol. Cell. Biol. 26, 7871-7879
27. Martin, D. G., Grimes, D. E., Baetz, K., and Howe, L. (2006) Methylation of histone H3 mediates the association of the NuA3 histone acetyltransferase with chromatin. Mol. Cell. Biol. 26, 3018-3028
28. Ishimi, Y., and Kikuchi, A. (1991) Identification and molecular cloning of yeast homolog of nucleosome assembly protein I, which facilitates nucleosome assembly in vitro. J. Biol. Chem. 266, 7025-7029
29. Park, Y. J., Chodaparambil, J. V., Bao, Y., McBryant, S. J., and Luger, K. (2005) Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J. Biol. Chem. 280, 1817-1825
30. Smart, S. K., Mackintosh, S. G., Edmondson, R. D., Taverna, S. D., and Tackett, A. J. (2009) Mapping the local protein interactome of the NuA3 histone acetyltransferase. Protein Sci. 18, 1987-1997
31. VanDemark, A. P., Xin, H., McCullough, L., Rawlins, R., Bentley, S., Heroux, A., Stillman, D. J., Hill, C. P., and Formosa, T. (2008) Structural and functional analysis of the Spt16p N-terminal domain reveals overlapping roles of yFACT subunits. J. Biol. Chem. 283, 5058-5068
32. Wagner, E. J., and Carpenter, P. B. (2012) Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell Biol. 13, 115-126
33. Strahl, B. D., Grant, P. A., Briggs, S. D., Sun, Z. W., Bone, J. R., Caldwell, J. A., Mollah, S., Cook, R. G., Shabanowitz, J., Hunt, D. F., and Allis, C. D. (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell. Biol. 22, 1298-1306
34. Kizer, K. O., Phatnani, H. P., Shibata, Y., Hall, H., Greenleaf, A. L., and Strahl, B. D. (2005) A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol. Cell. Biol. 25, 3305-3316
35. Krogan, N. J., Kim, M., Tong, A., Golshani, A., Cagney, G., Canadien, V., Richards, D. P., Beattie, B. K., Emili, A., Boone, C., Shilatifard, A., Buratowski, S., and Greenblatt, J. (2003) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23, 4207-4218
36. Li, J., Moazed, D., and Gygi, S. P. (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J. Biol. Chem. 277, 49383-49388
37. Schaft, D., Roguev, A., Kotovic, K. M., Shevchenko, A., Sarov, M., Shevchenko, A., Neugebauer, K. M., and Stewart, A. F. (2003) The histone 3 lysine 36 methyltransferase, SET2, is involved in transcriptional elongation. Nucleic Acids Res. 31, 2475-2482
38. Xiao, T., Hall, H., Kizer, K. O., Shibata, Y., Hall, M. C., Borchers, C. H., and Strahl, B. D. (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17, 654-663
39. Li, B., Howe, L., Anderson, S., Yates, J. R., 3rd, and Workman, J. L. (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 278, 8897-8903
40. Morris, S. A., Shibata, Y., Noma, K., Tsukamoto, Y., Warren, E., Temple, B., Grewal, S. I., and Strahl, B. D. (2005) Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryotic Cell 4, 1446-1454
41. Carrozza, M. J., Li, B., Florens, L., Suganuma, T., Swanson, S. K., Lee, K. K., Shia, W. J., Anderson, S., Yates, J., Washburn, M. P., and Workman, J. L. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123, 581-592
42. Huh, J. W., Wu, J., Lee, C. H., Yun, M., Gilada, D., Brautigam, C. A., and Li, B. (2012) Multivalent di-nucleosome recognition enables the Rpd3S histone deacetylase complex to tolerate decreased H3K36 methylation levels. EMBO J. 31, 3564-3574
43. Joshi, A. A., and Struhl, K. (2005) Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20, 971-978
44. Keogh, M. C., Kurdistani, S. K., Morris, S. A., Ahn, S. H., Podolny, V., Collins, S. R., Schuldiner, M., Chin, K., Punna, T., Thompson, N. J., Boone, C., Emili, A., Weissman, J. S., Hughes, T. R., Strahl, B. D., Grunstein, M., Greenblatt, J. F., Buratowski, S., and Krogan, N. J. (2005) Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123, 593-605
45. Li, B., Jackson, J., Simon, M. D., Fleharty, B., Gogol, M., Seidel, C., Workman, J. L., and Shilatifard, A. (2009) Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J. Biol. Chem. 284, 7970-7976
46. Sun, B., Hong, J., Zhang, P., Dong, X., Shen, X., Lin, D., and Ding, J. (2008) Molecular basis of the interaction of Saccharomyces cerevisiae Eaf3 chromo domain with methylated H3K36. J. Biol. Chem. 283, 36504-36512
47. Xu, C., Cui, G., Botuyan, MV., and 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
48. Li, B., Gogol, M., Carey, M., Pattenden, S. G., Seidel, C., and Workman, J. L. (2007) Infrequently transcribed long genes depend on the Set2/Rpd3S pathway for accurate transcription. Genes Dev. 21, 1422-1430
49. Lickwar, C. R., Rao, B., Shabalin, A. A., Nobel, A. B., Strahl, B. D., and Lieb, J. D. (2009) The Set2/Rpd3S pathway suppresses cryptic transcription without regard to gene length or transcription frequency. PloS One 4, e4886
50. Venkatesh, S., Smolle, M., Li, H., Gogol, M. M., Saint, M., Kumar, S., Natarajan, K., and Workman, J. L. (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489, 452-455
51. Maltby, V. E., Martin, B. J., Schulze, J. M., Johnson, I., Hentrich, T., Sharma, A., Kobor, M. S., and Howe, L. (2012) Histone H3 lysine 36 methylation targets the Isw1b remodeling complex to chromatin. Mol. Cell. Biol. 32, 3479-3485
52. Smolle, M., Venkatesh, S., Gogol, M. M., Li, H., Zhang, Y., Florens, L., Washburn, M. P., and Workman, J. L. (2012) Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19, 884-892
53. Lee, C. H., Wu, J., and Li, B. (2013) Chromatin remodelers fine-tune H3K36me-directed deacetylation of neighbor nucleosomes by Rpd3S. Mol. Cell 52, 255-263
54. Wu, H., Zeng, H., Lam, R., Tempel, W., Amaya, M. F., Xu, C., Dombrovski, L., Qiu, W., Wang, Y., and Min, J. (2011) Structural and histone binding ability characterizations of human PWWP domains. PloS One 6, e18919
55. Laue, K., Daujat, S., Crump, J. G., Plaster, N., Roehl, H. H., Tubingen Screen, C., Kimmel, C. B., Schneider, R., and Hammerschmidt, M. (2008) The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development 135, 1935-1946
56. Vezzoli, A., Bonadies, N., Allen, M. D., Freund, S. M., Santiveri, C. M., Kvinlaug, B. T., Huntly, B. J., Gottgens, B., and Bycroft, M. (2010) Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat. Struct. Mol. Biol. 17, 617-619
57. Dhayalan, A., Rajavelu, A., Rathert, P., Tamas, R., Jurkowska, R. Z., Ragozin, S., and Jeltsch, A. (2010) The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 285, 26114-26120
58. Pradeepa, M. M., Sutherland, H. G., Ule, J., Grimes, G. R., and Bickmore, W. A. (2012) Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. PLoS Genet. 8, e1002717
59. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P., Punna, T., Peregrin-Alvarez, J. M., Shales, M., Zhang, X., Davey, M., Robinson, M. D., Paccanaro, A., Bray, J. E., Sheung, A., Beattie, B., Richards, D. P., Canadien, V., Lalev, A., Mena, F., Wong, P., Starostine, A., Canete, M. M., Vlasblom, J., Wu, S., Orsi, C., Collins, S. R., Chandran, S., Haw, R., Rilstone, J. J., Gandi, K., Thompson, N. J., Musso, G., St Onge, P., Ghanny, S., Lam, M. H., Butland, G., Altaf-Ul, A. M., Kanaya, S., Shilatifard, A., O'Shea, E., Weissman, J. S., Ingles, C. J., Hughes, T. R., Parkinson, J., Gerstein, M., Wodak, S. J., Emili, A., and Greenblatt, J. F. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643
60. Maurer-Stroh, S., Dickens, N. J., Hughes-Davies, L., Kouzarides, T., Eisenhaber, F., and Ponting, C. P. (2003) The Tudor domain ?Royal Family': Tudor, plant Agenet, Chromo, PWWP, and MBT domains. Trends Biochem.l Sci. 28, 69-74
61. Tackett, A. J., Dilworth, D. J., Davey, M. J., O'Donnell, M., Aitchison, J. D., Rout, M. P., and Chait, B. T. (2005) Proteomic and genomic characterization of chromatin complexes at a boundary. J. Cell Biol.169, 35-47
62. Wang, Y., Kallgren, S. P., Reddy, B. D., Kuntz, K., Lopez-Maury, L., Thompson, J., Watt, S., Ma, C., Hou, H., Shi, Y., Yates, J. R., 3rd, Bahler, J., O'Connell, M. J., and Jia, S. (2012) Histone H3 lysine 14 acetylation is required for activation of a DNA damage checkpoint in fission yeast. J. Biol. Chem. 287, 4386-4393
63. Tackett, A. J., DeGrasse, J. A., Sekedat, M. D., Oeffinger, M., Rout, M. P., and Chait, B. T. (2005) I-DIRT, a general method for distinguishing between specific and nonspecific protein interactions. J. Proteome Res. 4, 1752-1756
64. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392
65. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
66. Vizcaino, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Rios, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H. J., Albar, J. P., Martinez-Bartolome, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) Proteome-Xchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226
67. Cote, R. G., Griss, J., Dianes, J. A., Wang, R., Wright, J. C., van den Toorn, H. W., van Breukelen, B., Heck, A. J., Hulstaert, N., Martens, L., Reisinger, F., Csordas, A., Ovelleiro, D., Perez-Rivevol, Y., Barsnes, H., Hermjakob, H., and Vizcaino, J. A. (2012) The PRoteomics IDEntification (PRIDE) Converter 2 framework: an improved suite of tools to facilitate data submission to the PRIDE database and the ProteomeXchange consortium. Mol. Cell. Proteomics 11, 1682-1689
68. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., O'Kelly, G., Schoenegger, A., Ovelleiro, D., Perez-Riverol, Y., Reisinger, F., Rios, D., Wang, R., and Hermjakob, H. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-D1069
69. Wang, R., Fabregat, A., Rios, D., Ovelleiro, D., Foster, J. M., Cote, R. G., Griss, J., Csordas, A., Perez-Riverol, Y., Reisinger, F., Hermjakob, H., Martens, L., and Vizcaino, J. A. (2012) PRIDE Inspector: a tool to visualize and validate MS proteomics data. Nat. Biotechnol. 30, 135-137
70. Rothbart, S. B., Krajewski, K., Strahl, B. D., and Fuchs, S. M. (2012) Peptide microarrays to interrogate the "histone code." Methods Enzymol. 512, 107-135
71. Rothbart, S. B., Krajewski, K., Nady, N., Tempel, W., Xue, S., Badeaux, A. I., Barsyte-Lovejoy, D., Martinez, J. Y., Bedford, M. T., Fuchs, S. M., Arrowsmith, C. H., and Strahl, B. D. (2012) Association of UHRF1 with methylated H3K9 directs the maintenance of DNA methylation. Nat. Struct. Mol. Biol. 19, 1155-1160
72. Janke, C., Magiera, M. M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E., and Knop, M. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962
73. Boeke, J. D., Trueheart, J., Natsoulis, G., and Fink, G. R. (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154, 164-175
74. Byrum, S. D., Raman, A., Taverna, S. D., and Tackett, A. J. (2012) ChAPMS: a method for identification of proteins and histone posttranslational modifications at a single genomic locus. Cell Reports 2, 198-205
75. Byrum, S. D., Taverna, S. D., and Tackett, A. J. (2013) Purification of a specific native genomic locus for proteomic analysis. Nucleic Acids Res. 41, e195
76. Kabani, M., Michot, K., Boschiero, C., and Werner, M. (2005) Anc1 interacts with the catalytic subunits of the general transcription factors TFIID and TFIIF, the chromatin remodeling complexes RSC and INO80, and the histone acetyltransferase complex NuA3. Biochem. Biophys. Res. Commun. 332, 398-403
77. Yap, K. L., and Zhou, M. M. (2010) Keeping it in the family: diverse histone recognition by conserved structural folds. Crit. Rev. Biochem. Mol. Biol. 45, 488-505
78. Dimmer, E. C., Huntley, R. P., Alam-Faruque, Y., Sawford, T., O'Donovan, C., Martin, M. J., Bely, B., Browne, P., Mun Chan, W., Eberhardt, R., Gardner, M., Laiho, K., Legge, D., Magrane, M., Pichler, K., Poggioli, D., Sehra, H., Auchincloss, A., Axelsen, K., Blatter, M. C., Boutet, E., Braconi-Quintaje, S., Breuza, L., Bridge, A., Coudert, E., Estreicher, A., Famiglietti, L., Ferro-Rojas, S., Feuermann, M., Gos, A., Gruaz-Gumowski, N., Hinz, U., Hulo, C., James, J., Jimenez, S., Jungo, F., Keller, G., Lemercier, P., Lieberherr, D., Masson, P., Moinat, M., Pedruzzi, I., Poux, S., Rivoire, C., Roechert, B., Schneider, M., Stutz, A., Sundaram, S., Tognolli, M., Bougueleret, L., Argoud-Puy, G., Cusin, I., Duek-Roggli, P., Xenarios, I., and Apweiler, R. (2012) The UniProt-GO Annotation database in 2011. Nucleic Acids Res. 40, D565-D570
79. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
80. Qiu, Y., Zhang, W., Zhao, C., Wang, Y., Wang, W., Zhang, J., Zhang, Z., Li, G., Shi, Y., Tu, X., and Wu, J. (2012) Solution structure of the Pdp1 PWWP domain reveals its unique binding sites for methylated H4K20 and DNA. Biochem. J. 442, 527-538
81. Wen, H., Li, Y., Xi, Y., Jiang, S., Stratton, S., Peng, D., Tanaka, K., Ren, Y., Xia, Z., Wu, J., Li, B., Barton, M. C., Li, W., Li, H., and Shi, X. (2014) ZMYND11 links histone H3.3K36me3 to transcription elongation and tumor suppression. Nature 508, 263-268
82. Youdell, M. L., Kizer, K. O., Kisseleva-Romanova, E., Fuchs, S. M., Duro, E., Strahl, B. D., and Mellor, J. (2008) Roles for Ctk1 and Spt6 in regulating the different methylation states of histone H3 lysine 36. Mol. Cell. Biol. 28, 4915-4926
83. Chruscicki, A., Macdonald, V. E., Young, B. P., Loewen, C. J., and Howe, L. J. (2010) Critical determinants for chromatin binding by Saccharomyces cerevisiae Yng1 exist outside of the plant homeodomain finger. Genetics 185, 469-477
84. Doolin, M. T., Johnson, A. L., Johnston, L. H., and Butler, G. (2001) Overlapping and distinct roles of the duplicated yeast transcription factors Ace2p and Swi5p. Mol. Microbiol. 40, 422-432
85. Tadauchi, T., Matsumoto, K., Herskowitz, I., and Irie, K. (2001) Posttranscriptional regulation through the HO 3-UTR by Mpt5, a yeast homolog of Pumilio and FBF. EMBO J. 20, 552-561
86. Keogh, M. C., Podolny, V., and Buratowski, S. (2003) Bur1 kinase is required for efficient transcription elongation by RNA polymerase II. Mol. Cell. Biol. 23, 7005-7018
87. Liu, Y., Warfield, L., Zhang, C., Luo, J., Allen, J., Lang, W. H., Ranish, J., Shokat, K. M., and Hahn, S. (2009) Phosphorylation of the transcription elongation factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol. Cell. Biol. 29, 4852-4863
88. Chu, Y., Sutton, A., Sternglanz, R., and Prelich, G. (2006) The BUR1 cyclin-dependent protein kinase is required for the normal pattern of histone methylation by SET2. Mol. Cell. Biol. 26, 3029-3038
89. Howe, L., Auston, D., Grant, P., John, S., Cook, R. G., Workman, J. L., and Pillus, L. (2001) Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev. 15, 3144-3154
90. Govind, C. K., Zhang, F., Qiu, H., Hofmeyer, K., and Hinnebusch, A. G. (2007) Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol. Cell 25, 31-42
91. Sterner, D. E., Belotserkovskaya, R., and Berger, S. L. (2002) SALSA, a variant of yeast SAGA, contains truncated Spt7, which correlates with activated transcription. Proc. Natl. Acad. Sci. U. S. A. 99, 11622-11627
92. Ullah, M., Pelletier, N., Xiao, L., Zhao, S. P., Wang, K., Degerny, C., Tahmasebi, S., Cayrou, C., Doyon, Y., Goh, S. L., Champagne, N., Cote, J., and Yang, X. J. (2008) Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol. Cell. Biol. 28, 6828-6843
93. Kimura, M., Suzuki, H., and Ishihama, A. (2002) Formation of a carboxyterminal domain phosphatase (Fcp1)/TFIIF/RNA polymerase II (pol II) complex in Schizosaccharomyces pombe involves direct interaction between Fcp1 and the Rpb4 subunit of pol II. Mol. Cell. Biol. 22, 1577-1588
94. Ginsburg, D. S., Govind, C. K., and Hinnebusch, A. G. (2009) NuA4 lysine acetyltransferase Esa1 is targeted to coding regions and stimulates transcription elongation with Gcn5. Mol. Cell. Biol. 29, 6473-6487
95. Sanso, M., Vargas-Perez, I., Quintales, L., Antequera, F., Ayte, J., and Hidalgo, E. (2011) Gcn5 facilitates Pol II progression, rather than recruitment to nucleosome-depleted stress promoters, in Schizosaccharomy-ces pombe. Nucleic Acids Res. 39, 6369-6379
96. Balasubramanian, R., Pray-Grant, M. G., Selleck, W., Grant, P. A., and Tan, S. (2002) Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J. Biol. Chem. 277, 7989-7995
97. Grant, P. A., Eberharter, A., John, S., Cook, R. G., Turner, B. M., and Workman, J. L. (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 274, 5895-5900
98. Kuo, Y. M., and Andrews, A. J. (2013) Quantitating the specificity and selectivity of Gcn5-mediated acetylation of histone H3. PloS One 8, e54896
99. Zhang, W., Bone, J. R., Edmondson, D. G., Turner, B. M., and Roth, S. Y. (1998) Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 17, 3155-3167
100. Lalonde, M. E., Avvakumov, N., Glass, K. C., Joncas, F. H., Saksouk, N., Holliday, M., Paquet, E., Yan, K., Tong, Q., Klein, B. J., Tan, S., Yang, X. J., Kutateladze, T. G., and Cote, J. (2013) Exchange of associated factors directs a switch in HBO1 acetyltransferase histone tail specificity. Genes Dev. 27, 2009-2024
101. Pryde, F., Jain, D., Kerr, A., Curley, R., Mariotti, F. R., and Vogelauer, M. (2009) H3 k36 methylation helps determine the timing of cdc45 association with replication origins. PloS One 4, e5882
102. Kremer, S. B., and Gross, D. S. (2009) SAGA and Rpd3 chromatin modification complexes dynamically regulate heat shock gene structure and expression. J. Biol. Chem. 284, 32914-32931
103. Kristjuhan, A., and Svejstrup, J. Q. (2004) Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 23, 4243-4252
104. Wyce, A., Xiao, T., Whelan, K. A., Kosman, C., Walter, W., Eick, D., Hughes, T. R., Krogan, N. J., Strahl, B. D., and Berger, S. L. (2007) H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol. Cell 27, 275-288
105. Cengiz, B., Gunduz, E., Gunduz, M., Beder, L. B., Tamamura, R., Bagci, C., Yamanaka, N., Shimizu, K., and Nagatsuka, H. (2010) Tumor-specific mutation and downregulation of ING5 detected in oral squamous cell carcinoma. Int.J. Cancer 127, 2088-2094
106. Avvakumov, N., and Cote, J. (2007) The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene 26, 5395-5407
107. Gunduz, M., Gunduz, E., Rivera, R. S., and Nagatsuka, H. (2008) The inhibitor of growth (ING) gene family: potential role in cancer therapy. Curr. Cancer Drug Targets 8, 275-284
108. Helin, K., and Dhanak, D. (2013) Chromatin proteins and modifications as drug targets. Nature 502, 480-488
109. Natoli, G. (2009) Control of NF-kappaB-dependent transcriptional responses by chromatin organization. Cold Spring Harbor Perspectives In Biology 1, a000224
110. Taverna, S. D., and Cole, P. A. (2010) Drug discovery: reader's block. Nature 468, 1050-1051