Hinge and chromoshadow of HP1α participate in recognition of K9 methylated histone H3 in nucleosomes

Journal of Molecular Biology

Volumn 425, Issue 1, 2013, Pages 54-70

  Mishima, Yuichi ^a   Watanabe, Makoto ^b,c   Kawakami, Toru ^c   Jayasinghe, Chanika D ^a   Otani, Junji ^d   Kikugawa, Yusuke ^d   Shirakawa, Masahiro ^d   Kimura, Hiroshi ^a   Nishimura, Osamu ^b,c   Aimoto, Saburo ^c   Tajima, Shoji ^a   Suetake, Isao ^a  

^a OSAKA UNIVERSITY   (Japan)

^b SHIMADZU CORPORATION   (Japan)

^c Institute for Protein Research   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

histone H3; HP1 ; methylation; nucleosome

Indexed keywords

HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1 ALPHA; HISTONE H3; LYSINE; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMOSHADOW DOMAIN; DNA BINDING; HINGE REGION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN METHYLATION;

EUKARYOTA;

EID: 84871808185     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.10.018     Document Type: Article

References (29)

1. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
2. T. Kouzarides Histone methylation in transcriptional control Curr. Opin. Genet. Dev. 12 2002 198 209
3. A.J. Bannister, P. Zegerman, J.F. Partridge, E.A. Miska, J.O. Thomas, R.C. Allshire, and T. Kouzarides Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain Nature 410 2001 120 124
4. J.C. Eissenberg, and S.C. Elgin The HP1 protein family: getting a grip on chromatin Curr. Opin. Genet. Dev. 10 2000 204 210
5. M. Lachner, D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins Nature 410 2001 116 120
6. W. Fischle, B.S. Tseng, H.L. Dormann, B.M. Ueberheide, B.A. Garcia, and J. Shabanowitz Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation Nature 438 2005 1116 1122
7. Q. Ye, I. Callebaut, A. Pezhman, J.C. Courvalin, and H.J. Worman Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR J. Biol. Chem. 272 1997 14983 14989
8. M.S. Lechner, D.C. Schultz, D. Negorev, G.G. Maul, and F.J. Rauscher 3rd. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain Biochem. Biophys. Res. Commun. 331 2005 929 937
9. D. Canzio, E.Y. Chang, S. Shankar, K.M. Kuchenbecker, M.D. Simon, and H.D. Madhani Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly Mol. Cell 41 2011 67 81
10. F. Munari, S. Soeroes, H.M. Zenn, A. Schomburg, N. Kost, and S. Schröder Methylation of lysine 9 in histone H3 directs alternative modes of highly dynamic interaction of heterochromatin protein hHP1β with the nucleosome J. Biol. Chem. 287 2012 33756 33765
11. R.R. Meehan, C.F. Kao, and S. Pennings HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain EMBO J. 22 2003 3164 3174
12. C. Muchardt, M. Guillemé, J.S. Seeler, D. Trouche, A. Dejean, and M. Yaniv Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1α EMBO Rep. 3 2002 975 981
13. X. Zhang, Z. Yang, S.I. Khan, J.R. Horton, H. Tamaru, E.U. Selker, and X. Cheng Structural basis for the product specificity of histone lysine methyltransferases Mol. Cell 12 2003 177 185
14. R.E. Collins, M. Tachibana, H. Tamaru, K.M. Smith, D. Jia, and X. Zhang In vitro and in vivo analyses of a Phe/Tyr switch controlling product specificity of histone lysine methyltransferases J. Biol. Chem. 280 2005 5563 5570
15. P. Rathert, X. Zhang, C. Freund, X. Cheng, and A. Jeltsch Analysis of the substrate specificity of the Dim-5 histone lysine methyltransferase using peptide arrays Chem. Biol. 15 2008 5 11
16. H. Kimura, Y. Hayashi-Takanaka, Y. Goto, N. Takizawa, and N. Nozaki The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies Cell Struct. Funct. 33 2008 61 73
17. T.J. Wigle, L.M. Provencher, J.L. Norris, J. Jin, J. Brown, S.V. Frye, and W.P. Janzen Accessing protein methyltransferase and demethylase enzymology using microfluidic capillary electrophoresis Chem. Biol. 17 2010 695 704
18. T. Schalch, S. Duda, D.F. Sargent, and T.J. Richmond X-ray structure of a tetranucleosome and its implications for the chromatin fibre Nature 436 2005 138 141
19. C.C. de la Cruz, A. Kirmizis, M.D. Simon, K. Isono, H. Koseki, and B. Panning The polycomb group protein SUZ12 regulates histone H3 lysine 9 methylation and HP1α distribution Chromosome Res. 15 2007 299 314
20. S. Cantaloube, K. Romeo, P. Le Baccon, G. Almouzni, and J.P. Quivy Characterization of chromatin domains by 3D fluorescence microscopy: an automated methodology for quantitative analysis and nuclei screening BioEssays 34 2012 509 517
21. J. Walker, P. Crowley, A.D. Moreman, and J. Barrett Biochemical properties of cloned glutathione S-transferases from Schistosoma mansoni and Schistosoma japonicum Mol. Biochem. Parasitol. 61 1993 255 264
22. Y. Huang, M.P. Myers, and R.M. Xu Crystal structure of the HP1-EMSY complex reveals an unusual mode of HP1 binding Structure 14 2006 703 712
23. H. Takeshima, I. Suetake, H. Shimahara, K. Ura, S. Tate, and S. Tajima Distinct DNA methylation activity of Dnmt3a and Dnmt3b towards naked and nucleosomal DNA J. Biochem. 139 2006 503 515
24. F. Sanger, S. Nicklen, and A.R. Coulson DNA sequencing with chain-terminating inhibitors Proc. Natl. Acad. Sci. USA 74 1977 5463 5467
25. A. Aoki, I. Suetake, J. Miyagawa, T. Fujio, T. Chijiwa, H. Sasaki, and S. Tajima Enzymatic properties of de novo-type mouse DNA (cytosine-5) methyltransferases Nucleic Acids Res. 29 2001 3506 3512
26. I. Suetake, D. Hayata, and S. Tajima The amino-terminus of mouse DNA methyltransferase 1 forms an independent domain and binds to DNA with the sequence involving PCNA binding motif J. Biochem. 140 2006 763 776
27. K. Luger, T.J. Rechsteiner, and T.J. Richmond Preparation of nucleosome core particle from recombinant histones Methods Enzymol. 304 1999 3 19
28. I. Suetake, Y. Mishima, H. Kimura, Y.H. Lee, Y. Goto, and H. Takeshima Characterization of DNA-binding activity in the N-terminal domain of the DNA methyltransferase Dnmt3a Biochem. J. 437 2011 141 148
29. D. Watanabe, I. Suetake, T. Tada, and S. Tajima Stage- and cell-specific expression of Dnmt3a and Dnmt3b during embryogenesis Mech. Dev. 118 2002 187 190