Reading the Combinatorial Histone Language

ACS Chemical Biology

Volumn 11, Issue 3, 2016, Pages 564-574

  Su, Zhangli ^a   Denu, John M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHROMATIN BINDING PROTEIN; HISTONE; UNCLASSIFIED DRUG; CHROMATIN;

CATALYSIS; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; COMBINATORIAL LIBRARY; EMBEDDING; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; CHROMATIN; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

CHROMATIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; PROTEIN DOMAINS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84961775708     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00864     Document Type: Review

References (110)

1. Kornberg, R. D. (1974) Chromatin structure: a repeating unit of histones and DNA Science 184, 868-871 10.1126/science.184.4139.868
2. Kornberg, R. D. and Klug, A. (1981) The nucleosome Sci. Am. 244, 52-64 10.1038/scientificamerican0281-52
3. Kornberg, R. D. and Lorch, Y. (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome Cell 98, 285-294 10.1016/S0092-8674(00)81958-3
4. Li, G. and Zhu, P. (2015) Structure and organization of chromatin fiber in the nucleus FEBS Lett. 589, 2893-2904 10.1016/j.febslet.2015.04.023
5. Cutter, A. R. and Hayes, J. J. (2015) A brief review of nucleosome structure FEBS Lett. 589, 2914-2922 10.1016/j.febslet.2015.05.016
6. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution Nature 389, 251-260 10.1038/38444
7. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W., and Richmond, T. J. (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution J. Mol. Biol. 319, 1097-1113 10.1016/S0022-2836(02)00386-8
8. Huang, H., Lin, S., Garcia, B. A., and Zhao, Y. (2015) Quantitative proteomic analysis of histone modifications Chem. Rev. 115, 2376-2418 10.1021/cr500491u
9. Bannister, A. J. and Kouzarides, T. (2011) Regulation of chromatin by histone modifications Cell Res. 21, 381-395 10.1038/cr.2011.22
10. House, N. C., Koch, M. R., and Freudenreich, C. H. (2014) Chromatin modifications and DNA repair: beyond double-strand breaks Front. Genet. 5, 296 10.3389/fgene.2014.00296
11. Swygert, S. G. and Peterson, C. L. (2014) Chromatin dynamics: interplay between remodeling enzymes and histone modifications Biochim. Biophys. Acta, Gene Regul. Mech. 1839, 728-736 10.1016/j.bbagrm.2014.02.013
12. Annalisa, I. and Robert, S. (2015) The role of linker histone H1 modifications in the regulation of gene expression and chromatin dynamics Biochim. Biophys. Acta, Gene Regul. Mech. S1874-9399 (15) 00189-3 10.1016/j.bbagrm.2015.09.003
13. Zentner, G. E. and Henikoff, S. (2013) Regulation of nucleosome dynamics by histone modifications Nat. Struct. Mol. Biol. 20, 259-266 10.1038/nsmb.2470
14. 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 10.1038/nsmb1338
15. Musselman, C. A., Lalonde, M. E., Cote, J., and Kutateladze, T. G. (2012) Perceiving the epigenetic landscape through histone readers Nat. Struct. Mol. Biol. 19, 1218-1227 10.1038/nsmb.2436
16. Bhaumik, S. R., Smith, E., and Shilatifard, A. (2007) Covalent modifications of histones during development and disease pathogenesis Nat. Struct. Mol. Biol. 14, 1008-1016 10.1038/nsmb1337
17. Greer, E. L. and Shi, Y. (2012) Histone methylation: a dynamic mark in health, disease and inheritance Nat. Rev. Genet. 13, 343-357 10.1038/nrg3173
18. Chi, P., Allis, C. D., and Wang, G. G. (2010) Covalent histone modifications - miswritten, misinterpreted and mis-erased in human cancers Nat. Rev. Cancer 10, 457-469 10.1038/nrc2876
19. Strahl, B. D. and Allis, C. D. (2000) The language of covalent histone modifications Nature 403, 41-45 10.1038/47412
20. Li, B., Carey, M., and Workman, J. L. (2007) The role of chromatin during transcription Cell 128, 707-719 10.1016/j.cell.2007.01.015
21. Oliver, S. S. and Denu, J. M. (2011) Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a "histone language" ChemBioChem 12, 299-307 10.1002/cbic.201000474
22. Fan, J., Krautkramer, K. A., Feldman, J. L., and Denu, J. M. (2015) Metabolic regulation of histone post-translational modifications ACS Chem. Biol. 10, 95-108 10.1021/cb500846u
23. Rothbart, S. B. and Strahl, B. D. (2014) Interpreting the language of histone and DNA modifications Biochim. Biophys. Acta, Gene Regul. Mech. 1839, 627-643 10.1016/j.bbagrm.2014.03.001
24. Yuan, Z. F., Arnaudo, A. M., and Garcia, B. A. (2014) Mass spectrometric analysis of histone proteoforms Annu. Rev. Anal. Chem. 7, 113-128 10.1146/annurev-anchem-071213-015959
25. Suganuma, T. and Workman, J. L. (2011) Signals and combinatorial functions of histone modifications Annu. Rev. Biochem. 80, 473-499 10.1146/annurev-biochem-061809-175347
26. Badeaux, A. I. and Shi, Y. (2013) Emerging roles for chromatin as a signal integration and storage platform Nat. Rev. Mol. Cell Biol. 14, 211-224 10.1038/nrm3545
27. Tan, M. J., Luo, H., Lee, S., Jin, F. L., Yang, J. S., Montellier, E., Buchou, T., Cheng, Z. Y., Rousseaux, S., Rajagopal, N., Lu, Z. K., Ye, Z., Zhu, Q., Wysocka, J., Ye, Y., Khochbin, S., Ren, B., and Zhao, Y. M. (2011) Identification of 67 Histone Marks and Histone Lysine Crotonylation as a New Type of Histone Modification Cell 146, 1015-1027 10.1016/j.cell.2011.08.008
28. Arnaudo, A. M. and Garcia, B. A. (2013) Proteomic characterization of novel histone post-translational modifications Epigenet. Chromatin 6, 24 10.1186/1756-8935-6-24
29. Kim, J., Daniel, J., Espejo, A., Lake, A., Krishna, M., Xia, L., Zhang, Y., and Bedford, M. T. (2006) Tudor, MBT and chromo domains gauge the degree of lysine methylation EMBO Rep. 7, 397-403 10.1038/sj.embor.7400625
30. Shi, X. B., Kachirskaia, I., Walter, K. L., Kuo, J. H. A., Lake, A., Davrazou, F., Chan, S. M., Martin, D. G. E., Fingerman, I. M., Briggs, S. D., Howe, L., Utz, P. J., Kutateladze, T. G., Lugovskoy, A. A., Bedford, M. T., and Gozani, O. (2007) Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36 J. Biol. Chem. 282, 2450-2455 10.1074/jbc.C600286200
31. Zhang, Q., Chakravarty, S., Ghersi, D., Zeng, L., Plotnikov, A. N., Sanchez, R., and Zhou, M. M. (2010) Biochemical profiling of histone binding selectivity of the yeast bromodomain family PLoS One 5, e8903 10.1371/journal.pone.0008903
32. 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 10.1371/journal.pone.0018919
33. Filippakopoulos, P., Picaud, S., Mangos, M., Keates, T., Lambert, J. P., Barsyte-Lovejoy, D., Felletar, I., Volkmer, R., Muller, S., Pawson, T., Gingras, A. C., Arrowsmith, C. H., and Knapp, S. (2012) Histone recognition and large-scale structural analysis of the human bromodomain family Cell 149, 214-231 10.1016/j.cell.2012.02.013
34. 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 10.3109/10409238.2010.512001
35. Musselman, C. A., Khorasanizadeh, S., and Kutateladze, T. G. (2014) Towards understanding methyllysine readout Biochim. Biophys. Acta, Gene Regul. Mech. 1839, 686-693 10.1016/j.bbagrm.2014.04.001
36. Fischle, W., Tseng, B. S., Dormann, H. L., Ueberheide, B. M., Garcia, B. A., Shabanowitz, J., Hunt, D. F., Funabiki, H., and Allis, C. D. (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation Nature 438, 1116-1122 10.1038/nature04219
37. Wilkinson, A. W. and Gozani, O. (2014) Histone-binding domains: strategies for discovery and characterization Biochim. Biophys. Acta, Gene Regul. Mech. 1839, 669-675 10.1016/j.bbagrm.2014.01.007
38. Karch, K. R., Denizio, J. E., Black, B. E., and Garcia, B. A. (2013) Identification and interrogation of combinatorial histone modifications Front. Genet. 4, 264 10.3389/fgene.2013.00264
39. Fuchs, S. M., Krajewski, K., Baker, R. W., Miller, V. L., and Strahl, B. D. (2011) Influence of combinatorial histone modifications on antibody and effector protein recognition Curr. Biol. 21, 53-58 10.1016/j.cub.2010.11.058
40. Bock, I., Dhayalan, A., Kudithipudi, S., Brandt, O., Rathert, P., and Jeltsch, A. (2011) Detailed specificity analysis of antibodies binding to modified histone tails with peptide arrays Epigenetics 6, 256-263 10.4161/epi.6.2.13837
41. Bua, D. J., Kuo, A. J., Cheung, P., Liu, C. L., Migliori, V., Espejo, A., Casadio, F., Bassi, C., Amati, B., Bedford, M. T., Guccione, E., and Gozani, O. (2009) Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks PLoS One 4, e6789 10.1371/journal.pone.0006789
42. Egelhofer, T. A., Minoda, A., Klugman, S., Lee, K., Kolasinska-Zwierz, P., Alekseyenko, A. A., Cheung, M. S., Day, D. S., Gadel, S., Gorchakov, A. A., Gu, T., Kharchenko, P. V., Kuan, S., Latorre, I., Linder-Basso, D., Luu, Y., Ngo, Q., Perry, M., Rechtsteiner, A., Riddle, N. C., Schwartz, Y. B., Shanower, G. A., Vielle, A., Ahringer, J., Elgin, S. C., Kuroda, M. I., Pirrotta, V., Ren, B., Strome, S., Park, P. J., Karpen, G. H., Hawkins, R. D., and Lieb, J. D. (2011) An assessment of histone-modification antibody quality Nat. Struct. Mol. Biol. 18, 91-93 10.1038/nsmb.1972
43. Heubach, Y., Planatscher, H., Sommersdorf, C., Maisch, D., Maier, J., Joos, T. O., Templin, M. F., and Poetz, O. (2013) From spots to beads-PTM-peptide bead arrays for the characterization of anti-histone antibodies Proteomics 13, 1010-1015 10.1002/pmic.201200383
44. Nishikori, S., Hattori, T., Fuchs, S. M., Yasui, N., Wojcik, J., Koide, A., Strahl, B. D., and Koide, S. (2012) Broad ranges of affinity and specificity of anti-histone antibodies revealed by a quantitative peptide immunoprecipitation assay J. Mol. Biol. 424, 391-399 10.1016/j.jmb.2012.09.022
45. Su, Z., Boersma, M. D., Lee, J. H., Oliver, S. S., Liu, S., Garcia, B. A., and Denu, J. M. (2014) ChIP-less analysis of chromatin states Epigenet. Chromatin 7, 7 10.1186/1756-8935-7-7
46. Garcia, B. A., Mollah, S., Ueberheide, B. M., Busby, S. A., Muratore, T. L., Shabanowitz, J., and Hunt, D. F. (2007) Chemical derivatization of histones for facilitated analysis by mass spectrometry Nat. Protoc. 2, 933-938 10.1038/nprot.2007.106
47. Young, N. L., DiMaggio, P. A., Plazas-Mayorca, M. D., Baliban, R. C., Floudas, C. A., and Garcia, B. A. (2009) High throughput characterization of combinatorial histone codes Mol. Cell. Proteomics 8, 2266-2284 10.1074/mcp.M900238-MCP200
48. Leroy, G., Dimaggio, P. A., Chan, E. Y., Zee, B. M., Blanco, M. A., Bryant, B., Flaniken, I. Z., Liu, S., Kang, Y., Trojer, P., and Garcia, B. A. (2013) A quantitative atlas of histone modification signatures from human cancer cells Epigenet. Chromatin 6, 20 10.1186/1756-8935-6-20
49. Taverna, S. D., Ueberheide, B. M., Liu, Y. F., Tackett, A. J., Diaz, R. L., Shabanowitz, J., Chait, B. T., Hunt, D. F., and Allis, C. D. (2007) Long-distance combinatorial linkage between methylation and acetylation on histone H3N termini Proc. Natl. Acad. Sci. U. S. A. 104, 2086-2091 10.1073/pnas.0610993104
50. Phanstiel, D., Brumbaugh, J., Berggren, W. T., Conard, K., Feng, X., Levenstein, M. E., McAlister, G. C., Thomson, J. A., and Coon, J. J. (2008) Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells Proc. Natl. Acad. Sci. U. S. A. 105, 4093-4098 10.1073/pnas.0710515105
51. Wang, Z. B., Zang, C. Z., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K. R., Roh, T. Y., Peng, W. Q., Zhang, M. Q., and Zhao, K. J. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome Nat. Genet. 40, 897-903 10.1038/ng.154
52. Ernst, J. and Kellis, M. (2010) Discovery and characterization of chromatin states for systematic annotation of the human genome Nat. Biotechnol. 28, 817-825 10.1038/nbt.1662
53. Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., Ku, M., Durham, T., Kellis, M., and Bernstein, B. E. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types Nature 473, 43-49 10.1038/nature09906
54. Kharchenko, P. V., Alekseyenko, A. A., Schwartz, Y. B., Minoda, A., Riddle, N. C., Ernst, J., Sabo, P. J., Larschan, E., Gorchakov, A. A., Gu, T., Linder-Basso, D., Plachetka, A., Shanower, G., Tolstorukov, M. Y., Luquette, L. J., Xi, R., Jung, Y. L., Park, R. W., Bishop, E. P., Canfield, T. K., Sandstrom, R., Thurman, R. E., MacAlpine, D. M., Stamatoyannopoulos, J. A., Kellis, M., Elgin, S. C., Kuroda, M. I., Pirrotta, V., Karpen, G. H., and Park, P. J. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster Nature 471, 480-485 10.1038/nature09725
55. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T. K., Koche, R. P., Lee, W., Mendenhall, E., O'Donovan, A., Presser, A., Russ, C., Xie, X., Meissner, A., Wernig, M., Jaenisch, R., Nusbaum, C., Lander, E. S., and Bernstein, B. E. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 448, 553-560 10.1038/nature06008
56. Zhu, J., Adli, M., Zou, J. Y., Verstappen, G., Coyne, M., Zhang, X., Durham, T., Miri, M., Deshpande, V., De Jager, P. L., Bennett, D. A., Houmard, J. A., Muoio, D. M., Onder, T. T., Camahort, R., Cowan, C. A., Meissner, A., Epstein, C. B., Shoresh, N., and Bernstein, B. E. (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues Cell 152, 642-654 10.1016/j.cell.2012.12.033
57. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., Jaenisch, R., Wagschal, A., Feil, R., Schreiber, S. L., and Lander, E. S. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells Cell 125, 315-326 10.1016/j.cell.2006.02.041
58. Voigt, P., LeRoy, G., Drury, W. J., 3rd, Zee, B. M., Son, J., Beck, D. B., Young, N. L., Garcia, B. A., and Reinberg, D. (2012) Asymmetrically modified nucleosomes Cell 151, 181-193 10.1016/j.cell.2012.09.002
59. Peach, S. E., Rudomin, E. L., Udeshi, N. D., Carr, S. A., and Jaffe, J. D. (2012) Quantitative assessment of chromatin immunoprecipitation grade antibodies directed against histone modifications reveals patterns of co-occurring marks on histone protein molecules Mol. Cell. Proteomics 11, 128-137 10.1074/mcp.M111.015941
60. Soldi, M. and Bonaldi, T. (2013) The proteomic investigation of chromatin functional domains reveals novel synergisms among distinct heterochromatin components Mol. Cell. Proteomics 12, 764-780 10.1074/mcp.M112.024307
61. Han, Y. and Garcia, B. A. (2013) Combining genomic and proteomic approaches for epigenetics research Epigenomics 5, 439-452 10.2217/epi.13.37
62. Rothbart, S. B., Dickson, B. M., Raab, J. R., Grzybowski, A. T., Krajewski, K., Guo, A. H., Shanle, E. K., Josefowicz, S. Z., Fuchs, S. M., Allis, C. D., Magnuson, T. R., Ruthenburg, A. J., and Strahl, B. D. (2015) An Interactive Database for the Assessment of Histone Antibody Specificity Mol. Cell 59, 502-511 10.1016/j.molcel.2015.06.022
63. Hattori, T., Taft, J. M., Swist, K. M., Luo, H., Witt, H., Slattery, M., Koide, A., Ruthenburg, A. J., Krajewski, K., Strahl, B. D., White, K. P., Farnham, P. J., Zhao, Y., and Koide, S. (2013) Recombinant antibodies to histone post-translational modifications Nat. Methods 10, 992-995 10.1038/nmeth.2605
64. Kungulovski, G., Kycia, I., Tamas, R., Jurkowska, R. Z., Kudithipudi, S., Henry, C., Reinhardt, R., Labhart, P., and Jeltsch, A. (2014) Application of histone modification-specific interaction domains as an alternative to antibodies Genome Res. 24, 1842-1853 10.1101/gr.170985.113
65. Voon, H. P., Hughes, J. R., Rode, C., De La Rosa-Velazquez, I. A., Jenuwein, T., Feil, R., Higgs, D. R., and Gibbons, R. J. (2015) ATRX Plays a Key Role in Maintaining Silencing at Interstitial Heterochromatic Loci and Imprinted Genes Cell Rep. 11, 405-418 10.1016/j.celrep.2015.03.036
66. Garske, A. L., Oliver, S. S., Wagner, E. K., Musselman, C. A., LeRoy, G., Garcia, B. A., Kutateladze, T. G., and Denu, J. M. (2010) Combinatorial profiling of chromatin binding modules reveals multisite discrimination Nat. Chem. Biol. 6, 283-290 10.1038/nchembio.319
67. Musselman, C. A., Lalonde, M. E., Cote, J., and Kutateladze, T. G. (2012) Perceiving the epigenetic landscape through histone readers Nat. Struct. Mol. Biol. 19, 1218-1227 10.1038/nsmb.2436
68. Ruthenburg, A. J., Li, H., Patel, D. J., and Allis, C. D. (2007) Multivalent engagement of chromatin modifications by linked binding modules Nat. Rev. Mol. Cell Biol. 8, 983-994 10.1038/nrm2298
69. Muller, M. M. and Muir, T. W. (2015) Histones: At the Crossroads of Peptide and Protein Chemistry Chem. Rev. 115, 2296-2349 10.1021/cr5003529
70. Bock, I., Kudithipudi, S., Tamas, R., Kungulovski, G., Dhayalan, A., and Jeltsch, A. (2011) Application of Celluspots peptide arrays for the analysis of the binding specificity of epigenetic reading domains to modified histone tails BMC Biochem. 12, 48 10.1186/1471-2091-12-48
71. Cai, L., Rothbart, S. B., Lu, R., Xu, B., Chen, W. Y., Tripathy, A., Rockowitz, S., Zheng, D., Patel, D. J., Allis, C. D., Strahl, B. D., Song, J., and Wang, G. G. (2013) An H3K36 methylation-engaging Tudor motif of polycomb-like proteins mediates PRC2 complex targeting Mol. Cell 49, 571-582 10.1016/j.molcel.2012.11.026
72. Wysocka, J., Swigut, T., Xiao, H., Milne, T. A., Kwon, S. Y., Landry, J., Kauer, M., Tackett, A. J., Chait, B. T., Badenhorst, P., Wu, C., and Allis, C. D. (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling Nature 442, 86-90 10.1038/nature04815
73. 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 10.1016/j.cell.2010.08.020
74. Noh, K. M., Maze, I., Zhao, D., Xiang, B., Wenderski, W., Lewis, P. W., Shen, L., Li, H., and Allis, C. D. (2015) ATRX tolerates activity-dependent histone H3 methyl/phos switching to maintain repetitive element silencing in neurons Proc. Natl. Acad. Sci. U. S. A. 112, 6820-6827 10.1073/pnas.1411258112
75. Nikolov, M. and Fischle, W. (2013) Systematic analysis of histone modification readout Mol. BioSyst. 9, 182-194 10.1039/C2MB25328C
76. Tsai, W. W., Wang, Z. X., Yiu, T. T., Akdemir, K. C., Xia, W. Y., Winter, S., Tsai, C. Y., Shi, X. B., Schwarzer, D., Plunkett, W., Aronow, B., Gozani, O., Fischle, W., Hung, M. C., Patel, D. J., and Barton, M. C. (2010) TRIM24 links a non-canonical histone signature to breast cancer Nature 468, 927-932 10.1038/nature09542
77. Dhayalan, A., Tamas, R., Bock, I., Tattermusch, A., Dimitrova, E., Kudithipudi, S., Ragozin, S., and Jeltsch, A. (2011) The ATRX-ADD domain binds to H3 tail peptides and reads the combined methylation state of K4 and K9 Hum. Mol. Genet. 20, 2195-2203 10.1093/hmg/ddr107
78. Iwase, S., Xiang, B., Ghosh, S., Ren, T., Lewis, P. W., Cochrane, J. C., Allis, C. D., Picketts, D. J., Patel, D. J., Li, H. T., and Shi, Y. (2011) ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome Nat. Struct. Mol. Biol. 18, 769-776 10.1038/nsmb.2062
79. Eustermann, S., Yang, J. C., Law, M. J., Amos, R., Chapman, L. M., Jelinska, C., Garrick, D., Clynes, D., Gibbons, R. J., Rhodes, D., Higgs, D. R., and Neuhaus, D. (2011) Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin Nat. Struct. Mol. Biol. 18, 777-782 10.1038/nsmb.2070
80. Xie, S., Jakoncic, J., and Qian, C. M. (2012) UHRF1 Double Tudor Domain and the Adjacent PHD Finger Act Together to Recognize K9me3-Containing Histone H3 Tail J. Mol. Biol. 415, 318-328 10.1016/j.jmb.2011.11.012
81. Arita, K., Isogai, S., Oda, T., Unoki, M., Sugita, K., Sekiyama, N., Kuwata, K., Hamamoto, R., Tochio, H., Sato, M., Ariyoshi, M., and Shirakawa, M. (2012) Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1 Proc. Natl. Acad. Sci. U. S. A. 109, 12950-12955 10.1073/pnas.1203701109
82. Nady, N., Lemak, A., Walker, J. R., Avvakumov, G. V., Kareta, M. S., Achour, M., Xue, S., Duan, S. L., Allali-Hassani, A., Zuo, X. B., Wang, Y. X., Bronner, C., Chedin, F., Arrowsmith, C. H., and Dhe-Paganon, S. (2011) Recognition of Multivalent Histone States Associated with Heterochromatin by UHRF1 Protein J. Biol. Chem. 286, 24300-24311 10.1074/jbc.M111.234104
83. Cheng, J. D., Yang, Y., Fang, J., Xiao, J. X., Zhu, T. T., Chen, F., Wang, P., Li, Z., Yang, H. R., and Xu, Y. H. (2013) Structural Insight into Coordinated Recognition of Trimethylated Histone H3 Lysine 9 (H3K9me3) by the Plant Homeodomain (PHD) and Tandem Tudor Domain (TTD) of UHRF1 (Ubiquitin-like, Containing PHD and RING Finger Domains, 1) Protein J. Biol. Chem. 288, 1329-1339 10.1074/jbc.M112.415398
84. 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 10.1038/nsmb.2391
85. Gelato, K. A., Tauber, M., Ong, M. S., Winter, S., Hiragami-Hamada, K., Sindlinger, J., Lemak, A., Bultsma, Y., Houliston, S., Schwarzer, D., Divecha, N., Arrowsmith, C. H., and Fischle, W. (2014) Accessibility of Different Histone H3-Binding Domains of UHRF1 Is Allosterically Regulated by Phosphatidylinositol 5-Phosphate Mol. Cell 54, 905-919 10.1016/j.molcel.2014.04.004
86. Wen, H., Li, Y. Y., Xi, Y. X., Jiang, S. M., Stratton, S., Peng, D. N., Tanaka, K., Ren, Y. F., Xia, Z., Wu, J., Li, B., Barton, M. C., Li, W., Li, H. T., and Shi, X. B. (2014) ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression Nature 508, 263-268 10.1038/nature13045
87. Guo, R., Zheng, L., Park, J. W., Lv, R., Chen, H., Jiao, F., Xu, W., Mu, S., Wen, H., Qiu, J., Wang, Z., Yang, P., Wu, F., Hui, J., Fu, X., Shi, X., Shi, Y. G., Xing, Y., Lan, F., and Shi, Y. (2014) BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated pre-mRNA processing Mol. Cell 56, 298-310 10.1016/j.molcel.2014.08.022
88. Nikolov, M., Stutzer, A., Mosch, K., Krasauskas, A., Soeroes, S., Stark, H., Urlaub, H., and Fischle, W. (2011) Chromatin affinity purification and quantitative mass spectrometry defining the interactome of histone modification patterns Mol. Cell. Proteomics 10, M110.005371 10.1074/mcp.M110.005371
89. Ruthenburg, A. J., Li, H., Milne, T. A., Dewell, S., McGinty, R. K., Yuen, M., Ueberheide, B., Dou, Y., Muir, T. W., Patel, D. J., and Allis, C. D. (2011) Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions Cell 145, 692-706 10.1016/j.cell.2011.03.053
90. Mansfield, R. E., Musselman, C. A., Kwan, A. H., Oliver, S. S., Garske, A. L., Davrazou, F., Denu, J. M., Kutateladze, T. G., and Mackay, J. P. (2011) Plant Homeodomain (PHD) Fingers of CHD4 Are Histone H3-binding Modules with Preference for Unmodified H3K4 and Methylated H3K9 J. Biol. Chem. 286, 11779-11791 10.1074/jbc.M110.208207
91. Oliver, S. S., Musselman, C. A., Srinivasan, R., Svaren, J. P., Kutateladze, T. G., and Denu, J. M. (2012) Multivalent Recognition of Histone Tails by the PHD Fingers of CHD5 Biochemistry 51, 6534-6544 10.1021/bi3006972
92. Du, J. M., Zhong, X. H., Bernatavichute, Y. V., Stroud, H., Feng, S. H., Caro, E., Vashisht, A. A., Terragni, J., Chin, H. G., Tu, A., Hetzel, J., Wohlschlegel, J. A., Pradhan, S., Patel, D. J., and Jacobsen, S. E. (2012) Dual Binding of Chromomethylase Domains to H3K9me2-Containing Nucleosomes Directs DNA Methylation in Plants Cell 151, 167-180 10.1016/j.cell.2012.07.034
93. Nguyen, U. T., Bittova, L., Muller, M. M., Fierz, B., David, Y., Houck-Loomis, B., Feng, V., Dann, G. P., and Muir, T. W. (2014) Accelerated chromatin biochemistry using DNA-barcoded nucleosome libraries Nat. Methods 11, 834-840 10.1038/nmeth.3022
94. Canzio, D., Chang, E. Y., Shankar, S., Kuchenbecker, K. M., Simon, M. D., Madhani, H. D., Narlikar, G. J., and Al-Sady, B. (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly Mol. Cell 41, 67-81 10.1016/j.molcel.2010.12.016
95. Kilic, S., Bachmann, A. L., Bryan, L. C., and Fierz, B. (2015) Multivalency governs HP1alpha association dynamics with the silent chromatin state Nat. Commun. 6, 7313 10.1038/ncomms8313
96. Feng, W. J., Yonezawa, M., Ye, J., Jenuwein, T., and Grummt, I. (2010) PHF8 activates transcription of rRNA genes through H3K4me3 binding and H3K9me1/2 demethylation Nat. Struct. Mol. Biol. 17, 445-450 10.1038/nsmb.1778
97. Horton, J. R., Upadhyay, A. K., Qi, H. H., Zhang, X., Shi, Y., and Cheng, X. D. (2010) Enzymatic and structural insights for substrate specificity of a family of jumonji histone lysine demethylases Nat. Struct. Mol. Biol. 17, 38-43 10.1038/nsmb.1753
98. Torres, I. O., Kuchenbecker, K. M., Nnadi, C. I., Fletterick, R. J., Kelly, M. J., and Fujimori, D. G. (2015) Histone demethylase KDM5A is regulated by its reader domain through a positive-feedback mechanism Nat. Commun. 6, 6204 10.1038/ncomms7204
99. Ballare, C., Lange, M., Lapinaite, A., Martin, G. M., Morey, L., Pascual, G., Liefke, R., Simon, B., Shi, Y., Gozani, O., Carlomagno, T., Benitah, S. A., and Di Croce, L. (2012) Phf19 links methylated Lys36 of histone H3 to regulation of Polycomb activity Nat. Struct. Mol. Biol. 19, 1257-1265 10.1038/nsmb.2434
100. Brien, G. L., Gambero, G., O'Connell, D. J., Jerman, E., Turner, S. A., Egan, C. M., Dunne, E. J., Jurgens, M. C., Wynne, K., Piao, L., Lohan, A. J., Ferguson, N., Shi, X., Sinha, K. M., Loftus, B. J., Cagney, G., and Bracken, A. P. (2012) Polycomb PHF19 binds H3K36me3 and recruits PRC2 and demethylase NO66 to embryonic stem cell genes during differentiation Nat. Struct. Mol. Biol. 19, 1273-1281 10.1038/nsmb.2449
101. Musselman, C. A., Avvakumov, N., Watanabe, R., Abraham, C. G., Lalonde, M. E., Hong, Z., Allen, C., Roy, S., Nunez, J. K., Nickoloff, J., Kulesza, C. A., Yasui, A., Cote, J., and Kutateladze, T. G. (2012) Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1 Nat. Struct. Mol. Biol. 19, 1266-1272 10.1038/nsmb.2435
102. Flynn, E. M., Huang, O. W., Poy, F., Oppikofer, M., Bellon, S. F., Tang, Y., and Cochran, A. G. (2015) A Subset of Human Bromodomains Recognizes Butyryllysine and Crotonyllysine Histone Peptide Modifications Structure 23, 1801-1814 10.1016/j.str.2015.08.004
103. Sabari, B. R., Tang, Z. Y., Huang, H., Yong-Gonzalez, V., Molina, H., Kong, H. E., Dai, L. Z., Shimada, M., Cross, J. R., Zhao, Y. M., Roeder, R. G., and Allis, C. D. (2015) Intracellular Crotonyl-CoA Stimulates Transcription through p300-Catalyzed Histone Crotonylation Mol. Cell 58, 203-215 10.1016/j.molcel.2015.02.029
104. Feldman, J. L., Baeza, J., and Denu, J. M. (2013) Activation of the protein deacetylase SIRT6 by long-chain fatty acids and widespread deacylation by mammalian sirtuins J. Biol. Chem. 288, 31350-31356 10.1074/jbc.C113.511261
105. Jiang, H., Khan, S., Wang, Y., Charron, G., He, B., Sebastian, C., Du, J., Kim, R., Ge, E., Mostoslavsky, R., Hang, H. C., Hao, Q., and Lin, H. (2013) SIRT6 regulates TNF-alpha secretion through hydrolysis of long-chain fatty acyl lysine Nature 496, 110-113 10.1038/nature12038
106. Zeng, L., Zhang, Q., Li, S., Plotnikov, A. N., Walsh, M. J., and Zhou, M. M. (2010) Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b Nature 466, 258-262 10.1038/nature09139
107. Qiu, Y., Liu, L., Zhao, C., Han, C., Li, F., Zhang, J., Wang, Y., Li, G., Mei, Y., Wu, M., Wu, J., and Shi, Y. (2012) Combinatorial readout of unmodified H3R2 and acetylated H3K14 by the tandem PHD finger of MOZ reveals a regulatory mechanism for HOXA9 transcription Genes Dev. 26, 1376-1391 10.1101/gad.188359.112
108. Li, Y. Y., Wen, H., Xi, Y. X., Tanaka, K., Wang, H. B., Peng, D. N., Ren, Y. F., Jin, Q. H., Dent, S. Y. R., Li, W., Li, H. T., and Shi, X. B. (2014) AF9 YEATS Domain Links Histone Acetylation to DOT1L-Mediated H3K79 Methylation Cell 159, 558-571 10.1016/j.cell.2014.09.049
109. Talbert, P. B. and Henikoff, S. (2010) Histone variants - ancient wrap artists of the epigenome Nat. Rev. Mol. Cell Biol. 11, 264-275 10.1038/nrm2861
110. Maze, I., Noh, K. M., Soshnev, A. A., and Allis, C. D. (2014) Every amino acid matters: essential contributions of histone variants to mammalian development and disease Nat. Rev. Genet. 15, 259-271 10.1038/nrg3673