The methyltransferase NSD3 has chromatin-binding motifs, PHD5-C5HCH, that are distinct from other NSD (nuclear receptor SET domain) family members in their histone H3 recognition

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 4692-4703

  He, Chao ^a   Li, Fudong ^a   Zhang, Jiahai ^a   Wu, Jihui ^a   Shi, Yunyu ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HUMAN DISEASE; METHYLTRANSFERASES; N-TERMINALS; NUCLEAR RECEPTORS;

CHROMOSOMES;

PROTEINS;

CELL NUCLEUS RECEPTOR; CYSTEINYLHISTIDINE RICH DOMAIN; FIFTH PLANT HOMEODOMAIN; HISTONE H3; HISTONE H3K36; HISTONE H3K4; HISTONE H3K9; HOMEODOMAIN PROTEIN; METHYLTRANSFERASE; NUCLEAR RECEPTOR SET DOMAIN; NUCLEAR RECEPTOR SET DOMAIN 1; NUCLEAR RECEPTOR SET DOMAIN 2; NUCLEAR RECEPTOR SET DOMAIN 3; NUCLEAR RECEPTOR SET DOMAIN 3 METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; CRYSTAL STRUCTURE; HISTONE METHYLATION; HUMAN; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CHROMATIN; CRYSTALLOGRAPHY, X-RAY; EPIGENESIS, GENETIC; GENOMICS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84874074359     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.426148     Document Type: Article

References (50)

1. Strahl, B. D., and Allis, C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45
2. Taverna, S. D., Li, H., Ruthenburg, A. J., and 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
3. Kurotaki, N., Imaizumi, K., Harada, N., Masuno, M., Kondoh, T., Nagai, T., Ohashi, H., Naritomi, K., Tsukahara, M., Makita, Y., Sugimoto, T., Sonoda, T., Hasegawa, T., Chinen, Y., Tomita Ha, H. A., Kinoshita, A., Mizuguchi, T., Yoshiura Ki, K., Ohta, T., Kishino, T., Fukushima, Y., Niikawa, N., and Matsumoto, N. (2002) Haploinsufficiency of NSD1 causes Sotos syndrome. Nat. Genet. 30, 365-366
4. Faravelli, F. (2005) NSD1 mutations in Sotos syndrome. Am. J. Med. Genet. C 137, 24-31
5. Wright, T. J., and Ricke., D. O., Denison, K., Abmayr, S., Cotter, P. D., Hirschhorn, K., Keinänen, M., McDonald-McGinn, D., Somer, M., Spinner, N., Yang-Feng, T., Zackai, E., and Altherr, M. R. (1997) A transcript map of the newly defined 165 kb Wolf-Hirschhorn syndrome critical region. Hum. Mol. Genet. 6, 317-324
6. Rosati, R., La Starza, R., Veronese, A., Aventin, A., Schwienbacher, C., Vallespi, T., Negrini, M., and Martelli., M. F., and Mecucci, C. (2002) NUP98 is fused to the NSD3 gene in acute myeloid leukemia associated with t(8; 11)(p11.2;p15). Blood 99, 3857-3860
7. Cerveira, N., Correia, C., Dória, S., Bizarro, S., Rocha, P., Gomes, P., Torres, L., Norton, L., Borges, B. S., Castedo, S., and Teixeira, M. R. (2003) Frequency of NUP98-NSD1 fusion transcript in childhood acute myeloid leukaemia. Leukemia 17, 2244-2247
8. Keats, J. J., Reiman, T., Maxwell, C. A., and Taylor., B. J., Larratt, L. M., Mant, M. J., and Belch., A. R., and Pilarski, L. M. (2003) In multiple myeloma, t(4; 14)(p16;q32) is an adverse prognostic factor irrespective of FGFR3 expression. Blood 101, 1520-1529
9. Keats, J. J., and Maxwell., C. A., Taylor, B. J., Hendzel, M. J., Chesi, M., and Bergsagel., P. L., Larratt, L. M., Mant, M. J., Reiman, T., and Belch., A. R., and Pilarski, L. M. (2005) Overexpression of transcripts originating from the MMSET locus characterizes all t(4;14)(p16;q32)-positive multiple myeloma patients. Blood 105, 4060-4069
10. Angrand, P. O., Apiou, F., Stewart, A. F., Dutrillaux, B., Losson, R., and Chambon, P. (2001) NSD3, a new SET domain-containing gene, maps to 8p12 and is amplified in human breast cancer cell lines. Genomics 74, 79-88
11. Lucio-Eterovic, A. K., and Carpenter, P. B. (2011) An open and shut case for the role of NSD proteins as oncogenes. Transcription 2, 158-161
12. Wagner, E. J., and Carpenter, P. B. (2012) Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell Biol. 13, 115-126
13. Rayasam, G. V., Wendling, O., Angrand, P. O., Mark, M., Niederreither, K., Song, L., Lerouge, T., and Hager., G. L., Chambon, P., and Losson, R. (2003) NSD1 is essential for early post-implantation development and has a cat-alytically active SET domain. EMBO J. 22, 3153-3163
14. Nimura, K., Ura, K., Shiratori, H., Ikawa, M., Okabe, M., Schwartz, R. J., and Kaneda, Y. (2009) A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome. Nature 460, 287-291
15. Douglas, J., Coleman, K., Tatton-Brown, K., Hughes, H. E., and Temple., I. K., Cole, T. R., Rahman, N., and Childhood Overgrowth Collaboration (2005) Evaluation of NSD2 and NSD3 in overgrowth syndromes. Eur. J. Hum. Genet. 13, 150-153
16. 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
17. Kuo, A. J., Cheung, P., Chen, K., Zee, B. M., Kioi, M., Lauring, J., Xi, Y., Park, B. H., Shi, X., and 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
18. Qiao, Q., Li, Y., Chen, Z., Wang, M., Reinberg, D., and Xu, R. M. (2011) The structure of NSD1 reveals an autoregulatory mechanism underlying histone H3K36 methylation. J. Biol. Chem. 286, 8361-8368
19. Lucio-Eterovic, A. K., Singh, M. M., and Gardner., J. E., Veerappan, C. S., Rice, J. C., and Carpenter, P. B. (2010) Role for the nuclear receptor-binding SET domain protein 1 (NSD1) methyltransferasein coordinating lysine 36 methylation at histone 3 with RNA polymerase II function. Proc. Natl. Acad. Sci. U.S.A. 107, 16952-16957
20. Fang, R., and Barbera., A. J., Xu, Y., Rutenberg, M., Leonor, T., Bi, Q., Lan, F., Mei, P., and Yuan., G. C., Lian, C., Peng, J., Cheng, D., Sui, G., Kaiser, U. B., Shi, Y., and Shi, Y. G. (2010) Human LSD2/KDM1b/AOF1 regulates gene transcription by modulating intragenic H3K4me2 methylation. Mol. Cell 39, 222-233
21. Shi, X., Hong, T., Walter, K. L., Ewalt, M., Michishita, E., Hung, T., Carney, D., Peña, P., Lan, F., Kaadige, M. R., Lacoste, N., Cayrou, C., Davrazou, F., Saha, A., Cairns, B.R., Ayer, D.E., Kutateladze, T. G., Shi, Y., Côté, J., Chua, K. F., and Gozani, O. (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442, 96-99
22. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
23. Shen, W., Xu, C., Huang, W., Zhang, J., and Carlson., J. E., Tu, X., Wu, J., and Shi, Y. (2007) Solution structure of human Brg1 bromodomain and its specific binding to acetylated histone tails. Biochemistry 46, 2100-2110
24. Farrow, N. A., Muhandiram, R., Singer, A. U., and Pascal., S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33, 5984-6003
25. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R., and Leslie, A. G. (2011) iMOSFLM. A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281
26. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82
27. Winn, M. D., and Ballard., C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., and Evans., P. R., Keegan, R. M., Krissinel, E. B., and Leslie., A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
28. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A 64, 112-122
29. Langer, G., and Cohen., S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/ wARP version 7. Nat. Protoc. 3, 1171-1179
30. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
31. Murshudov, G. N., and Vagin., A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
32. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
33. Laskowski, R. A., and Macarthur., M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck. A program to check the sterochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
34. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-549
35. Lan, F., and Collins., R. E., De Cegli, R., Alpatov, R., Horton, J. R., Shi, X., Gozani, O., Cheng, X., and Shi, Y. (2007) Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448, 718-722
36. Li, Y., and Li, H. (2012) Many keys to push. Diversifying the "readership" of plant homeodomain fingers. Acta Biochim. Biophys. Sin. 44, 28-39
37. Slama, P., and Geman, D. (2011) Identification of family-determining residues in PHD fingers. Nucleic Acids Res. 39, 1666-1679
38. Chignola, F., Gaetani, M., Rebane, A., Org, T., Mollica, L., Zucchelli, C, Spitaleri, A., Mannella, V., Peterson, P., and Musco, G. (2009) The solution structure of the first PHD finger of autoimmune regulator in complex with non-modified histone H3 tail reveals the antagonistic role of H3R2 methylation. Nucleic Acids Res. 37, 2951-2961
39. Mansfield, R.E., Musselman, C. A., Kwan, A.H, Oliver, S.S., Garske, A.L., Davrazou, F., Denu, J.M., Kutateladze, T. G., and Mackay, J. P. (2011) Plant homeodomain (PHD) fingers of CHD4 are histone H3-binding modules with preference for unmodified H3K4 and methylated H3K9. J. Biol. Chem. 286, 11779-11791
40. Xi, Q., Wang, Z., Zaromytidou, A. I., Zhang, X. H, Chow-Tsang, L. F., Liu, J. X., Kim, H, Barlas, A., Manova-Todorova, K., Kaartinen, V., Studer, L., Mark, W., Patel, D. J., and Massagué, J. (2011) A poised chromatin platform for TGF-β access to master regulators. Cell 147, 1511-1524
41. Qin, S., Jin, L., Zhang, J., Liu, L., Ji, P., Wu, M., Wu, J., and Shi, Y. (2011) Recognition of unmodified histone H3 by the first PHD finger of bro-modomain-PHD finger protein 2 provides insights into the regulation of histone acetyltransferases monocytic leukemic zinc-finger protein (MOZ) and MOZ-related factor (MORF). J. Biol. Chem. 286, 36944-36955
42. Letunic, I., Doerks, T., and Bork, P. (2012) SMART 7. Recent updates to the protein domain annotation resource. Nucleic Acids Res. 40, D302-305
43. Punta, M., Coggill, P. C, Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C, Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L., Eddy, S. R., Bateman, A., and Finn, R. D. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-301
44. Wang, G. G., Cai, L., Pasillas, M. P., and Kamps, M. P. (2007) NUP98-NSD1 links H3K36 methylation to Hox-A gene activation and leukaemo-genesis. Nat. Cell Biol. 9, 804-812
45. Nielsen, A. L., Jørgensen, P., Lerouge, T., Cerviño, M., Chambon, P., and Losson, R. (2004) Nizp1, a novel multitype zinc finger protein that interacts with the NSD1 histone lysine methyltransferase through a unique C2HR motif. Mol. Cell. Biol. 24, 5184-5196
46. Zeng, L., Zhang, Q., Li, S., Plotnikov, A. N., and Walsh., M. J., and Zhou, M. M. (2010) Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466, 258-262
47. Qiu, Y., Liu, L., Zhao, C, Han, C, Li, F., Zhang, J., Wang, Y., Li, G., Mei, Y., Wu, M., Wu, J., and Shi, Y. (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
48. Iwase, S., Xiang, B., Ghosh, S., Ren, T., and Lewis., P. W., Cochrane, J. C, Allis, C. D., Picketts, D. J., Patel, D. J., Li, H., and Shi, Y. (2011) ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat Struct. Mol. Biol. 18, 769-776
49. Eustermann, S., Yang, J. C, Law, M. J., Amos, R., Chapman, L. M., Jelinska, C., Garrick, D., Clynes, D., Gibbons, R. J., Rhodes, D., Higgs, D. R., and Neuhaus, D. (2011) Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat. Struct. Mol. Biol. 18, 777-782
50. Musselman, C. A., Ramírez, J., Sims, J. K., and Mansfield., R. E., Oliver, S. S., Denu, J. M., and Mackay., J. P., Wade, P. A., Hagman, J., and Kutateladze, T. G. (2012) Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc. Natl. Acad. Sci. U.S.A. 109, 787-792