Structural and biochemical studies of human lysine methyltransferase Smyd3 reveal the important functional roles of its post-SET and TPR domains and the regulation of its activity by DNA binding

Nucleic Acids Research

Volumn 39, Issue 10, 2011, Pages 4438-4449

  Xu, Shutong ^a,b   Wu, Jian ^a   Sun, Bingfa ^a,b   Zhong, Chen ^a   Ding, Jianping ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE LYSINE METHYLTRANSFERASE; HYDROXYL GROUP; PROTEIN SET; PROTEIN SMYD3; S ADENOSYLHOMOCYSTEINE; TETRATRICOPEPTIDE REPEAT PROTEIN; TYROSINE; UNCLASSIFIED DRUG; HISTONE; LYSINE; SMYD3 PROTEIN, HUMAN;

ARTICLE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA FLANKING REGION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; AMINO ACID SEQUENCE; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; BIOCATALYSIS; DNA; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; LYSINE; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; S-ADENOSYLHOMOCYSTEINE;

EID: 79961241001     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr019     Document Type: Article

References (51)

1. Bhaumik, S.R., Smith, E. and Shilatifard, A. (2007) Covalent modifications of histones during development and disease pathogenesis. Nat. Struct. Mol. Biol., 14, 1008-1016. (Pubitemid 350060343)
2. Martin, C. and Zhang, Y. (2005) The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol., 6, 838-849. (Pubitemid 41568733)
3. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C.P., Allis, C.D. et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature, 406, 593-599. (Pubitemid 30641039)
4. Roguev, A., Schaft, D., Shevchenko, A., Pijnappel, W.W., Wilm, M., Aasland, R. and Stewart, A.F. (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J., 20, 7137-7148. (Pubitemid 34062305)
5. Cheng, X., Collins, R.E. and Zhang, X. (2005) Structural and sequence motifs of protein (histone) methylation enzymes. Annu. Rev. Biophys. Biomol. Struct., 34, 267-294. (Pubitemid 40847726)
6. Hamamoto, R., Furukawa, Y., Morita, M., Iimura, Y., Silva, F.P., Li, M., Yagyu, R. and Nakamura, Y. (2004) SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat. Cell Biol., 6, 731-740. (Pubitemid 39144478)
7. Brown, M.A., Sims, R.J. 3rd, Gottlieb, P.D. and Tucker, P.W. (2006) Identification and characterization of Smyd2: a split SET/MYND domain-containing histone H3 lysine 36-specific methyltransferase that interacts with the Sin3 histone deacetylase complex. Mol. Cancer, 5, 26.
8. Tan, X., Rotllant, J., Li, H., De Deyne, P. and Du, S.J. (2006) SmyD1, a histone methyltransferase, is required for myofibril organization and muscle contraction in zebrafish embryos. Proc. Natl Acad. Sci. USA, 103, 2713-2718.
9. Abu-Farha, M., Lambert, J.P., Al-Madhoun, A.S., Elisma, F., Skerjanc, I.S. and Figeys, D. (2008) The tale of two domains: proteomics and genomics analysis of SMYD2, a new histone methyltransferase. Mol. Cell Proteomics, 7, 560-572. (Pubitemid 351472465)
10. Huang, J., Perez-Burgos, L., Placek, B.J., Sengupta, R., Richter, M., Dorsey, J.A., Kubicek, S., Opravil, S., Jenuwein, T. and Berger, S.L. (2006) Repression of p53 activity by Smyd2-mediated methylation. Nature, 444, 629-632. (Pubitemid 44864441)
11. Kunizaki, M., Hamamoto, R., Silva, F.P., Yamaguchi, K., Nagayasu, T., Shibuya, M., Nakamura, Y. and Furukawa, Y. (2007) The lysine 831 of vascular endothelial growth factor receptor 1 is a novel target of methylation by SMYD3. Cancer Res., 67, 10759-10765. (Pubitemid 350145903)
12. Noma, K., Allis, C.D. and Grewal, S.I. (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science, 293, 1150-1155. (Pubitemid 32758098)
13. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J. and Kouzarides, T. (2002) Active genes are tri-methylated at K4 of histone H3. Nature, 419, 407-411.
14. Schneider, R., Bannister, A.J., Myers, F.A., Thorne, A.W., Crane-Robinson, C. and Kouzarides, T. (2004) Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol., 6, 73-77. (Pubitemid 38425733)
15. Cao, Y. (2009) Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci. Signal, 2, re1.
16. Tsuge, M., Hamamoto, R., Silva, F.P., Ohnishi, Y., Chayama, K., Kamatani, N., Furukawa, Y. and Nakamura, Y. (2005) A variable number of tandem repeats polymorphism in an E2F-1 binding element in the 50 flanking region of SMYD3 is a risk factor for human cancers. Nat. Genet., 37, 1104-1107. (Pubitemid 41486663)
17. Wu, H., Min, J., Lunin, V.V., Antoshenko, T., Dombrovski, L., Zeng, H., Allali-Hassani, A., Campagna-Slater, V., Vedadi, M., Arrowsmith, C.H. et al. (2010) Structural biology of human H3K9 methyltransferases. PLoS One, 5, e8570.
18. Jacobs, S.A., Harp, J.M., Devarakonda, S., Kim, Y., Rastinejad, F. and Khorasanizadeh, S. (2002) The active site of the SET domain is constructed on a knot. Nat. Struct. Biol., 9, 833-838. (Pubitemid 35257783)
19. Min, J., Zhang, X., Cheng, X., Grewal, S.I. and Xu, R.M. (2002) Structure of the SET domain histone lysine methyltransferase Clr4. Nat. Struct. Biol., 9, 828-832. (Pubitemid 35257782)
20. Trievel, R.C., Beach, B.M., Dirk, L.M., Houtz, R.L. and Hurley, J.H. (2002) Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell, 111, 91-103.
21. Wilson, J.R., Jing, C., Walker, P.A., Martin, S.R., Howell, S.A., Blackburn, G.M., Gamblin, S.J. and Xiao, B. (2002) Crystal structure and functional analysis of the histone methyltransferase SET7/9. Cell, 111, 105-115.
22. Zhang, X., Tamaru, H., Khan, S.I., Horton, J.R., Keefe, L.J., Selker, E.U. and Cheng, X. (2002) Structure of the Neurospora SET domain protein DIM-5, a histone H3 lysine methyltransferase. Cell, 111, 117-127.
23. Kwon, T., Chang, J.H., Kwak, E., Lee, C.W., Joachimiak, A., Kim, Y.C., Lee, J. and Cho, Y. (2003) Mechanism of histone lysine methyl transfer revealed by the structure of SET7/9-AdoMet. EMBO J., 22, 292-303. (Pubitemid 36119435)
24. Manzur, K.L., Farooq, A., Zeng, L., Plotnikova, O., Koch, A.W., Sachchidanand and Zhou, M.M. (2003) A dimeric viral SET domain methyltransferase specific to Lys27 of histone H3. Nat. Struct. Biol., 10, 187-196. (Pubitemid 36297988)
25. Xiao, B., Jing, C., Wilson, J.R., Walker, P.A., Vasisht, N., Kelly, G., Howell, S., Taylor, I.A., Blackburn, G.M. and Gamblin, S.J. (2003) Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature, 421, 652-656. (Pubitemid 36227675)
26. Xiao, B., Jing, C., Kelly, G., Walker, P.A., Muskett, F.W., Frenkiel, T.A., Martin, S.R., Sarma, K., Reinberg, D., Gamblin, S.J. et al. (2005) Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev., 19, 1444-1454. (Pubitemid 41003011)
27. Qian, C., Wang, X., Manzur, K., Sachchidanand, Farooq, A., Zeng, L., Wang, R. and Zhou, M.M. (2006) Structural insights of the specificity and catalysis of a viral histone H3 lysine 27 methyltransferase. J. Mol. Biol., 359, 86-96.
28. Briknarova, K., Zhou, X., Satterthwait, A., Hoyt, D.W., Ely, K.R. and Huang, S. (2008) Structural studies of the SET domain from RIZ1 tumor suppressor. Biochem. Biophys. Res. Commun., 366, 807-813.
29. Southall, S.M., Wong, P.S., Odho, Z., Roe, S.M. and Wilson, J.R. (2009) Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol. Cell, 33, 181-191.
30. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326. (Pubitemid 27085611)
31. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., D54, 905-921.
32. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr., D60, 2126-2132. (Pubitemid 41742764)
33. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., D53, 240-255. (Pubitemid 27235885)
34. Laskowski, R.A., Macarthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
35. Chang, Y., Ganesh, T., Horton, J.R., Spannhoff, A., Liu, J., Sun, A., Zhang, X., Bedford, M.T., Shinkai, Y., Snyder, J.P. et al. (2010) Adding a lysine mimic in the design of potent inhibitors of histone lysine methyltransferases. J. Mol. Biol., 400, 1-7.
36. Chang, Y., Zhang, X., Horton, J.R., Upadhyay, A.K., Spannhoff, A., Liu, J., Snyder, J.P., Bedford, M.T. and Cheng, X. (2009) Structural basis for G9a-like protein lysine methyltransferase inhibition by BIX-01294. Nat. Struct. Mol. Biol., 16, 312-317.
37. Couture, J.F., Collazo, E., Brunzelle, J.S. and Trievel, R.C. (2005) Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev., 19, 1455-1465. (Pubitemid 41003012)
38. Zhang, X., Yang, Z., Khan, S.I., Horton, J.R., Tamaru, H., Selker, E.U. and Cheng, X. (2003) Structural basis for the product specificity of histone lysine methyltransferases. Mol. Cell, 12, 177-185. (Pubitemid 36957834)
39. Chen, S., Prapapanich, V., Rimerman, R.A., Honore, B. and Smith, D.F. (1996) Interactions of p60, a mediator of progesterone receptor assembly, with heat shock proteins hsp90 and hsp70. Mol. Endocrinol., 10, 682-693. (Pubitemid 26176276)
40. Pratt, W.B. and Toft, D.O. (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev., 18, 306-360. (Pubitemid 27246880)
41. Dolinski, K.J., Cardenas, M.E. and Heitman, J. (1998) CNS1 encodes an essential p60/Sti1 homolog in Saccharomyces cerevisiae that suppresses cyclophilin 40 mutations and interacts with Hsp90. Mol. Cell. Biol., 18, 7344-7352. (Pubitemid 28533054)
42. Marsh, J.A., Kalton, H.M. and Gaber, R.F. (1998) Cns1 is an essential protein associated with the hsp90 chaperone complex in Saccharomyces cerevisiae that can restore cyclophilin 40-dependent functions in cpr7Delta cells. Mol. Cell. Biol., 18, 7353-7359. (Pubitemid 28533055)
43. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F.U. and Moarefi, I. (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell, 101, 199-210. (Pubitemid 32004747)
44. Trievel, R.C., Flynn, E.M., Houtz, R.L. and Hurley, J.H. (2003) Mechanism of multiple lysine methylation by the SET domain enzyme Rubisco LSMT. Nat. Struct. Biol., 10, 545-552. (Pubitemid 36792906)
45. Guo, H.B. and Guo, H. (2007) Mechanism of histone methylation catalyzed by protein lysine methyltransferase SET7/9 and origin of product specificity. Proc. Natl Acad. Sci. USA, 104, 8797-8802. (Pubitemid 47175391)
46. Gross, C.T. and McGinnis, W. (1996) DEAF-1, a novel protein that binds an essential region in a Deformed response element. EMBO J., 15, 1961-1970. (Pubitemid 26119229)
47. Gottlieb, P.D., Pierce, S.A., Sims, R.J., Yamagishi, H., Weihe, E.K., Harriss, J.V., Maika, S.D., Kuziel, W.A., King, H.L., Olson, E.N. et al. (2002) Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat. Genet., 31, 25-32.
48. Ansieau, S. and Leutz, A. (2002) The conserved Mynd domain of BS69 binds cellular and oncoviral proteins through a common PXLXP motif. J. Biol. Chem., 277, 4906-4910. (Pubitemid 34968527)
49. Scarr, R.B. and Sharp, P.A. (2002) PDCD2 is a negative regulator of HCF-1 (C1). Oncogene, 21, 5245-5254. (Pubitemid 34948136)
50. Liu, Y., Chen, W., Gaudet, J., Cheney, M.D., Roudaia, L., Cierpicki, T., Klet, R.C., Hartman, K., Laue, T.M., Speck, N.A. et al. (2007) Structural basis for recognition of SMRT/N-CoR by the MYND domain and its contribution to AML1/ETO's activity. Cancer Cell, 11, 483-497. (Pubitemid 46856906)
51. Sawada, K., Yang, Z., Horton, J.R., Collins, R.E., Zhang, X. and Cheng, X. (2004) Structure of the conserved core of the yeast Dot1p, a nucleosomal histone H3 lysine 79 methyltransferase. J. Biol. Chem., 279, 43296-43306. (Pubitemid 39372225)