Evolving catalytic properties of the MLL family SET domain

Structure

Volumn 23, Issue 10, 2015, Pages 1921-1933

  Zhang, Ying ^a   Mittal, Anshumali ^a   Reid, James ^b   Reich, Stephanie ^b   Gamblin, Steven J ^a   Wilson, Jon R ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b Domainex Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; METHYL GROUP; METHYLTRANSFERASE; MIXED LINEAGE LEUKEMIA PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN 1; MIXED LINEAGE LEUKEMIA PROTEIN 4; MULTIPROTEIN COMPLEX; PHENYLALANINE; TETRAPEPTIDE; UNCLASSIFIED DRUG; CHROMATIN; DNA BINDING PROTEIN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HYBRID PROTEIN; MLL PROTEIN, HUMAN; MLL4 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; CATALYSIS; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME MECHANISM; GENE TARGETING; HUMAN; INTRINSIC ACTIVITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BIOCATALYSIS; CHEMISTRY; CHROMATIN; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SF9 CELL LINE; SPODOPTERA; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BIOCATALYSIS; CHROMATIN; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; KINETICS; LYSINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYELOID-LYMPHOID LEUKEMIA PROTEIN; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SF9 CELLS; SPODOPTERA;

EID: 84943585360     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.07.018     Document Type: Article

References (58)

1. V. Avdic, P. Zhang, S. Lanouette, A. Groulx, V. Tremblay, J. Brunzelle, and J.F. Couture Structural and biochemical insights into MLL1 core complex assembly Structure 19 2011 101 108
2. S. Bailey The Ccp4 suite - programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
3. A.J. Bannister, and T. Kouzarides Regulation of chromatin by histone modifications Cell Res. 21 2011 381 395
4. I. Berger, D.J. Fitzgerald, and T.J. Richmond Baculovirus expression system for heterologous multiprotein complexes Nat. Biotechnol. 22 2004 1583 1587
5. A.S. Bledau, K. Schmidt, K. Neumann, U. Hill, G. Ciotta, A. Gupta, D.C. Torres, J. Fu, A. Kranz, A.F. Stewart, and et al. The H3K4 methyltransferase Setd1a is first required at the epiblast stage, whereas Setd1b becomes essential after gastrulation Development 141 2014 1022 1035
6. F. Cao, E.C. Townsend, H. Karatas, J. Xu, L. Li, S. Lee, L. Liu, Y. Chen, P. Ouillette, J. Zhu, and et al. Targeting MLL1 H3K4 methyltransferase activity in mixed-lineage leukemia Mol. Cell 53 2014 247 261
7. M.S. Cosgrove, and A. Patel Mixed lineage leukemia: a structure-function perspective of the MLL1 protein FEBS J. 277 2010 1832 1842
8. J.F. Couture, and G. Skiniotis Assembling a COMPASS Epigenetics 8 2013 349 354
9. J.F. Couture, E. Collazo, J.S. Brunzelle, and R.C. Trievel Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase Genes Dev. 19 2005 1455 1465
10. J.F. Couture, L.M. Dirk, J.S. Brunzelle, R.L. Houtz, and R.C. Trievel Structural origins for the product specificity of SET domain protein methyltransferases Proc. Natl. Acad. Sci. USA 105 2008 20659 20664
11. P.M. Dehe, B. Dichtl, D. Schaft, A. Roguev, M. Pamblanco, R. Lebrun, A. Rodriguez-Gil, M. Mkandawire, K. Landsberg, A. Shevchenko, and et al. Protein interactions within the Set1 complex and their roles in the regulation of histone 3 lysine 4 methylation J. Biol. Chem. 281 2006 35404 35412
12. S. Denissov, H. Hofemeister, H. Marks, A. Kranz, G. Ciotta, S. Singh, K. Anastassiadis, H.G. Stunnenberg, and A.F. Stewart Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant Development 141 2014 526 537
13. S.C. Dillon, X. Zhang, R.C. Trievel, and X. Cheng The SET-domain protein superfamily: protein lysine methyltransferases Genome Biol. 6 2005 227
14. Y. Dou, and J.L. Hess Mechanisms of transcriptional regulation by MLL and its disruption in acute leukemia Int. J. Hematol. 87 2008 10 18
15. Y. Dou, T.A. Milne, A.J. Ruthenburg, S. Lee, J.W. Lee, G.L. Verdine, C.D. Allis, and R.G. Roeder Regulation of MLL1 H3K4 methyltransferase activity by its core components Nat. Struct. Mol. Biol. 13 2006 713 719
16. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
17. P. Ernst, and C.R. Vakoc WRAD: enabler of the SET1-family of H3K4 methyltransferases Brief. Funct. Genomics 11 2012 217 226
18. R.J. Frandsen, J.A. Andersson, M.B. Kristensen, and H. Giese Efficient four fragment cloning for the construction of vectors for targeted gene replacement in filamentous fungi BMC Mol. Biol. 9 2008 70
19. K. Guitot, S. Scarabelli, T. Drujon, G. Bolbach, M. Amoura, F. Burlina, A. Jeltsch, S. Sagan, and D. Guianvarc'h Label-free measurement of histone lysine methyltransferases activity by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry Anal. Biochem. 456 2014 25 31
20. C. Guo, C.C. Chang, M. Wortham, L.H. Chen, D.N. Kernagis, X. Qin, Y.W. Cho, J.T. Chi, G.A. Grant, R.E. Mclendon, and et al. Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways Proc. Natl. Acad. Sci. USA 109 2012 17603 17608
21. G. Hallson, R.E. Hollebakken, T. Li, M. Syrzycka, I. Kim, S. Cotsworth, K.A. Fitzpatrick, D.A. Sinclair, and B.M. Honda dSet1 is the main H3K4 di- and tri-methyltransferase throughout Drosophila development Genetics 190 2012 91 100
22. D. Hu, A.S. Garruss, X. Gao, M.A. Morgan, M. Cook, E.R. Smith, and A. Shilatifard The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells Nat. Struct. Mol. Biol. 20 2013 1093 1097
23. I. Issaeva, Y. Zonis, T. Rozovskaia, K. Orlovsky, C.M. Croce, T. Nakamura, A. Mazo, L. Eisenbach, and E. Canaani Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth Mol. Cell. Biol. 27 2007 1889 1903
24. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
25. T. Kusch Histone H3 lysine 4 methylation revisited Transcription 3 2012 310 314
26. J.E. Lee, C. Wang, S. Xu, Y.W. Cho, L. Wang, X. Feng, A. Baldridge, V. Sartorelli, L. Zhuang, W. Peng, and et al. H3K4 mono- and di-methyltransferase MLL4 is required for enhancer activation during cell differentiation Elife 2 2013 e01503
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. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
29. H. McWilliam, W. Li, M. Uludag, S. Squizzato, Y.M. Park, N. Buso, A.P. Cowley, and R. Lopez Analysis tool web services from the EMBL-EBI Nucleic Acids Res. 41 2013 W597 W600
30. L. Micale, B. Augello, C. Maffeo, A. Selicorni, F. Zucchetti, C. Fusco, P. De Nittis, M.T. Pellico, B. Mandriani, R. Fischetto, and et al. Molecular analysis, pathogenic mechanisms, and readthrough therapy on a large cohort of Kabuki syndrome patients Hum. Mutat. 35 2014 841 850
31. T. Miller, N.J. Krogan, J. Dover, H. Erdjument-Bromage, P. Tempst, M. Johnston, J.F. Greenblatt, and A. Shilatifard COMPASS: a complex of proteins associated with a trithorax-related SET domain protein Proc. Natl. Acad. Sci. USA 98 2001 12902 12907
32. M.A. Morgan, and A. Shilatifard Drosophila SETs its sights on cancer: Trr/MLL3/4 COMPASS-like complexes in development and disease Mol. Cell. Biol. 33 2013 1698 1701
33. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
34. Z. Odho, S.M. Southall, and J.R. Wilson Characterization of a novel WDR5-binding site that recruits RbBP5 through a conserved motif to enhance methylation of histone H3 lysine 4 by mixed lineage leukemia protein-1 J. Biol. Chem. 285 2010 32967 32976
35. A. Patel, V.E. Vought, V. Dharmarajan, and M.S. Cosgrove A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex J. Biol. Chem. 283 2008 32162 32175
36. A. Patel, V.E. Vought, V. Dharmarajan, and M.S. Cosgrove A novel non-SET domain multi-subunit methyltransferase required for sequential nucleosomal histone H3 methylation by the mixed lineage leukemia protein-1 (MLL1) core complex J. Biol. Chem. 286 2011 3359 3369
37. S. Reich, L.H. Puckey, C.L. Cheetham, R. Harris, A.A. Ali, U. Bhattacharyya, K. Maclagan, K.A. Powell, C. Prodromou, L.H. Pearl, and et al. Combinatorial domain hunting: an effective approach for the identification of soluble protein domains adaptable to high-throughput applications Protein Sci. 15 2006 2356 2365
38. A. Roguev, D. Schaft, A. Shevchenko, W.W. Pijnappel, M. Wilm, R. Aasland, and A.F. Stewart The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4 EMBO J. 20 2001 7137 7148
39. A.J. Ruthenburg, C.D. Allis, and J. Wysocka Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark Mol. Cell 25 2007 15 30
40. A. Schlichter, and B.R. Cairns Histone trimethylation by Set1 is coordinated by the RRM, autoinhibitory, and catalytic domains EMBO J. 24 2005 1222 1231
41. A. Shilatifard The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis Annu. Rev. Biochem. 81 2012 65 95
42. S.A. Shinsky, M. Hu, V.E. Vought, S.B. Ng, M.J. Bamshad, J. Shendure, and M.S. Cosgrove A non-active-site SET domain surface crucial for the interaction of MLL1 and the RbBP5/Ash2L heterodimer within MLL family core complexes J. Mol. Biol. 426 2014 2283 2299
43. S.A. Shinsky, K.E. Monteith, S. Viggiano, and M.S. Cosgrove Biochemical reconstitution and phylogenetic comparison of human SET1 family core complexes involved in histone methylation J. Biol. Chem. 290 2015 6361 6375
44. E. Smith, C. Lin, and A. Shilatifard The super elongation complex (SEC) and MLL in development and disease Genes Dev. 25 2011 661 672
45. S.M. Southall, P.S. Wong, Z. Odho, S.M. Roe, and J.R. Wilson Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks Mol. Cell 33 2009 181 191
46. Y.H. Takahashi, G.H. Westfield, A.N. Oleskie, R.C. Trievel, A. Shilatifard, and G. Skiniotis Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human Proc. Natl. Acad. Sci. USA 108 2011 20526 20531
47. V. Tremblay, P. Zhang, C.P. Chaturvedi, J. Thornton, J.S. Brunzelle, G. Skiniotis, A. Shilatifard, M. Brand, and J.F. Couture Molecular basis for DPY-30 association to COMPASS-like and NURF complexes Structure 22 2014 1821 1830
48. R. Van Nuland, A.H. Smits, P. Pallaki, P.W. Jansen, M. Vermeulen, and H.T. Timmers Quantitative dissection and stoichiometry determination of the human SET1/MLL histone methyltransferase complexes Mol. Cell. Biol. 33 2013 2067 2077
49. H. Wu, J. Min, V.V. Lunin, T. Antoshenko, L. Dombrovski, H. Zeng, A. Allali-Hassani, V. Campagna-Slater, M. Vedadi, C.H. Arrowsmith, and et al. Structural biology of human H3K9 methyltransferases PLoS One 5 2010 e8570
50. H. Wu, H. Zeng, A. Dong, F. Li, H. He, G. Senisterra, A. Seitova, S. Duan, P.J. Brown, M. Vedadi, and et al. Structure of the catalytic domain of EZH2 reveals conformational plasticity in cofactor and substrate binding sites and explains oncogenic mutations PLoS One 8 2013 e83737
51. L. Wu, S.Y. Lee, B. Zhou, U.T. Nguyen, T.W. Muir, S. Tan, and Y. Dou ASH2L regulates ubiquitylation signaling to MLL: trans-regulation of H3 K4 methylation in higher eukaryotes Mol. Cell 49 2013 1108 1120
52. B. Xiao, C. Jing, J.R. Wilson, P.A. Walker, N. Vasisht, G. Kelly, S. Howell, I.A. Taylor, G.M. Blackburn, and S.J. Gamblin Structure and catalytic mechanism of the human histone methyltransferase SET7/9 Nature 421 2003 652 656
53. B. Xiao, J.R. Wilson, and S.J. Gamblin SET domains and histone methylation Curr. Opin. Struct. Biol. 13 2003 699 705
54. A. Yokoyama, Z. Wang, J. Wysocka, M. Sanyal, D.J. Aufiero, I. Kitabayashi, W. Herr, and M.L. Cleary Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression Mol. Cell. Biol. 24 2004 5639 5649
55. X. Zhang, H. Tamaru, S.I. Khan, J.R. Horton, L.J. Keefe, E.U. Selker, and X. Cheng Structure of the Neurospora SET domain protein DIM-5, a histone H3 lysine methyltransferase Cell 111 2002 117 127
56. 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
57. P. Zhang, H. Lee, J.S. Brunzelle, and J.F. Couture The plasticity of WDR5 peptide-binding cleft enables the binding of the SET1 family of histone methyltransferases Nucleic Acids Res. 40 2012 4237 4246
58. P. Zhang, C.P. Chaturvedi, V. Tremblay, M. Cramet, J.S. Brunzelle, G. Skiniotis, M. Brand, A. Shilatifard, and J.F. Couture A phosphorylation switch on RbBP5 regulates histone H3 Lys4 methylation Genes Dev. 29 2015 123 128