Histone H4 lysine 20 (H4K20) methylation, expanding the signaling potential of the proteome one methyl moiety at a time

Molecular and Cellular Proteomics

Volumn 15, Issue 3, 2016, Pages 755-764

  Van Nuland, Rick ^a   Gozani, Or ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H4; LYSINE; PROTEOME; CHROMATIN; HISTONE;

BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; CATALYSIS; CHROMATIN; DNA DAMAGE; DNA REPLICATION; GENE EXPRESSION; GENE SILENCING; HISTONE METHYLATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GENETIC EPIGENESIS; HUMAN; METABOLISM; METHYLATION; PROTEIN PROCESSING;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; LYSINE; METHYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SIGNAL TRANSDUCTION;

EID: 84962572943     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.R115.054742     Document Type: Review

References (90)

1. International Human Genome Sequencing Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431, 931-945
2. Pan, Q., Shai, O., Lee, L. J., Frey, B. J., and Blencowe, B. J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 40, 1413-1415
3. Minguez, P., Parca, L., Diella, F., Mende, D. R., Kumar, R., Helmer-Citterich, M., Gavin, A. C., van Noort, V., and Bork, P. (2012) Deciphering a global network of functionally associated post-translational modifications. Mol. Syst. Biol. 8, 599
4. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260
5. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705
6. Black, J. C., Van Rechem, C., and Whetstine, J. R. (2012) Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol. Cell 48, 491-507
7. Suganuma, T., and Workman, J. L. (2011) Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 80, 473-499
8. 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
9. Turner, B. M. (2005) Reading signals on the nucleosome with a new nomenclature for modified histones. Nat. Struct. Mol. Biol. 12, 110-112
10. Moore, K. E., and Gozani, O. (2014) An unexpected journey: lysine methylation across the proteome. Biochim. Biophys. Acta 1839, 1395-1403
11. Beck, D. B., Oda, H., Shen, S. S., and Reinberg, D. (2012) PR-Set7 and H4K20me1: at the crossroads of genome integrity, cell cycle, chromosome condensation, and transcription. Genes Dev. 26, 325-337
12. Jørgensen, S., Schotta, G., and Sørensen, C. S. (2013) Histone H4 lysine 20 methylation: key player in epigenetic regulation of genomic integrity. Nucleic Acids Res. 41, 2797-2806
13. Schotta, G., Sengupta, R., Kubicek, S., Malin, S., Kauer, M., Callén, E., Celeste, A., Pagani, M., Opravil, S., De La Rosa-Velazquez, I. A., Espejo, A., Bedford, M. T., Nussenzweig, A., Busslinger, M., and Jenuwein, T. (2008) A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22, 2048-2061
14. 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. Epigenetics Chromatin 6, 20
15. Pesavento, J. J., Yang, H., Kelleher, N. L., and Mizzen, C. A. (2008) Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol. Cell. Biol. 28, 468-486
16. Evertts, A. G., Manning, A. L., Wang, X., Dyson, N. J., Garcia, B. A., and Coller, H. A. (2013) H4K20 methylation regulates quiescence and chromatin compaction. Mol. Biol. Cell 24, 3025-3037
17. Nishioka, K., Rice, J. C., Sarma, K., Erdjument-Bromage, H., Werner, J., Wang, Y., Chuikov, S., Valenzuela, P., Tempst, P., Steward, R., Lis, J. T., Allis, C. D., and Reinberg, D. (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9, 1201-1213
18. Fang, J., Feng, Q., Ketel, C. S., Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Tempst, P., Simon, J. A., and Zhang, Y. (2002) Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 12, 1086-1099
19. Pannetier, M., Julien, E., Schotta, G., Tardat, M., Sardet, C., Jenuwein, T., and Feil, R. (2008) PR-SET7 and SUV4-20H regulate H4 lysine-20 methylation at imprinting control regions in the mouse. EMBO Rep. 9, 998-1005
20. Schotta, G., Lachner, M., Sarma, K., Ebert, A., Sengupta, R., Reuter, G., Reinberg, D., and Jenuwein, T. (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251-1262
21. Couture, J. F., Collazo, E., Brunzelle, J. S., and Trievel, R. C. (2005) Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev. 19, 1455-1465
22. Xiao, B., Jing, C., Kelly, G., Walker, P. A., Muskett, F. W., Frenkiel, T. A., Martin, S. R., Sarma, K., Reinberg, D., Gamblin, S. J., and Wilson, J. R. (2005) Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev. 19, 1444-1454
23. Kuo, A. J., Song, J., Cheung, P., Ishibe-Murakami, S., Yamazoe, S., Chen, J. K., Patel, D. J., and Gozani, O. (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484, 115-119
24. Pei, H., Zhang L., Luo, K., Qin, Y., Chesi, M., Fei, F., Bergsagel, P. L., Wang, L., You, Z., Lou, Z. (2011) MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470, 124-128
25. Li, Y., Trojer, P., Xu, C. F., Cheung, P., Kuo, A., Drury, W. J., 3rd, Qiao, Q., Neubert, T. A., Xu, R. M., Gozani, O., and Reinberg, D. (2009) The target of the NSD family of histone lysine methyltransferases depends on the nature of the substrate. J. Biol. Chem. 284, 34283-34295
26. Kuo, A. J., Cheung, P., Chen, K., Zee, B. M., Kioi, M., Lauring, J., Xi, Y., Park, B. H., Shi, X., Garcia, B. A., Li, W., and Gozani, O. (2011) NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming. Mol. Cell 44, 609-620
27. Van Aller, G. S., Reynoird, N., Barbash, O., Huddleston, M., Liu, S., Zmoos, A. F., McDevitt, P., Sinnamon, R., Le, B., Mas, G., Annan, R., Sage, J., Garcia, B. A., Tummino, P. J., Gozani, O., and Kruger, R. G. (2012) Smyd3 regulates cancer cell phenotypes and catalyzes histone H4 lysine 5 methylation. Epigenetics 7, 340-343
28. Kudithipudi, S., Kusevic, D., Weirich, S., and Jeltsch, A. (2014) Specificity analysis of protein lysine methyltransferases using SPOT peptide arrays. J. Vis. Exp. 93, e52203
29. Kudithipudi, S., Lungu, C., Rathert, P., Happel, N., and Jeltsch, A. (2014) Substrate specificity analysis and novel substrates of the protein lysine methyltransferase NSD1. Chem. Biol. 21, 226-237
30. Yang, H., Pesavento, J. J., Starnes, T. W., Cryderman, D. E., Wallrath, L. L., Kelleher, N. L., and Mizzen, C. A. (2008) Preferential dimethylation of histone H4 lysine 20 by Suv4-20. J. Biol. Chem. 283, 12085-12092
31. Southall, S. M., Cronin, N. B., and Wilson, J. R. (2014) A novel route to product specificity in the Suv4-20 family of histone H4K20 methyltransferases. Nucleic Acids Res. 42, 661-671
32. Wu, H., Siarheyeva, A., Zeng, H., Lam, R., Dong, A., Wu, X. H., Li, Y., Schapira, M., Vedadi, M., and Min, J. (2013) Crystal structures of the human histone H4K20 methyltransferases SUV420H1 and SUV420H2. FEBS Lett. 587, 3859-3868
33. Oda, H., Okamoto, I., Murphy, N., Chu, J., Price, S. M., Shen, M. M., Torres-Padilla, M. E., Heard, E., and Reinberg, D. (2009) Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol. Cell. Biol. 29, 2278-22795
34. McKay, D. J., Klusza, S., Penke, T. J., Meers, M. P., Curry, K. P., McDaniel, S. L., Malek P. Y., Cooper, S. W., Tatomer, D. C., Lieb, J. D., Strahl, B. D., Duronio, R. J., and Matera, A. G. (2015) Interrogating the function of metazoan histones using engineered gene clusters. Dev. Cell 32, 373-386
35. Shi, X., Kachirskaia, I., Yamaguchi, H., West, L. E., Wen, H., Wang, E. W., Dutta, S., Appella, E., and Gozani, O. (2007) Modulation of p53 function by SET8-mediated methylation at lysine 382. Mol. Cell 27, 636-646
36. Dhami, G. K., Liu, H., Galka, M., Voss, C., Wei, R., Muranko, K., Kaneko, T., Cregan, S. P., Li, L., and Li, S. S. (2013) Dynamic methylation of Numb by Set8 regulates its binding to p53 and apoptosis. Mol. Cell 50, 565-576
37. Takawa, M., Cho, H. S., Hayami, S., Toyokawa, G., Kogure, M., Yamane, Y., Iwai, Y., Maejima, K., Ueda, K., Masuda, A., Dohmae, N., Field, H. I., Tsunoda, T., Kobayashi, T., Akasu, T., Sugiyama, M., Ohnuma, S., Atomi, Y., Ponder, B. A., Nakamura, Y., and Hamamoto, R. (2012) Histone lysine methyltransferase SETD8 promotes carcinogenesis by deregulating PCNA expression. Cancer Res. 72, 3217-3227
38. Mosammaparast, N., and Shi, Y. (2010) Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu. Rev. Biochem. 79, 155-179
39. Feng, W., 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
40. Qi, H. H., Sarkissian, M., Hu, G. Q., Wang, Z., Bhattacharjee, A., Gordon, D. B., Gonzales, M., Lan, F., Ongusaha, P. P., Huarte, M., Yaghi, N. K., Lim, H., Garcia, B. A., Brizuela, L., Zhao, K., Roberts, T. M., and Shi, Y. (2010) Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466, 503-507
41. Liu, W., Tanasa, B., Tyurina, O. V., Zhou, T. Y., Gassmann, R., Liu, W. T., Ohgi, K. A., Benner, C., Garcia-Bassets, I., Aggarwal, A. K., Desai, A., Dorrestein, P. C., Glass, C. K., and Rosenfeld, M. G. (2010) PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression. Nature 466, 508-512
42. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120
43. Bannister, A. J., Zegerman, P., Partridge, J. F., Miska, E. A., Thomas, J. O., Allshire, R. C., and Kouzarides, T. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124
44. Hahn, M., Dambacher, S., Dulev, S., Kuznetsova, A. Y., Eck, S., Worz, S., Sadic, D., Schulte, M., Mallm, J. P., Maiser, A., Debs, P., von Melchner, H., Leonhardt, H., Schermelleh, L., Rohr, K., Rippe, K., Storchova, Z., and Schotta, G. (2013) Suv4-20h2 mediates chromatin compaction and is important for cohesin recruitment to heterochromatin. Genes Dev. 27, 859-872
45. Abbas, T., Shibata, E., Park, J., Jha, S., Karnani, N., and Dutta, A. (2010) CRL4 (Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell 40, 9-21
46. Centore, R. C., Havens, C. G., Manning, A. L., Li, J. M., Flynn, R. L., Tse, A., Jin, J., Dyson, N. J., Walter, J. C., and Zou, L. (2010) CRL4 (Cdt2) - mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell 40, 22-33
47. Jørgensen, S., Eskildsen, M., Fugger, K., Hansen, L., Larsen, M. S., Kousholt, A. N., Syljuåsen, R. G., Trelle, M. B., Jensen, O. N., Helin, K., and Sørensen, C. S. (2011) SET8 is degraded via PCNA-coupled CRL4 (CDT2) ubiquitylation in S phase and after UV irradiation. J. Cell Biol. 192, 43-54
48. Oda, H., Hübner, M. R., Beck, D. B., Vermeulen, M., Hurwitz, J., Spector, D. L., and Reinberg, D. (2010) Regulation of the histone H4 monomethylase PR-Set7 by CRL4 (Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 40, 364-376
49. Tardat, M., Brustel, J., Kirsh, O., Lefevbre, C., Callanan, M., Sardet, C., and Julien, E. (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 12, 1086-1093
50. Wu, S., Wang, W., Kong, X., Congdon, L. M., Yokomori, K., Kirschner, M. W., and Rice, J. C. (2010) Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev. 24, 2531-2542
51. Havens, C. G., and Walter, J. C. (2011) Mechanism of CRL4 (Cdt2), a PCNA-dependent E3 ubiquitin ligase. Genes Dev. 25, 1568-1582
52. Sanders, S. L., Portoso, M., Mata, J., Bähler, J., Allshire, R. C., and Kouzarides, T. (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603-614
53. Houston, S. I., McManus, K. J., Adams, M. M., Sims, J. K., Carpenter, P. B., Hendzel, M. J., and Rice, J. C. (2008) Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J. Biol. Chem. 283, 19478-19488
54. Musselman, C. A., Lalonde, M. E., Côté, J., and Kutateladze, T. G. (2012) Perceiving the epigenetic landscape through histone readers. Nat. Struct. Mol. Biol. 19, 1218-1227
55. Polo, S. E., and Jackson, S. P. (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25, 409-433
56. Botuyan, M. V., Lee, J., Ward, I. M., Kim, J. E., Thompson, J. R., Chen, J., and Mer, G. (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373
57. Greeson, N. T., Sengupta, R., Arida, A. R., Jenuwein, T., and Sanders, S. L. (2008) Di-methyl H4 lysine 20 targets the checkpoint protein Crb2 to sites of DNA damage. J. Biol. Chem. 283, 33168-33174
58. Tuzon, C. T., Spektor, T., Kong, X., Congdon, L. M., Wu, S., Schotta, G., Yokomori, K., and Rice, J. C. (2014) Concerted activities of distinct H4K20 methyltransferases at DNA double-strand breaks regulate 53BP1 nucleation and NHEJ-directed repair. Cell Rep. 8, 430-438
59. Arias, E. E., and Walter, J. C. (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518
60. Méchali, M., Yoshida, K., Coulombe, P., and Pasero, P. (2013) Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr. Opin. Genet. Dev. 23, 124-131
61. Tardat, M., Murr, R., Herceg, Z., Sardet, C., and Julien, E. (2007) PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J. Cell Biol. 179, 1413-1426
62. Jørgensen, S., Elvers, I., Trelle, M. B., Menzel, T., Eskildsen, M., Jensen, O. N., Helleday, T., Helin, K., and Sørensen, C. S. (2007) The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 179, 1337-1345
63. Lee, J., and Zhou, P. (2010) SETting the clock for histone H4 monomethylation. Mol. Cell 40, 345-346
64. Beck, D. B., Burton, A., Oda, H., Ziegler-Birling, C., Torres-Padilla, M. E., and Reinberg, D. (2012) The role of PR-Set7 in replication licensing depends on Suv4-20h. Genes Dev. 26, 2580-2589
65. Siddiqui, K., On, K. F., and Diffley, J. F. (2013) Regulating DNA replication in eukarya. Cold Spring Harb. Perspect. Biol. 5, a012930
66. Shen, Z., Sathyan, K. M., Geng, Y., Zheng, R., Chakraborty, A., Freeman, B., Wang, F., Prasanth, K. V., and Prasanth, S. G. (2010) A WD-repeat protein stabilizes ORC binding to chromatin. Mol. Cell 40, 99-111
67. Bicknell, L. S., Bongers, E. M., Leitch, A., Brown, S., Schoots, J., Harley, M. E., Aftimos, S., Al-Aama, J. Y., Bober, M., Brown, P. A., van Bokhoven, H., Dean, J., Edrees, A. Y., Feingold, M., Fryer, A., Hoefsloot, L. H., Kau, N., Knoers, N. V., Mackenzie, J., Opitz, J. M., Sarda, P., Ross, A., Temple, I. K., Toutain, A., Wise, C. A., Wright, M., and Jackson, A. P. (2011) Mutations in the pre-replication complex cause Meier-Gorlin syndrome. Nat. Genet. 43, 356-359
68. Bicknell, L. S., Walker, S., Klingseisen, A., Stiff, T., Leitch, A., Kerzendorfer, C., Martin, C. A., Yeyati, P., Al Sanna, N., Bober, M., Johnson, D., Wise, C., Jackson, A. P., O'Driscoll, M., and Jeggo, P. A. (2011) Mutations in ORC1, encoding the largest subunit of the origin recognition complex, cause microcephalic primordial dwarfism resembling Meier-Gorlin syndrome. Nat. Genet. 43, 350-355
69. Klingseisen, A., and Jackson, A. P. (2011) Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev. 25, 2011-2024
70. Guernsey, D. L., Matsuoka, M., Jiang, H., Evans, S., Macgillivray, C., Nightingale, M., Perry, S., Ferguson, M., LeBlanc, M., Paquette, J., Patry, L., Rideout, A. L., Thomas, A., Orr, A., McMaster, C. R., Michaud, J. L., Deal, C., Langlois, S., Superneau, D. W., Parkash, S., Ludman, M., Skidmore, D. L., and Samuels, M. E. (2011) Mutations in origin recognition complex gene ORC4 cause Meier-Gorlin syndrome. Nat. Genet. 43, 360-364
71. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007), High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837
72. Li, Y., Sun, L., Zhang, Y., D., Wang, Wang, F., Liang, J., Gui, B., and Shang, Y. (2011) The histone modifications governing TFF1 transcription mediated by estrogen receptor. J. Biol. Chem. 286, 13925-13936
73. Li, Z., Nie, F., Wang, S., and Li, L. (2011) Histone H4 Lys 20 monomethylation by histone methylase SET8 mediates Wnt target gene activation. Proc. Natl. Acad. Sci. U. S. A. 108, 3116-3123
74. Congdon, L. M., Houston, S. I., Veerappan, C. S., Spektor, T. M., and Rice, J. C. (2010) PR-Set7-mediated monomethylation of histone H4 lysine 20 at specific genomic regions induces transcriptional repression. J. Cell. Biochem. 110, 609-619
75. Karachentsev, D., Sarma, K., Reinberg, D., and Steward, R. (2005) PR-Set7-dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. Genes Dev. 19, 431-435
76. 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
77. Min, J., Allali-Hassani, A., Nady, N., Qi, C., Ouyang, H., Liu, Y., MacKenzie, F., Vedadi, M., and Arrowsmith, C. H. (2007) L3MBTL1 recognition of mono- and dimethylated histones. Nat. Struct. Mol. Biol. 14, 1229-1230
78. Trojer, P., Li, G., Sims, R. J., 3rd, Vaquero, A., Kalakonda, N., Boccuni, P., Lee, D., Erdjument-Bromage, H., Tempst, P., Nimer, S. D., Wang, Y. H., and Reinberg, D. (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129, 915-928
79. Scharf, A. N., Meier, K., Seitz, V., Kremmer, E., Brehm, A., and Imhof, A. (2009) Monomethylation of lysine 20 on histone H4 facilitates chromatin maturation. Mol. Cell. Biol. 29, 57-67
80. Benevento, M., Tonge, P. D., Puri, M. C., Nagy, A., Heck, A. J., and Munoz, J. (2015) Fluctuations in histone H4 isoforms during cellular reprogramming monitored by middle-down proteomics. Proteomics 15, 3219-3231
81. Pesavento, J. J., Bullock, C. R., LeDuc, R. D., Mizzen, C. A., and Kelleher, N. L. (2008) Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J. Biol. Chem. 283, 14927-14937
82. 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
83. Guo, Y., Nady, N., Qi, C., Allali-Hassani, A., Zhu, H., Pan, P., Adams-Cioaba, M. A., Amaya, M. F., Dong, A., Vedadi, M., Schapira, M., Read, R. J., Arrowsmith, C. H., and Min, J. (2009) Methylation-state-specific recognition of histones by the MBT repeat protein L3MBTL2. Nucleic Acids Res. 37, 2204-2210
84. Kim, D., Blus, B. J., Chandra, V., Huang, P., Rastinejad, F., and Khorasanizadeh, S. (2010) Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain. Nat. Struct. Mol. Biol. 17, 1027-1029
85. Wang, Y., Reddy, B., Thompson, J., Wang, H., Noma, K., Yates, J. R., 3rd, and Jia, S. (2009) Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol. Cell 33, 428-437
86. 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
87. Lee, J., Thompson, J. R., Botuyan, M. V., and Mer, G. (2008) Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor. Nat. Struct. Mol. Biol. 15, 109-111
88. Mallette, F. A., Mattiroli, F., Cui, G., Young, L. C., Hendzel, M. J., Mer, G., Sixma, T. K., and Richard, S. (2012) RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J. 31, 1865-1878
89. Hirano, Y., Hizume, K., Kimura, H., Takeyasu, K., Haraguchi, T., and Hiraoka, Y. (2012) Lamin B receptor recognizes specific modifications of histone H4 in heterochromatin formation. J. Biol. Chem. 287, 42654-42663
90. Chan, K. M., and Zhang, Z. (2012) Leucine-rich repeat and WD repeatcontaining protein 1 is recruited to pericentric heterochromatin by trimethylated lysine 9 of histone H3 and maintains heterochromatin silencing. J. Biol. Chem. 287, 15024-15033