The ATRX-ADD domain binds to H3 tail peptides and reads the combined methylation state of K4 and K9

Human Molecular Genetics

Volumn 20, Issue 11, 2011, Pages 2195-2203

  Dhayalan, Arunkumar ^a,b   Tamas, Raluca ^a   Bock, Ina ^a   Tattermusch, Anna ^a   Dimitrova, Emilia ^a   Kudithipudi, Srikanth ^a   Ragozin, Sergey ^a   Jeltsch, Albert ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

^b PONDICHERRY UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 3; DNA METHYLTRANSFERASE 3L; HISTONE H3; LYSINE; METHYLTRANSFERASE; NUCLEAR PROTEIN; PROTEIN ATRX; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; GENE MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION;

3T3 CELLS; ALPHA-THALASSEMIA; AMINO ACID SEQUENCE; ANIMALS; CHROMATIN; CLONING, MOLECULAR; DNA HELICASES; GENE EXPRESSION; HEK293 CELLS; HISTONES; HUMANS; LYSINE; MENTAL RETARDATION, X-LINKED; METHYLATION; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY;

EID: 79955995634     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr107     Document Type: Article

References (35)

1. Gibbons, R.J., Picketts, D.J., Villard, L. and Higgs, D.R. (1995) Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell, 80, 837-845.
2. Gibbons, R.J., Brueton, L., Buckle, V.J., Burn, J., Clayton-Smith, J., Davison, B.C., Gardner, R.J., Homfray, T., Kearney, L., Kingston, H.M. et al. (1995) Clinical and hematologic aspects of the X-linked alpha-thalassemia/mental retardation syndrome (ATR-X). Am. J. Med. Genet., 55, 288-299.
3. Gibbons, R.J., Wada, T., Fisher, C.A., Malik, N., Mitson, M.J., Steensma, D.P., Fryer, A., Goudie, D.R., Krantz, I.D. and Traeger-Synodinos, J. (2008) Mutations in the chromatin-associated protein ATRX. Hum. Mutat., 29, 796-802.
4. Garrick, D., Sharpe, J.A., Arkell, R., Dobbie, L., Smith, A.J., Wood, W.G., Higgs, D.R. and Gibbons, R.J. (2006) Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet., 2, e58.
5. Xue, Y., Gibbons, R., Yan, Z., Yang, D., McDowell, T.L., Sechi, S., Qin, J., Zhou, S., Higgs, D. and Wang, W. (2003) The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl Acad. Sci. USA, 100, 10635-10640.
6. McDowell, T.L., Gibbons, R.J., Sutherland, H., O'Rourke, D.M., Bickmore, W.A., Pombo, A., Turley, H., Gatter, K., Picketts, D.J., Buckle, V.J. et al. (1999) Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc. Natl Acad. Sci. USA, 96, 13983-13988.
7. Picketts, D.J., Tastan, A.O., Higgs, D.R. and Gibbons, R.J. (1998) Comparison of the human and murine ATRX gene identifies highly conserved, functionally important domains. Mamm. Genome, 9, 400-403.
8. Le Douarin, B., Nielsen, A.L., Garnier, J.M., Ichinose, H., Jeanmougin, F., Losson, R. and Chambon, P. (1996) A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J., 15, 6701-6715.
9. Cardoso, C., Timsit, S., Villard, L., Khrestchatisky, M., Fontes, M. and Colleaux, L. (1998) Specific interaction between the XNP/ATR-X gene product and the SET domain of the human EZH2 protein. Hum. Mol. Genet., 7, 679-684.
10. Nan, X., Hou, J., Maclean, A., Nasir, J., Lafuente, M.J., Shu, X., Kriaucionis, S. and Bird, A. (2007) Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl Acad. Sci. USA, 104, 2709-2714.
11. Xie, S., Wang, Z., Okano, M., Nogami, M., Li, Y., He, W.W., Okumura, K. and Li, E. (1999) Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene, 236, 87-95.
12. Aapola, U., Kawasaki, K., Scott, H.S., Ollila, J., Vihinen, M., Heino, M., Shintani, A., Kawasaki, K., Minoshima, S., Krohn, K. et al. (2000) Isolation and initial characterization of a novel zinc finger gene, DNMT3L, on 21q22.3, related to the cytosine-5-methyltransferase 3 gene family. Genomics, 65, 293-298.
13. Argentaro, A., Yang, J.C., Chapman, L., Kowalczyk, M.S., Gibbons, R.J., Higgs, D.R., Neuhaus, D. and Rhodes, D. (2007) Structural consequences of disease-causing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc. Natl Acad. Sci. USA, 104, 11939-11944.
14. Badens, C., Lacoste, C., Philip, N., Martini, N., Courrier, S., Giuliano, F., Verloes, A., Munnich, A., Leheup, B., Burglen, L. et al. (2006) Mutations in PHD-like domain of the ATRX gene correlate with severe psychomotor impairment and severe urogenital abnormalities in patients with ATRX syndrome. Clin. Genet., 70, 57-62.
15. Baker, L.A., Allis, C.D. and Wang, G.G. (2008) PHD fingers in human diseases: disorders arising from misinterpreting epigenetic marks. Mutat. Res., 647, 3-12.
16. 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.
17. Ooi, S.K., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., Erdjument-Bromage, H., Tempst, P., Lin, S.P., Allis, C.D. et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature, 448, 714-717.
18. Otani, J., Nankumo, T., Arita, K., Inamoto, S., Ariyoshi, M. and 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.
19. Zhang, Y., Jurkowska, R., Soeroes, S., Rajavelu, A., Dhayalan, A., Bock, I., Rathert, P., Brandt, O., Reinhardt, R., Fischle, W. et al. (2010) Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res., 38, 4246-4253.
20. Wong, L.H., McGhie, J.D., Sim, M., Anderson, M.A., Ahn, S., Hannan, R.D., George, A.J., Morgan, K.A., Mann, J.R. and Choo, K.H. (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res., 20, 351-360.
21. Goldberg, A.D., Banaszynski, L.A., Noh, K.M., Lewis, P.W., Elsaesser, S.J., Stadler, S., Dewell, S., Law, M., Guo, X., Li, X. et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell, 140, 678-691.
22. Lewis, P.W., Elsaesser, S.J., Noh, K.M., Stadler, S.C. and Allis, C.D. (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl Acad. Sci. USA, 107, 14075-14080.
23. Cardoso, C., Lutz, Y., Mignon, C., Compe, E., Depetris, D., Mattei, M.G., Fontes, M. and Colleaux, L. (2000) ATR-X mutations cause impaired nuclear location and altered DNA binding properties of the XNP/ATR-X protein. J. Med. Genet., 37, 746-751.
24. Peters, A.H., Mermoud, J.E., O'Carroll, D., Pagani, M., Schweizer, D., Brockdorff, N. and Jenuwein, T. (2002) Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat. Genet., 30, 77-80.
25. Guenatri, M., Bailly, D., Maison, C. and Almouzni, G. (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol., 166, 493-505.
26. Baumann, C., Schmidtmann, A., Muegge, K. and De La Fuente, R. (2008) Association of ATRX with pericentric heterochromatin and the Y chromosome of neonatal mouse spermatogonia. BMC Mol. Biol., 9, 29.
27. Jeltsch, A. and Lanio, T. (2002) Site-directed mutagenesis by polymerase chain reaction. Methods Mol. Biol., 182, 85-94.
28. 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, 263-265.
29. Gao, T., Collins, R.E., Horton, J.R., Zhang, X., Zhang, R., Dhayalan, A., Tamas, R., Jeltsch, A. and Cheng, X. (2009) The ankyrin repeat domain of Huntingtin interacting protein 14 contains a surface aromatic cage, a potential site for methyl-lysine binding. Proteins, 76, 772-777.
30. Rathert, P., Dhayalan, A., Murakami, M., Zhang, X., Tamas, R., Jurkowska, R., Komatsu, Y., Shinkai, Y., Cheng, X. and Jeltsch, A. (2008) Protein lysine methyltransferase G9a acts on non-histone targets. Nat. Chem. Biol., 4, 344-346.
31. Winkler, D.F., Hilpert, K., Brandt, O. and Hancock, R.E. (2009) Synthesis of peptide arrays using SPOT-technology and the CelluSpots-method. Methods Mol. Biol., 570, 157-174.
32. Jeltsch, A., Hoggett, J. and Urbanke, C. (2005) In Meyers, R.A. (ed.), Encyclopedia of Molecular Cell Biology and Molecular Medicine. Wiley-VCH, Vol. 11, pp. 391-410.
33. Shechter, D., Dormann, H.L., Allis, C.D. and Hake, S.B. (2007) Extraction, purification and analysis of histones. Nat. Protoc., 2, 1445-1457.
34. Brand, M., Rampalli, S., Chaturvedi, C.P. and Dilworth, F.J. (2008) Analysis of epigenetic modifications of chromatin at specific gene loci by native chromatin immunoprecipitation of nucleosomes isolated using hydroxyapatite chromatography. Nat. Protoc., 3, 398-409.
35. Jacobs, S.A. and Khorasanizadeh, S. (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science, 295, 2080-2083.