A structural perspective on readout of epigenetic histone and DNA methylation marks

Cold Spring Harbor Perspectives in Biology

Volumn 8, Issue 3, 2016, Pages

  Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HOMEODOMAIN PROTEIN; LONG UNTRANSLATED RNA; NONHISTONE PROTEIN; NUCLEOSOME;

BIOLOGICAL MODEL; CHEMISTRY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENETICS; METABOLISM; METHYLATION; MOLECULAR MODEL; NUCLEOSOME; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN PROCESSING;

CHROMOSOMAL PROTEINS, NON-HISTONE; CPG ISLANDS; DNA METHYLATION; EPIGENOMICS; HISTONES; HOMEODOMAIN PROTEINS; METHYLATION; MODELS, GENETIC; MODELS, MOLECULAR; NUCLEOSOMES; PROTEIN DOMAINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, LONG NONCODING;

EID: 84959483542     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a018754     Document Type: Article

References (290)

1. Ali M, Yan K, Lalonde ME, Degerny C, Rothbart SB, Strahl BD, Cote J, Yang XJ, Kutateladze TG. 2012. Tandem PHD fingers of MORF/MOZ acetyltransferases display selectivity for acetylated histone H3 and are required for the association with chromatin. J Mol Biol 424: 328-338.
2. Allfrey VG, Faulkner R, Mirsky AE. 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci 51: 786-794.
3. Allis CD, Muir TW. 2011. Spreading chromatin into chemical biology. Chembiochem 12: 264-279.
4. Allis CD, Jeuwein T, Reinberg D. 2014. Overview and concepts. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a018739.
5. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23: 185-188.
6. Argentaro A, Yang JC, Chapman L, Kowalczyk MS, Gibbons RJ, Higgs DR, Neuhaus D, Rhodes D. 2007. Structural consequences of diseasecausing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc Natl Acad Sci 104: 11939-11944.
7. Arita K, Ariyoshi M, Tochio H, Nakamura Y, Shirakawa M. 2008. Recognition of hemi-methylatedDNA by the SRA protein UHRF1 by a baseflipping mechanism. Nature 455: 818-821.
8. Arita K, Isogai S, Oda T, Unoki M, Sugita K, Sekiyama N, Kuwata K, Hamamoto R, Tochio H, Sato M, et al. 2012. Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1. Proc Natl Acad Sci 109: 12950-12955.
9. Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE. 2011. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution. Science 334: 977-982.
10. Arrowsmith CH, Bountra C, Fish PV, Lee K, Schapira M. 2012. Epigenetic protein families: A new frontier for drug discovery. Nat Rev Drug Discov 11: 384-400.
11. Avvakumov GV, Walker JR, Xue S, Li Y, Duan S, Bronner C, Arrowsmith CH, Dhe-Paganon S. 2008. Structural basis for recognition of hemimethylated DNA by the SRA domain of human UHRF1. Nature 455: 822-825.
12. Ballare C, Lange M, Lapinaite A, Martin GM, Morey L, Pascual G, Liefke R, Simon B, Shi Y, Gozani O, et al. 2012. Phf19 links methylated Lys36 of histone H3 to regulation of Polycomb activity. Nat Struct Mol Biol 19: 1257-1265.
13. Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Res 21: 381-395.
14. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, Luger K, Kaye KM. 2006. The nucleosomal surface as a docking station for Kaposi’s sarcoma herpesvirus LANA. Science 311: 856-861.
15. Barlow DP, Bartolomei MS. 2014. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 6: a018382.
16. Bartke T, Vermeulen M, Xhemalce B, Robson SC, Mann M, Kouzarides T. 2010. Nucleosome-interacting proteins regulated byDNA and histone methylation. Cell 143: 470-484.
17. Baylin SB, Jones PA. 2011. Adecade of exploring the cancer epigenome— Biological and translational implications. Nat Rev Cancer 11: 726-734.
18. Baylin SB, Jones PA. 2014. Epigenetic determinants of cancer. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019505.
19. Becker PB, Workman JL. 2013. Nucleosome remodeling and epigenetics. Cold Spring Harb Perspect Biol 5: a017905.
20. Bedford MT, Clarke SG. 2009. Protein arginine methylation in mammals: Who, what, and why. Mol Cell 33: 1-13.
21. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
22. Bhutani N, Burns DM, Blau HM. 2011. DNA demethylation dynamics. Cell 146: 866-872.
23. Bian C, Xu C, Ruan J, Lee KK, Burke TL, Tempel W, Barsyte D, Li J, Wu M, Zhou BO, et al. 2011. Sgf29 binds histone H3K4me2/3 and is required for SAGA complex recruitment and histone H3 acetylation. EMBO J 30: 2829-2842.
24. Bicknell LS, Walker S, Klingseisen A, Stiff T, Leitch A, Kerzendorfer C, Martin CA, Yeyati P, Al Sanna N, Bober M, et al. 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.
25. Bienz M. 2006. The PHD finger, a nuclear protein-interaction domain. Trends Biochem Sci 31: 35-40.
26. Black JC, Van Rechem C, Whetstine JR. 2012. Histone lysine methylation dynamics: Establishment, regulation, and biological impact. Mol Cell 48: 491-507.
27. Bonasio R, Lecona E, Reinberg D. 2010. MBT domain proteins in development and disease. Semin Cell Dev Biol 21: 221-230.
28. Booth MJ, Branco MR, Ficz G, Oxley D, Krueger F, Reik W, Balasubramanian S. 2012. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336: 934-937.
29. Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, Jacobsen SE. 2007. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760-1764.
30. Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J, 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.
31. Brahms H, Meheus L, de Brabandere V, Fischer U, Luhrmann R. 2001. Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B′ and the Sm-like protein LSm4, and their interactionwith the SMN protein. RNA 7: 1531-1542.
32. Branco MR, Ficz G, Reik W. 2012. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13: 7-13.
33. Brehm A, Tufteland KR, Aasland R, Becker PB. 2004. The many colours of chromodomains. Bioessays 26: 133-140.
34. Brien GL, Gambero G, O’Connell DJ, Jerman E, Turner SA, Egan CM, Dunne EJ, Jurgens MC, Wynne K, Piao L, et al. 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.
35. Brockdorff N, Turner BM. 2014. Dosage compensation in mammals. Cold Spring Harb Perspect Biol 10.1101/cshperspect.a019406.
36. Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF. 1991. A gene from the region of the human X inactivation centre is expressed exclusively fromthe inactive X chromosome. Nature 349: 38-44.
37. Bua DJ, Kuo AJ, Cheung P, Liu CL, Migliori V, Espejo A, Casadio F, Bassi C, Amati B, Bedford MT, et al. 2009. Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. PLoS One 4: e6789.
38. Buck-Koehntop BA, Stanfield RL, Ekiert DC, Martinez-Yamout MA, Dyson HJ, Wilson IA, Wright PE. 2012. Molecular basis for recognition of methylated and specific DNA sequences by the zinc finger protein Kaiso. Proc Natl Acad Sci 109: 15229-15234.
39. Busslinger M, Tarakhovsky A. 2014. Epigenetic control of immunity. Cold Spring Harb Perspect Biol 6: a019307.
40. Cai L, Rothbart SB, Lu R, Xu B, Chen WY, Tripathy A, Rockowitz S, Zheng D, Patel DJ, Allis CD, Strahl BD, et al. 2013. An H3K36 methylationengaging Tudor motif of Polycomb-like proteins mediates PRC2 complex targeting. Mol Cell 49: 571-582.
41. Callebaut I, Courvalin JC, Mornon JP. 1999. The BAH (bromo-adjacent homology) domain: A link betweenDNA methylation, replication and transcriptional regulation. FEBS Lett 446: 189-193.
42. Cedar H, Bergman Y. 2009. Linking DNA methylation and histone modification: Patterns and paradigms. Nat Rev Genet 10: 295-304.
43. Chatterjee C, McGinty RK, Fierz B, Muir TW. 2010. Disulfide-directed histone ubiquitylation reveals plasticity in hDot1L activation. Nat Chem Biol 6: 267-269.
44. Chen J, Santillan DA, Koonce M, Wei W, Luo R, Thirman MJ, Zeleznik-Le NJ, Diaz MO. 2008. Loss of MLL PHD finger 3 is necessary for MLLENL-induced hematopoietic stem cell immortalization. Cancer Res 68: 6199-6207.
45. Chen C, Nott TJ, Jin J, Pawson T. 2011. Deciphering arginine methylation: Tudor tells the tale. Nat Rev Mol Cell Biol 12: 629-642.
46. Cheng X. 2014. Structural and functional coordination of DNA and histone methylation. Cold Spring Harb Perspect Biol 6: a018747.
47. Cheng J, Yang Y, Fang J, Xiao J, Zhu T, Chen F, Wang P, Li Z, Yang H, Xu Y. 2013. Structural insight into coordinated recognition of H3K9me3 by the plant homeodomain (PHD) and tandem tudor domain (TTD) of the UHRF1 (ubiquitin-like, containing PHD and RING finger domains, 1) protein. J Biol Chem 288: 1329-1339.
48. Chi P, Allis CD, Wang GG. 2010. Covalent histone modifications—Miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 10: 457-469.
49. Chignola F, Gaetani M, Rebane A, Org T, Mollica L, Zucchelli C, Spitaleri A, Mannella V, Peterson P, Musco G. 2009. The solution structure of the first PHD finger of autoimmune regulator in complex with nonmodified histone H3 tail reveals the antagonistic role of H3R2 methylation. Nucleic Acids Res 37: 2951-2961.
50. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
51. Clouaire T, Stancheva I. 2008.Methyl-CpG binding proteins: Specialized transcriptional repressors or structural components of chromatin? Cell Mol Life Sci 65: 1509-1522.
52. Collins RE, Northrop JP, Horton JR, Lee DY, Zhang X, Stallcup MR, Cheng X. 2008. The ankyrin repeats of G9a and GLP histone methyltransferases are mono-and dimethyllysine binding modules. Nat Struct Mol Biol 15: 245-250.
53. Couture JF, Collazo E, Trievel RC. 2006. Molecular recognition of histone H3 by the WD40 protein WDR5. Nat Struct Mol Biol 13: 698-703.
54. Davis L, Chin JW. 2012. Designer proteins: Applications of genetic code expansion in cell biology. Nat Rev Mol Cell Biol 13: 168-182.
55. Dawson PE, Kent SB. 2000. Synthesis of native proteins by chemical ligation. Annu Rev Biochem 69: 923-960.
56. Dawson MA, Kouzarides T. 2012. Cancer epigenetics: From mechanism to therapy. Cell 150: 12-27.
57. Dawson MA, Bannister AJ, Gottgens B, Foster SD, Bartke T, Green AR, Kouzarides T. 2009. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 461: 819-822.
58. Dekker J, Misteli T. 2014. Long-range chromatin interactions. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019356.
59. Dou Y, Milne TA, Tackett AJ, Smith ER, Fukuda A, Wysocka J, Allis CD, Chait BT, Hess JL, Roeder RG. 2005. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121: 873-885.
60. Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, Vashisht AA, Terragni J, Chin HG, Tu A, et al. 2012. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151: 167-180.
61. Duncker BP, Chesnokov IN, McConkey BJ. 2009. The origin recognition complex protein family. Genome Biol 10: 214.
62. Elgin SC, Reuter G. 2013. Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila. Cold SpringHarb Perspect Biol 5: a017780.
63. Eustermann S, Yang JC, Law MJ, Amos R, Chapman LM, Jelinska C, Garrick D, Clynes D, Gibbons RJ, Rhodes D, et al. 2011.Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat Struct Mol Biol 18: 777-782.
64. Fair K, Anderson M, Bulanova E, Mi H, Tropschug M, Diaz MO. 2001. Protein interactions of the MLL PHD fingers modulate MLL target gene regulation in human cells. Mol Cell Biol 21: 3589-3597.
65. Falk S, Ravaud S, Koch J, Sinning I. 2010. The C terminus of the Alb3 membrane insertase recruits cpSRP43 to the thylakoid membrane. J Biol Chem 285: 5954-5962.
66. Fiedler M, Sanchez-Barrena MJ, Nekrasov M, Mieszczanek J, Rybin V, Muller J, Evans P, Bienz M. 2008. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol Cell 30: 507-518.
67. Fierz B, Muir TW. 2012. Chromatin as an expansive canvas for chemical biology. Nat Chem Biol 8: 417-427.
68. Fischle W, Wang Y, Allis CD. 2003a. Binary switches and modification cassettes in histone biology and beyond. Nature 425: 475-479.
69. Fischle W, Wang Y, Allis CD. 2003b. Histone and chromatin cross-talk. Curr Opin Cell Biol 15: 172-183.
70. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J, Hunt DF, Funabiki H, Allis CD. 2005. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438: 1116-1122.
71. Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F, Khorasanizadeh S. 2005. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181-1185.
72. Frederiks F, Stulemeijer IJ, Ovaa H, van Leeuwen F. 2011. A modified epigenetics toolbox to study histone modifications on the nucleosome core. Chembiochem 12: 308-313.
73. Fuchs SM, Krajewski K, Baker RW, Miller VL, Strahl BD. 2011. Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr Biol 21: 53-58.
74. Gardner KE, Allis CD, Strahl BD. 2011. Operating on chromatin, a colorful language where context matters. J Mol Biol 409: 36-46.
75. Garske AL, Oliver SS, Wagner EK, Musselman CA, LeRoy G, Garcia BA, Kutateladze TG, Denu JM. 2010. Combinatorial profiling of chromatin binding modules reveals multisite discrimination. Nat Chem Biol 6: 283-290.
76. Goforth RL, Peterson EC, Yuan J, Moore MJ, Kight AD, Lohse MB, Sakon J, Henry RL. 2004. Regulation of the GTPase cycle in post-translational signal recognition particle-based protein targeting involves cpSRP43. J Biol Chem 279: 43077-43084.
77. Goodwin GH, Nicolas RH. 2001. The BAH domain, polybromo and the RSC chromatin remodelling complex. Gene 268: 1-7.
78. Greer EL, Shi Y. 2012. Histone methylation: A dynamic mark in health, disease and inheritance. Nat Rev Genet 13: 343-357.
79. Grimm C, Matos R, Ly-Hartig N, Steuerwald U, Lindner D, Rybin V, Muller J, Muller CW. 2009. Molecular recognition of histone lysine methylation by the Polycomb group repressor dSfmbt. EMBO J 28: 1965-1977.
80. Grossniklaus U, Paro R. 2014. Transcriptional silencing by Polycombgroup proteins. Cold Spring Harb Perspect Biol 6: a019331.
81. Grow EJ, Wysocka J. 2010. Flipping MLL1’s switch one proline at a time. Cell 141: 1108-1110.
82. Grunstein M, Gasser SM. 2013. Epigenetics in Saccharomyces cerevisiae. Cold Spring Harb Perspect Biol 5: a017491.
83. Guccione E, Bassi C, Casadio F, Martinato F, Cesaroni M, Schuchlautz H, Luscher B, Amati B. 2007. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449: 933-937.
84. Guil S, Esteller M. 2012. Cis-acting noncoding RNAs: Friends and foes. Nat Struct Mol Biol 19: 1068-1075.
85. Guo Y, Nady N, Qi C, Allali-Hassani A, Zhu H, Pan P, Adams-Cioaba MA, Amaya MF, Dong A, Vedadi M, et al. 2009. Methylation-state-specific recognition of histones by the MBTrepeat protein L3MBTL2. Nucleic Acids Res 37: 2204-2210.
86. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, et al. 2010. Long non-codingRNAHOTAIRreprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076.
87. Guttman M, Rinn JL. 2012. Modular regulatory principles of large noncoding RNAs. Nature 482: 339-346.
88. Han Z, Guo L, Wang H, Shen Y, Deng XW, Chai J. 2006. Structural basis for the specific recognition of methylated histone H3 lysine 4 by the WD-40 protein WDR5. Mol Cell 22: 137-144.
89. Hashimoto H, Horton JR, Zhang X, Bostick M, Jacobsen SE, Cheng X. 2008. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455: 826-829.
90. Hashimoto H, Horton JR, Zhang X, Cheng X. 2009. UHRF1, a modular multi-domain protein, regulates replication-coupled crosstalk between DNA methylation and histone modifications. Epigenetics 4: 8-14.
91. Hashimoto H, Zhang X, Cheng X. 2012. Excision of thymine and 5-hydroxymethyluracil by the MBD4 DNA glycosylase domain: Structural basis and implications for active DNA demethylation. Nucleic Acids Res 40: 8276-8284.
92. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, et al. 2011. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307.
93. Henikoff S, Smith MM. 2014. Histone variants and epigenetics. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019364.
94. Herold JM, Ingerman LA, Gao C, Frye SV. 2011a. Drug discovery toward antagonists of methyl-lysine binding proteins. Curr Chem Genomics 5: 51-61.
95. Herold JM, Wigle TJ, Norris JL, Lam R, Korboukh VK, Gao C, Ingerman LA, Kireev DB, Senisterra G, Vedadi M, et al. 2011b. Small-molecule ligands of methyl-lysine binding proteins. J Med Chem 54: 2504-2511.
96. Hirota T, Lipp JJ, Toh BH, Peters JM. 2005. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438: 1176-1180.
97. Ho KL, McNae IW, Schmiedeberg L, Klose RJ, Bird AP, Walkinshaw MD. 2008. MeCP2 binding to DNA depends upon hydration at methyl-CpG. Mol Cell 29: 525-531.
98. Holdermann I, Meyer NH, Round A, Wild K, Sattler M, Sinning I. 2012. Chromodomains read the arginine code of post-translational targeting. Nat Struct Mol Biol 19: 260-263.
99. Hom RA, Chang PY, Roy S, Musselman CA, Glass KC, Selezneva AI, Gozani O, Ismagilov RF, Cleary ML, Kutateladze TG. 2010.Molecular mechanism of MLL PHD3 and RNA recognition by the Cyp33 RRM domain. J Mol Biol 400: 145-154.
100. Hossain M, Stillman B. 2012. Meier-Gorlin syndrome mutations disrupt an Orc1 CDK inhibitory domain and cause centrosome reduplication. Genes Dev 26: 1797-1810.
101. Hou Z, Bernstein DA, Fox CA, Keck JL. 2005. Structural basis of the Sir1-origin recognition complex interaction in transcriptional silencing. Proc Natl Acad Sci 102: 8489-8494.
102. Hsu HC, Stillman B, Xu RM. 2005. Structural basis for origin recognition complex 1 protein-silence information regulator 1 protein interaction in epigenetic silencing. Proc Natl Acad Sci 102: 8519-8524.
103. Hu L, Li Z, Wang P, Lin Y, Xu Y. 2011. Crystal structure of PHD domain of UHRF1 and insights into recognition of unmodified histone H3 arginine residue 2. Cell Res 21: 1374-1378.
104. Huang Y, Fang J, Bedford MT, Zhang Y, Xu RM. 2006. Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312: 748-751.
105. Huang R, Holbert MA, Tarrant MK, Curtet S, Colquhoun DR, Dancy BM, Dancy BC, Hwang Y, Tang Y, Meeth K, et al. 2010. Site-specific introduction of an acetyl-lysine mimic into peptides and proteins by cysteine alkylation. J Am Chem Soc 132: 9986-9987.
106. Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, Simon MD, Kutateladze TG, Gozani O. 2009. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell 33: 248-256.
107. Huyen Y, Zgheib O, Ditullio RA Jr., Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432: 406-411.
108. Hyllus D, Stein C, Schnabel K, Schiltz E, Imhof A, Dou Y, Hsieh J, Bauer UM. 2007. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev 21: 3369-3380.
109. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303.
110. Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, Psulkowski E, Fredericks WJ, White DE, Maul GG, et al. 2007. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 28: 823-837.
111. Iwase S, Xiang B, Ghosh S, Ren T, Lewis PW, Cochrane JC, Allis CD, Picketts DJ, Patel DJ, Li H, et al. 2011. ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat Struct Mol Biol 18: 769-776.
112. Jackson JP, Lindroth AM, Cao X, Jacobsen SE. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556-560.
113. Jacobs SA, Khorasanizadeh S. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083.
114. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, Eissenberg JC, Allis CD, Khorasanizadeh S. 2001. Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J 20: 5232-5241.
115. Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293: 1074-1080.
116. Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, Schulick RD, Tang LH, Wolfgang CL, Choti MA, et al. 2011. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331: 1199-1203.
117. Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, Jacobsen SE. 2007. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17: 379-384.
118. Jones PA. 2012. Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492.
119. Jones PA, Liang G. 2009. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 10: 805-811.
120. Kan PY, Caterino TL, Hayes JJ. 2009. The H4 tail domain participates in intra-and internucleosome interactionswith protein andDNAduring folding and oligomerization of nucleosome arrays. Mol Cell Biol 29: 538-546.
121. Khorasanizadeh S. 2011. Recognition of methylated histones: New twists and variations. Curr Opin Struct Biol 21: 744-749.
122. Kim WY, Sharpless NE. 2006. The regulation of INK4/ARF in cancer and aging. Cell 127: 265-275.
123. Kim D, Blus BJ, Chandra V, Huang P, Rastinejad F, Khorasanizadeh S. 2010. Corecognition of DNA and a methylated histone tail by the MSL3 chromodomain. Nat Struct Mol Biol 17: 1027-1029.
124. Kireev D, Wigle TJ, Norris-Drouin J, Herold JM, Janzen WP, Frye SV. 2010. Identification of non-peptide malignant brain tumor (MBT) repeat antagonists by virtual screening of commercially available compounds. J Med Chem 53: 7625-7631.
125. Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Bahler J, Green RD, Kouzarides T. 2007. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449: 928-932.
126. Klingseisen A, Jackson AP. 2011. Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev 25: 2011-2024.
127. Klose RJ, Bird AP. 2006. Genomic DNA methylation: The mark and its mediators. Trends Biochem Sci 31: 89-97.
128. Koga H, Matsui S, Hirota T, Takebayashi S, Okumura K, Saya H. 1999. A human homolog of Drosophila lethal(3)malignant brain tumor (l(3)mbt) protein associates with condensed mitotic chromosomes. Oncogene 18: 3799-3809.
129. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
130. Kouzarides T, Berger SL. 2007. Chromatin modifications and their mechanism. In Epigenetics (ed. Allis CD, Jenuwen T, Reinberg D), pp. 191-209. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
131. Kriaucionis S, Heintz N. 2009. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930.
132. Kriaucionis S, Tahiliani M. 2014. Expanding the epigenetic landscape: Novel modifications of cytosine in genomic DNA. Cold Spring Harb Perspect Biol 6: a018630.
133. Kugel JF, Goodrich JA. 2012. Non-coding RNAs: Key regulators of mammalian transcription. Trends Biochem Sci 37: 144-151.
134. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, Patel DJ, Gozani O. 2012. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484: 115-119.
135. Lan F, Collins RE, De Cegli R, Alpatov R, Horton JR, Shi X, Gozani O, Cheng X, Shi Y. 2007. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448: 718-722.
136. Latham JA, Dent SY. 2007. Cross-regulation of histone modifications. Nat Struct Mol Biol 14: 1017-1024.
137. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-220.
138. Law JA, Du J, Hale CJ, Feng S, Krajewski K, Palanca AM, Strahl BD, Patel DJ, Jacobsen SE. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498: 385-389.
139. Lee JT. 2012. Epigenetic regulation by long noncodingRNAs. Science 338: 1435-1439.
140. Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, Bhaumik SR, Shilatifard A. 2007. Histone cross talk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131: 1084-1096.
141. Lee J, Thompson JR, Botuyan MV, 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.
142. Li E, Bird A. 2007. DNA methylation in mammals. In Epigenetics (ed. Allis CD, Jenuwen T, Reinberg D), pp. 341-356. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
143. Li E, Zhang Y. 2014. DNA methylation in mammals. Cold Spring Harb Perspect Biol 6: a019133.
144. Li H, Ilin S, Wang W, Duncan EM, Wysocka J, Allis CD, Patel DJ. 2006. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442: 91-95.
145. Li H, Fischle W, Wang W, Duncan EM, Liang L, Murakami-Ishibe S, Allis CD, Patel DJ. 2007a. Structural basis for lower lysine methylation statespecific readout by MBTrepeats of L3MBTL1 and an engineered PHD finger. Mol Cell 28: 677-691.
146. Li X, Lee YK, Jeng JC, Yen Y, Schultz DC, Shih HM, Ann DK. 2007b. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J Biol Chem 282: 36177-36189.
147. Liu CC, Schultz PG. 2010. Adding new chemistries to the genetic code. Annu Rev Biochem 79: 413-444.
148. Liu H, Wang JY, Huang Y, Li Z, Gong W, Lehmann R, Xu RM. 2010a. Structural basis for methylarginine-dependent recognition of Aubergine by Tudor. Genes Dev 24: 1876-1881.
149. Liu K, Chen C, Guo Y, Lam R, Bian C, Xu C, Zhao DY, Jin J, MacKenzie F, Pawson T, et al. 2010b. Structural basis for recognition of arginine methylated Piwi proteins by the extended Tudor domain. Proc Natl Acad Sci 107: 18398-18403.
150. Liu Y, Toh H, Sasaki H, Zhang X, Cheng X. 2012. An atomic model of Zfp57 recognition of CpG methylation within a specific DNA sequence. Genes Dev 26: 2374-2379.
151. Lopes EC, Valls E, Figueroa ME, Mazur A, Meng FG, Chiosis G, Laird PW, Schreiber-Agus N, Greally JM, Prokhortchouk E, et al. 2008. Kaiso contributes to DNA methylation-dependent silencing of tumor suppressor genes in colon cancer cell lines. Cancer Res 68: 7258-7263.
152. Lucchesi JC, Kuroda MI. 2014. Dosage compensation in Drosophila. Cold Spring Harb Perspect Biol 6: a019398.
153. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
154. Luger K, Dechassa ML, Tremethick DJ. 2012. New insights into nucleosome and chromatin structure: An ordered state or a disordered affair? Nat Rev Mol Cell Biol 13: 436-447.
155. Ma JC, Dougherty DA. 1997. The Cation-p interaction. Chem Rev 97: 1303-1324.
156. Makde RD, England JR, Yennawar HP, Tan S. 2010. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467: 562-566.
157. Marazzi I, Ho JS, Kim J, Manicassamy B, Dewell S, Albrecht RA, Seibert CW, Schaefer U, Jeffrey KL, Prinjha RK, et al. 2012. Suppression of the antiviral response by an influenza histone mimic. Nature 483: 428-433.
158. Marmorstein R, Zhou M-M. 2014. Writers and readers of histone acetylation: Structure, mechanism, and inhibition. Cold Spring Harb Perspect Biol 6: a018762.
159. Martienssen R, Moazed D. 2014. RNAi and heterochromatin assembly. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019323.
160. Mathioudakis N, Palencia A, Kadlec J, Round A, Tripsianes K, Sattler M, Pillai RS, Cusack S. 2012. The multiple Tudor domain-containing protein TDRD1 is a molecular scaffold for mouse Piwi proteins and piRNA biogenesis factors. RNA 18: 2056-2072.
161. Matthews AG, Kuo AJ, Ramon-Maiques S, Han S, Champagne KS, Ivanov D, Gallardo M, Carney D, Cheung P, Ciccone DN, et al. 2007. RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450: 1106-1110.
162. Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP. 2003. The Tudor domain ‘Royal Family’: Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 28: 69-74.
163. McGinty RK, Kim J, Chatterjee C, Roeder RG, Muir TW. 2008. Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453: 812-816.
164. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, et al. 2008. Genomescale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-770.
165. Migliori V, Muller J, Phalke S, Low D, Bezzi M, Mok WC, Sahu SK, Gunaratne J, Capasso P, Bassi C, et al. 2012. Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat Struct Mol Biol 19: 136-144.
166. Miller TC, Rutherford TJ, Johnson CM, Fiedler M, Bienz M. 2010. Allosteric remodelling of the histone H3 binding pocket in the Pygo2 PHD finger triggered by its binding to the B9L/BCL9 co-factor. J Mol Biol 401: 969-984.
167. Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL. 2002. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 10: 1107-1117.
168. Milne TA, Kim J, Wang GG, Stadler SC, Basrur V, Whitcomb SJ, Wang Z, Ruthenburg AJ, Elenitoba-Johnson KS, Roeder RG, et al. 2010. Multiple interactions recruit MLL1 and MLL1 fusion proteins to the HOXA9 locus in leukemogenesis. Mol Cell 38: 853-863.
169. Min J, Zhang Y, Xu RM. 2003. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823-1828.
170. Min J, Allali-Hassani A, Nady N, Qi C, Ouyang H, Liu Y, MacKenzie F, Vedadi M, Arrowsmith CH. 2007. L3MBTL1 recognition of monoand dimethylated histones. Nat Struct Mol Biol 14: 1229-1230.
171. Moazed D. 2009. Small RNAs in transcriptional gene silencing and genome defence. Nature 457: 413-420.
172. Musselman CA, Kutateladze TG. 2011. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res 39: 9061-9071.
173. Musselman CA, Avvakumov N, Watanabe R, Abraham CG, Lalonde ME, Hong Z, Allen C, Roy S, Nunez JK, Nickoloff J, et al. 2012a.Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1. Nat Struct Mol Biol 19: 1266-1272.
174. Musselman CA, Lalonde ME, Cote J, Kutateladze TG. 2012b. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol 19: 1218-1227.
175. Musselman CA, Ramirez J, Sims JK, Mansfield RE, Oliver SS, Denu JM, Mackay JP, Wade PA, Hagman J, Kutateladze TG. 2012c. Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc Natl Acad Sci 109: 787-792.
176. Nady N, Lemak A, Walker JR, Avvakumov GV, Kareta MS, Achour M, Xue S, Duan S, Allali-Hassani A, Zuo X, et al. 2011. Recognition of multivalent histone states associated with heterochromatin by UHRF1 protein. J Biol Chem 286: 24300-24311.
177. Nady N, Krichevsky L, Zhong N, Duan S, Tempel W, Amaya MF, Ravichandran M, Arrowsmith CH. 2012. Histone recognition by human malignant brain tumor domains. J Mol Biol 423: 702-718.
178. Nakamura Y, Umehara T, Hamana H, Hayashizaki Y, Inoue M, Kigawa T, Shirouzu M, Terada T, Tanaka A, Padmanabhan B, et al. 2007. Crystal structure analysis of the PHD domain of the transcription co-activator Pygopus. J Mol Biol 370: 80-92.
179. Nakamura T, Liu YJ, Nakashima H, Umehara H, Inoue K, Matoba S, Tachibana M, Ogura A, Shinkai Y, Nakano T. 2012. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486: 415-419.
180. Neumann H, Wang K, Davis L, Garcia-Alai M, Chin JW. 2010. Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 464: 441-444.
181. Ng HH, Xu RM, Zhang Y, Struhl K. 2002. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 277: 34655-34657.
182. Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV, Laue ED. 2002. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416: 103-107.
183. Ohki I, Shimotake N, Fujita N, Jee J, Ikegami T, Nakao M, Shirakawa M. 2001. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105: 487-497.
184. Oliver SS, Denu JM. 2011. Dynamic interplay between histone H3 modifications and protein interpreters: Emerging evidence for a ‘histone language’. Chembiochem 12: 299-307.
185. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, et al. 2007. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717.
186. Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M, Shirakawa M. 2009. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep 10: 1235-1241.
187. Park S, Osmers U, Raman G, Schwantes RH, Diaz MO, Bushweller JH. 2010. The PHD3 domain of MLL acts as a CYP33-regulated switch between MLL-mediated activation and repression. Biochemistry 49: 6576-6586.
188. Pascual J, Martinez-Yamout M, Dyson HJ, Wright PE. 2000. Structure of the PHD zinc finger from human Williams-Beuren syndrome transcription factor. J Mol Biol 304: 723-729.
189. Patel A, Dharmarajan V, Cosgrove MS. 2008. Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. J Biol Chem 283: 32158-32161.
190. Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R, Kutateladze TG. 2006. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442: 100-103.
191. Peng J, Wysocka J. 2008. It takes a PHD to SUMO. Trends Biochem Sci 33: 191-194.
192. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. 1996. Requirement for Xist in X chromosome inactivation. Nature 379: 131-137.
193. Pikaard CS, Mittelsten Scheid O. 2014. Epigenetic regulation in plants. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019315.
194. Qi J. 2014. Bromodomain and extraterminal domain inhibitors (BETi) for cancer therapy: Chemical modulation of chromatin structure. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a018663.
195. Qiu C, Sawada K, Zhang X, Cheng X. 2002. The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat Struct Biol 9: 217-224.
196. Qiu Y, Liu L, Zhao C, Han C, Li F, Zhang J, Wang Y, Li G, Mei Y, Wu M, et al. 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.
197. Rajakumara E, Law JA, Simanshu DK, Voigt P, Johnson LM, Reinberg D, Patel DJ, Jacobsen SE. 2011a. A dual flip-out mechanism for 5mC recognition by the Arabidopsis SUVH5 SRA domain and its impact on DNA methylation and H3K9 dimethylation in vivo. Genes Dev 25: 137-152.
198. Rajakumara E, Wang Z, Ma H, Hu L, Chen H, Lin Y, Guo R, Wu F, Li H, Lan F, et al. 2011b. PHD finger recognition of unmodified histone H3R2 links UHRF1 to regulation of euchromatic gene expression. Mol Cell 43: 275-284.
199. Ram O, Goren A, Amit I, Shoresh N, Yosef N, Ernst J, Kellis M, Gymrek M, Issner R, Coyne M, et al. 2011. Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 147: 1628-1639.
200. Ramon-Maiques S, Kuo AJ, Carney D, Matthews AG, Oettinger MA, Gozani O, Yang W. 2007. The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2. Proc Natl Acad Sci 104: 18993-18998.
201. Reik W, Surani MA. 2014. Germline and pluripotent stem cells. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019422.
202. Rinn JL. 2014. lncRNAs: Linking RNA to chromatin. Cold Spring Harb Perspect Biol 6: a018614.
203. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
204. Robertson KD. 2005. DNA methylation and human disease. Nat Rev Genet 6: 597-610.
205. Rothbart SB, Krajewski K, Nady N, Tempel W, Xue S, Badeaux AI, Barsyte-Lovejoy D, Martinez JY, Bedford MT, Fuchs SM, et al. 2012. Association of UHRF1with methylated H3K9 directs the maintenance of DNA methylation. Nat Struct Mol Biol 19: 1155-1160.
206. Roy S, Musselman CA, Kachirskaia I, Hayashi R, Glass KC, Nix JC, Gozani O, Appella E, Kutateladze TG. 2010. Structural insight into p53 recognition by the 53BP1 tandem Tudor domain. J Mol Biol 398: 489-496.
207. Ruthenburg AJ, Wang W, Graybosch DM, Li H, Allis CD, Patel DJ, Verdine GL. 2006. Histone H3 recognition and presentation by theWDR5 module of the MLL1 complex. Nat Struct Mol Biol 13: 704-712.
208. Ruthenburg AJ, Allis CD, Wysocka J. 2007a. Methylation of lysine 4 on histone H3: Intricacy of writing and reading a single epigenetic mark. Mol Cell 25: 15-30.
209. Ruthenburg AJ, Li H, Patel DJ, Allis CD. 2007b.Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8: 983-994.
210. Ruthenburg AJ, Li H, Milne TA, Dewell S, McGinty RK, Yuen M, Ueberheide B, Dou Y, Muir TW, Patel DJ, et al. 2011. Recognition of amononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 145: 692-706.
211. Sampath SC, Marazzi I, Yap KL, Krutchinsky AN, Mecklenbrauker I, Viale A, Rudensky E, Zhou MM, Chait BT, Tarakhovsky A. 2007. Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol Cell 27: 596-608.
212. Sanchez R, Zhou MM. 2011. The PHD finger: A versatile epigenome reader. Trends Biochem Sci 36: 364-372.
213. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T. 2002. Active genes are trimethylated at K4 of histone H3. Nature 419: 407-411.
214. Sarg B, Helliger W, Talasz H, Koutzamani E, Lindner HH. 2004. Histone H4 hyperacetylation precludes histone H4 lysine 20 trimethylation. J Biol Chem 279: 53458-53464.
215. Sasai N, Nakao M, Defossez PA. 2010. Sequence-specific recognition of methylated DNA by human zinc-finger proteins. Nucleic Acids Res 38: 5015-5022.
216. Sathyamurthy A, Allen MD, Murzin AG, Bycroft M. 2003. Crystal structure of the malignant brain tumor (MBT) repeats in Sex Comb on Midleg-like 2 (SCML2). J Biol Chem 278: 46968-46973.
217. Schaefer U. 2014. Pharmacological inhibition of bromodomain-containing proteins in inflammation. Cold Spring Harb Perspect Biol 6: a018671.
218. Schalch T, Job G, Noffsinger VJ, Shanker S, Kuscu C, Joshua-Tor L, Partridge JF. 2009. High-affinity binding of Chp1 chromodomain to K9 methylated histone H3 is required to establish centromeric heterochromatin. Mol Cell 34: 36-46.
219. Schuetz A, Allali-Hassani A, Martin F, Loppnau P, Vedadi M, Bochkarev A, Plotnikov AN, Arrowsmith CH, Min J. 2006. Structural basis for molecular recognition and presentation of histone H3 by WDR5. EMBO J 25: 4245-4252.
220. Selenko P, Sprangers R, Stier G, Buhler D, Fischer U, Sattler M. 2001. SMN tudor domain structure and its interactionwith the Sm proteins. Nat Struct Biol 8: 27-31.
221. Serganov A, Patel DJ. 2012. Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 41: 343-370.
222. Seto E, Yoshida M. 2014. Erasers of histone acetylation: The histone deacetylase enzymes. Cold Spring Harb Perspect Biol 6: a018713.
223. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, et al. 2007. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450: 908-912.
224. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, et al. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96-99.
225. Shilatifard A. 2006. Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269.
226. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. 2006. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311: 844-847.
227. Simon MD, Chu F, Racki LR, de la Cruz CC, Burlingame AL, Panning B, Narlikar GJ, Shokat KM. 2007. The site-specific installation of methyllysine analogs into recombinant histones. Cell 128: 1003-1012.
228. Sims RJ 3rd, Chen CF, Santos-Rosa H, Kouzarides T, Patel SS, Reinberg D. 2005. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 280: 41789-41792.
229. Sims RJ 3rd, Rojas LA, Beck D, Bonasio R, Schuller R, Drury WJ 3rd, Eick D, Reinberg D. 2011. The C-terminal domain of RNA polymerase II is modified by site-specific methylation. Science 332: 99-103.
230. Siomi MC, Mannen T, Siomi H. 2010. Howdoes the royal family of Tudor rule the PIWI-interacting RNA pathway? Genes Dev 24: 636-646.
231. Slater LM, Allen MD, Bycroft M. 2003. Structural variation in PWWP domains. J Mol Biol 330: 571-576.
232. Song JJ, Kingston RE. 2008.WDR5interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J Biol Chem 283: 35258-35264.
233. Song JJ, Garlick JD, Kingston RE. 2008. Structural basis of histone H4 recognition by p55. Genes Dev 22: 1313-1318.
234. Song J, Rechkoblit O, Bestor TH, Patel DJ. 2011. Structure of DNMT1-DNA complex reveals a role for autoinhibition in maintenance DNA methylation. Science 331: 1036-1040.
235. Song J, Teplova M, Ishibe-Murakami S, Patel DJ. 2012. Structure-based mechanistic insights into DNMT1-mediated maintenance DNA methylation. Science 335: 709-712.
236. Sprangers R, Groves MR, Sinning I, Sattler M. 2003. High-resolution X-ray andNMRstructures of theSMNTudor domain: Conformational variation in the binding site for symmetrically dimethylated arginine residues. J Mol Biol 327: 507-520.
237. Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature 403: 41-45.
238. Sukackaite R, Grazulis S, Tamulaitis G, Siksnys V. 2012. The recognition domain of the methyl-specific endonucleaseMcrBC flips out 5-methylcytosine. Nucleic Acids Res 40: 7552-7562.
239. Sun ZW, Allis CD. 2002. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
240. 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.
241. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935.
242. Tan S, Davey CA. 2011. Nucleosome structural studies. Curr Opin Struct Biol 21: 128-136.
243. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, et al. 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.
244. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. 2007. How chromatin-binding modules interpret histone modifications: Lessons from professional pocket pickers. Nat Struct Mol Biol 14: 1025-1040.
245. Tripsianes K, Madl T, Machyna M, Fessas D, Englbrecht C, Fischer U, Neugebauer KM, Sattler M. 2011. Structural basis for dimethylarginine recognition by the Tudor domains of human SMN and SPF30 proteins. Nat Struct Mol Biol 18: 1414-1420.
246. Trojer P, Reinberg D. 2008. Beyond histone methyl-lysine binding: How malignant brain tumor (MBT) protein L3MBTL1 impacts chromatin structure. Cell Cycle 7: 578-585.
247. Trojer P, Li G, Sims RJ 3rd, Vaquero A, Kalakonda N, Boccuni P, Lee D, Erdjument-Bromage H, Tempst P, Nimer SD, et al. 2007. L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129: 915-928.
248. Trojer P, Cao AR, Gao Z, Li Y, Zhang J, Xu X, Li G, Losson R, Erdjument-Bromage H, Tempst P, et al. 2011. L3MBTL2 protein acts in concert with PcG protein-mediated monoubiquitination of H2A to establish a repressive chromatin structure. Mol Cell 42: 438-450.
249. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. 2010a. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689-693.
250. Tsai WW, Wang Z, Yiu TT, Akdemir KC, Xia W, Winter S, Tsai CY, Shi X, Schwarzer D, Plunkett W, et al. 2010b. TRIM24 links a non-canonical histone signature to breast cancer. Nature 468: 927-932.
251. van Holde K, Zlatanova J. 2007. Chromatin fiber structure:Where is the problem now? Semin Cell Dev Biol 18: 651-658.
252. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, et al. 2010. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142: 967-980.
253. Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, Kvinlaug BT, Huntly BJ, Gottgens B, Bycroft M. 2010.Molecular basis of histoneH3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol 17: 617-619.
254. Voigt P, Reinberg D. 2011. Histone tails: Ideal motifs for probing epigenetics through chemical biology approaches. Chembiochem 12: 236-252.
255. Wang Z, Patel DJ. 2011. Combinatorial readout of dual histone modifications by paired chromatin-associated modules. J Biol Chem 286: 18363-18368.
256. Wang WK, Tereshko V, Boccuni P, MacGrogan D, Nimer SD, Patel DJ. 2003. Malignant brain tumor repeats: A three-leaved propeller architecture with ligand/peptide binding pockets. Structure 11: 775-789.
257. Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H, Luo JL, Patel DJ, Allis CD. 2009. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. sNature 459: 847-851.
258. Wang M, Mok MW, Harper H, Lee WH, Min J, Knapp S, Oppermann U, Marsden B, Schapira M. 2010a. Structural genomics of histone tail recognition. Bioinformatics 26: 2629-2630.
259. Wang Z, Song J, Milne TA, Wang GG, Li H, Allis CD, Patel DJ. 2010b. Pro isomerization inMLL1PHD3-bromocassette connectsH3K4mereadout to CyP33 and HDAC-mediated repression. Cell 141: 1183-1194.
260. Wang C, Shen J, Yang Z, Chen P, Zhao B, Hu W, Lan W, Tong X, Wu H, Li G, et al. 2011. Structural basis for site-specific reading of unmodified R2 of histone H3 tail by UHRF1 PHD finger. Cell Res 21: 1379-1382.
261. West LE, Roy S, Lachmi-Weiner K, Hayashi R, Shi X, Appella E, Kutateladze TG, Gozani O. 2010. The MBTrepeats of L3MBTL1 link SET8-mediated p53 methylation at lysine 382 to target gene repression. J Biol Chem 285: 37725-37732.
262. Williams K, Christensen J, Helin K. 2012. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep 13: 28-35.
263. Wolfe SA, Nekludova L, Pabo CO. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu Rev Biophys Biomol Struct 29: 183-212.
264. Wu H, Zhang Y. 2011. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 25: 2436-2452.
265. Wu H, D’Alessio AC, Ito S, Xia K, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y. 2011a. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473: 389-393.
266. Wu L, Zee BM, Wang Y, Garcia BA, Dou Y. 2011b. The RING finger protein MSL2 in the MOF complex is an E3 ubiquitin ligase for H2B K34 and is involved in crosstalkwith H3 K4 and K79 methylation. Mol Cell 43: 132-144.
267. Wysocka J, Swigut T, Milne TA, Dou Y, Zhang X, Burlingame AL, Roeder RG, Brivanlou AH, Allis CD. 2005. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121: 859-872.
268. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, et al. 2006. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86-90.
269. Xi Q, Wang Z, Zaromytidou AI, Zhang XH, Chow-Tsang LF, Liu JX, Kim H, Barlas A, Manova-Todorova K, Kaartinen V, et al. 2011. A poised chromatin platform for TGF-b access to master regulators. Cell 147: 1511-1524.
270. Xia ZB, Anderson M, Diaz MO, Zeleznik-Le NJ. 2003. MLL repression domain interacts with histone deacetylases, the polycomb group proteins HPC2 and BMI-1, and the corepressor C-terminal-binding protein. Proc Natl Acad Sci 100: 8342-8347.
271. Xiao S, Xie D, Cao X, Yu P, Xing X, Chen CC, Musselman M, Xie M, West FD, Lewin HA, et al. 2012. Comparative epigenomic annotation of regulatory DNA. Cell 149: 1381-1392.
272. Xie S, Jakoncic J, Qian C. 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.
273. 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.
274. Xu Y, Wu F, Tan L, Kong L, Xiong L, Deng J, Barbera AJ, Zheng L, Zhang H, Huang S, et al. 2011. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42: 451-464.
275. Yamada K, Frouws TD, Angst B, Fitzgerald DJ, DeLuca C, Schimmele K, Sargent DF, Richmond TJ. 2011. Structure and mechanism of the chromatin remodelling factor ISW1a. Nature 472: 448-453.
276. Yang N, Xu RM. 2012. Structure and function of the BAH domain in chromatin biology. Crit Rev Biochem Mol Biol 48: 211-221.
277. Yang Y, Lu Y, Espejo A, Wu J, Xu W, Liang S, Bedford MT. 2010. TDRD3 is an effector molecule for arginine-methylated histone marks. Mol Cell 40: 1016-1023.
278. Yang N, Wang W, Wang Y, Wang M, Zhao Q, Rao Z, Zhu B, Xu RM. 2012. Distinct mode of methylated lysine-4 of histone H3 recognition by tandem tudor-like domains of Spindlin1. Proc Natl Acad Sci 109: 17954-17959.
279. Yap KL, Zhou MM. 2010. Keeping it in the family: Diverse histone recognition by conserved structural folds. Crit Rev Biochem Mol Biol 45: 488-505.
280. Yap KL, Zhou MM. 2011. Structure and mechanisms of lysine methylation recognition by the chromodomain in gene transcription. Biochemistry 50: 1966-1980.
281. Yuan CC, Matthews AG, Jin Y, Chen CF, Chapman BA, Ohsumi TK, Glass KC, Kutateladze TG, Borowsky ML, Struhl K, et al. 2012. Histone H3R2 symmetric dimethylation and histone H3K4 trimethylation are tightly correlated in eukaryotic genomes. Cell Rep 1: 83-90.
282. Zeng L, Yap KL, Ivanov AV, Wang X, Mujtaba S, Plotnikova O, Rauscher FJ 3rd, Zhou MM. 2008. Structural insights into human KAP1 PHD finger-bromodomain and its role in gene silencing. Nat Struct Mol Biol 15: 626-633.
283. Zeng L, Zhang Q, Li S, Plotnikov AN, Walsh MJ, Zhou MM. 2010. Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466: 258-262.
284. Zhang Z, Hayashi MK, Merkel O, Stillman B, Xu RM. 2002. Structure and function of the BAH-containing domain of Orc1p in epigenetic silencing. EMBO J 21: 4600-4611.
285. Zhang K, Lin W, Latham JA, Riefler GM, Schumacher JM, Chan C, Tatchell K, Hawke DH, Kobayashi R, Dent SY. 2005. The Set1 methyltransferase opposes Ipl1 aurora kinase functions in chromosome segregation. Cell 122: 723-734.
286. Zhang P, Du J, Sun B, Dong X, Xu G, Zhou J, Huang Q, Liu Q, Hao Q, Ding J. 2006. Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3. Nucleic Acids Res 34: 6621-6628.
287. Zhang L, Lu X, Lu J, Liang H, Dai Q, Xu GL, Luo C, Jiang H, He C. 2012. Thymine DNA glycosylase specifically recognizes 5-carboxylcytosinemodified DNA. Nat Chem Biol 8: 328-330.
288. Zhao Y, Garcia BA. 2014. Comprehensive catalog of currently documented histone modifications. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a025064.
289. Zhou VW, Goren A, Bernstein BE. 2011. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12: 7-18.
290. Zoghbi HY, Beaudet AL. 2014. Epigenetics and human disease. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a019497.