analysis, and biological evaluations. J Med Chem 50(6):1241–1253. https://doi.org/10.1021/
jm061213n
93. Ren C, Smith SG, Yap K, Li S, Li J, Mezei M, Rodriguez Y, Vincek A, Aguilo F, Walsh MJ,
Zhou MM (2016) Structure-guided discovery of selective antagonists for the chromodomain
of polycomb repressive protein CBX7. ACS Med Chem Lett 7(6):601–605. https://doi.org/10.
1021/acsmedchemlett.6b00042
94. Milosevich N, Gignac MC, McFarlane J, Simhadri C, Horvath S, Daze KD, Croft CS, Dheri A,
Quon TT, Douglas SF, Wulff JE, Paci I, Hof F (2016) Selective inhibition of CBX6: a
methyllysine reader protein in the polycomb family. ACS Med Chem Lett 7(2):139–144.
https://doi.org/10.1021/acsmedchemlett.5b00378
95. Brahms H, Meheus L, de Brabandere V, Fischer U, Lührmann R (2001) Symmetrical
dimethylation of arginine residues in spliceosomal Sm protein B/B’ and the Sm-like protein
LSm4, and their interaction with the SMN protein. RNA 7(11):1531–1542
96. 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(7):1361–1373. https://doi.org/10.1016/j.cell.2006.10.043
97. 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(7015):406–411. https://doi.org/10.1038/
nature03114
98. Kim J, Daniel J, Espejo A, Lake A, Krishna M, Xia L, Zhang Y, Bedford MT (2006) Tudor,
MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep 7(4):397–403.
https://doi.org/10.1038/sj.embor.7400625
99. Chen C, Jin J, James DA, Adams-Cioaba MA, Park JG, Guo Y, Tenaglia E, Xu C, Gish G,
Min J, Pawson T (2009) Mouse Piwi interactome identifies binding mechanism of Tdrkh
Tudor domain to arginine methylated Miwi. Proc Natl Acad Sci U S A 106(48):20336–20341.
https://doi.org/10.1073/pnas.0911640106
100. Liu H, Wang JY, Huang Y, Li Z, Gong W, Lehmann R, Xu RM (2010) Structural basis for
methylarginine-dependent recognition of Aubergine by Tudor. Genes Dev 24(17):1876–1881.
https://doi.org/10.1101/gad.1956010
101. Liu K, Chen C, Guo Y, Lam R, Bian C, Xu C, Zhao DY, Jin J, MacKenzie F, Pawson T, Min J
(2010) Structural basis for recognition of arginine methylated Piwi proteins by the extended
Tudor domain. Proc Natl Acad Sci U S A 107(43):18398–18403. https://doi.org/10.1073/pnas.
1013106107
102. Liu K, Guo Y, Liu H, Bian C, Lam R, Liu Y, Mackenzie F, Rojas LA, Reinberg D,
Bedford MT, Xu RM, Min J (2012) Crystal structure of TDRD3 and methyl-arginine binding
characterization of TDRD3, SMN and SPF30. PLoS One 7(2):e30375. https://doi.org/10.
1371/journal.pone.0030375
103. Sikorsky T, Hobor F, Krizanova E, Pasulka J, Kubicek K, Stefl R (2012) Recognition of
asymmetrically dimethylated arginine by TDRD3. Nucleic Acids Res 40(22):11748–11755.
https://doi.org/10.1093/nar/gks929
104. 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(12):1414–1420. https://doi.org/10.
1038/nsmb.2185
105. Liu L, Zhen XT, Denton E, Marsden BD, Schapira M (2012) ChromoHub: a data hub for
navigators of chromatin-mediated signalling. Bioinformatics 28(16):2205–2206. https://doi.
org/10.1093/bioinformatics/bts340
106. Ballare C, Lange M, Lapinaite A, Martin GM, Morey L, Pascual G, Liefke R, Simon B, Shi Y,
Gozani O, Carlomagno T, Benitah SA, Di Croce L (2012) Phf19 links methylated Lys36 of
histone H3 to regulation of Polycomb activity. Nat Struct Mol Biol 19(12):1257–1265. https://
doi.org/10.1038/nsmb.2434
107. Cai L, Rothbart SB, Lu R, Xu B, Chen WY, Tripathy A, Rockowitz S, Zheng D, Patel DJ,
Allis CD, Strahl BD, Song J, Wang GG (2013) An H3K36 methylation-engaging Tudor motif
Methyl-Readers and Inhibitors
389
jm061213n
93. Ren C, Smith SG, Yap K, Li S, Li J, Mezei M, Rodriguez Y, Vincek A, Aguilo F, Walsh MJ,
Zhou MM (2016) Structure-guided discovery of selective antagonists for the chromodomain
of polycomb repressive protein CBX7. ACS Med Chem Lett 7(6):601–605. https://doi.org/10.
1021/acsmedchemlett.6b00042
94. Milosevich N, Gignac MC, McFarlane J, Simhadri C, Horvath S, Daze KD, Croft CS, Dheri A,
Quon TT, Douglas SF, Wulff JE, Paci I, Hof F (2016) Selective inhibition of CBX6: a
methyllysine reader protein in the polycomb family. ACS Med Chem Lett 7(2):139–144.
https://doi.org/10.1021/acsmedchemlett.5b00378
95. Brahms H, Meheus L, de Brabandere V, Fischer U, Lührmann R (2001) Symmetrical
dimethylation of arginine residues in spliceosomal Sm protein B/B’ and the Sm-like protein
LSm4, and their interaction with the SMN protein. RNA 7(11):1531–1542
96. 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(7):1361–1373. https://doi.org/10.1016/j.cell.2006.10.043
97. 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(7015):406–411. https://doi.org/10.1038/
nature03114
98. Kim J, Daniel J, Espejo A, Lake A, Krishna M, Xia L, Zhang Y, Bedford MT (2006) Tudor,
MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep 7(4):397–403.
https://doi.org/10.1038/sj.embor.7400625
99. Chen C, Jin J, James DA, Adams-Cioaba MA, Park JG, Guo Y, Tenaglia E, Xu C, Gish G,
Min J, Pawson T (2009) Mouse Piwi interactome identifies binding mechanism of Tdrkh
Tudor domain to arginine methylated Miwi. Proc Natl Acad Sci U S A 106(48):20336–20341.
https://doi.org/10.1073/pnas.0911640106
100. Liu H, Wang JY, Huang Y, Li Z, Gong W, Lehmann R, Xu RM (2010) Structural basis for
methylarginine-dependent recognition of Aubergine by Tudor. Genes Dev 24(17):1876–1881.
https://doi.org/10.1101/gad.1956010
101. Liu K, Chen C, Guo Y, Lam R, Bian C, Xu C, Zhao DY, Jin J, MacKenzie F, Pawson T, Min J
(2010) Structural basis for recognition of arginine methylated Piwi proteins by the extended
Tudor domain. Proc Natl Acad Sci U S A 107(43):18398–18403. https://doi.org/10.1073/pnas.
1013106107
102. Liu K, Guo Y, Liu H, Bian C, Lam R, Liu Y, Mackenzie F, Rojas LA, Reinberg D,
Bedford MT, Xu RM, Min J (2012) Crystal structure of TDRD3 and methyl-arginine binding
characterization of TDRD3, SMN and SPF30. PLoS One 7(2):e30375. https://doi.org/10.
1371/journal.pone.0030375
103. Sikorsky T, Hobor F, Krizanova E, Pasulka J, Kubicek K, Stefl R (2012) Recognition of
asymmetrically dimethylated arginine by TDRD3. Nucleic Acids Res 40(22):11748–11755.
https://doi.org/10.1093/nar/gks929
104. 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(12):1414–1420. https://doi.org/10.
1038/nsmb.2185
105. Liu L, Zhen XT, Denton E, Marsden BD, Schapira M (2012) ChromoHub: a data hub for
navigators of chromatin-mediated signalling. Bioinformatics 28(16):2205–2206. https://doi.
org/10.1093/bioinformatics/bts340
106. Ballare C, Lange M, Lapinaite A, Martin GM, Morey L, Pascual G, Liefke R, Simon B, Shi Y,
Gozani O, Carlomagno T, Benitah SA, Di Croce L (2012) Phf19 links methylated Lys36 of
histone H3 to regulation of Polycomb activity. Nat Struct Mol Biol 19(12):1257–1265. https://
doi.org/10.1038/nsmb.2434
107. Cai L, Rothbart SB, Lu R, Xu B, Chen WY, Tripathy A, Rockowitz S, Zheng D, Patel DJ,
Allis CD, Strahl BD, Song J, Wang GG (2013) An H3K36 methylation-engaging Tudor motif
Methyl-Readers and Inhibitors
389
