Structural basis for activity regulation of MLL family methyltransferases

Nature

Volumn 530, Issue 7591, 2016, Pages 447-452

  Li, Yanjing ^a,b   Han, Jianming ^a,b   Zhang, Yuebin ^c   Cao, Fang ^d   Liu, Zhijun ^a,b   Li, Shuai ^e   Wu, Jian ^a,b   Hu, Chunyi ^a,b   Wang, Yan ^a,b   Shuai, Jin ^a,b   Chen, Juan ^a,b   Cao, Liaoran ^c   Li, Dangsheng ^f   Shi, Pan ^b   Tian, Changlin ^b,g   Zhang, Jian ^e   Dou, Yali ^d   Li, Guohui ^c   Chen, Yong ^a,b   Lei, Ming ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^d UNIVERSITY OF MICHIGAN   (United States)

^e SHANGHAI JIAO TONG UNIVERSITY   (China)

^f Chinese Academy of Sciences   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CANCER; ENZYME ACTIVITY; GENE EXPRESSION; PLASTICITY; PROTEIN;

ASH2L PROTEIN, HUMAN; DNA BINDING PROTEIN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; MIXED LINEAGE LEUKEMIA PROTEIN; MLL PROTEIN, HUMAN; MLL3 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; MUTANT PROTEIN; NUCLEAR PROTEIN; PROTEIN BINDING; RBBP5 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; WDR5 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTANT PROTEINS; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS;

EID: 84959348993     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16952     Document Type: Article

References (41)

1. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
2. Shilatifard, A. Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr. Opin. Cell Biol. 20, 341-348 (2008).
3. Ruthenburg, A. J., Allis, C. D., Wysocka, J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25, 15-30 (2007).
4. Ansari, K. I., Mandal, S. S. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS J. 277, 1790-1804 (2010).
5. Wang, P. et al. Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol. Cell. Biol. 29, 6074-6085 (2009).
6. Krivtsov, A. V., Armstrong, S. A. MLL translocations, histone modifications and leukaemia stem-cell development. Nature Rev. Cancer 7, 823-833 (2007).
7. Ansari, K. I., Mishra, B. P., Mandal, S. S. MLL histone methylases in gene expression, hormone signaling and cell cycle. Front. Biosci. 14, 3483-3495 (2009).
8. Parsons, D. W. et al. The genetic landscape of the childhood cancer medulloblastoma. Science 331, 435-439 (2011).
9. Morin, R. D. et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476, 298-303 (2011).
10. Li, Y. et al. A mutation screen in patients with Kabuki syndrome. Hum. Genet. 130, 715-724 (2011).
11. Pleasance, E. D. et al. A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463, 184-190 (2010).
12. Dalgliesh, G. L. et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 463, 360-363 (2010).
13. Dou, Y. et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nature Struct. Mol. Biol. 13, 713-719 (2006).
14. Patel, A., Dharmarajan, V., Vought, V. E., Cosgrove, M. S. On the mechanism of multiple lysine methylation by the human mixed lineage leukemia protein-1 (MLL1) core complex. J. Biol. Chem. 284, 24242-24256 (2009).
15. Southall, S. M., Wong, P. S., Odho, Z., Roe, S. M., Wilson, J. R. Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol. Cell 33, 181-191 (2009).
16. Steward, M. M. et al. Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nature Struct. Mol. Biol. 13, 852-854 (2006).
17. Dou, Y., Hess, J. L. Mechanisms of transcriptional regulation by MLL and its disruption in acute leukemia. Int. J. Hematol. 87, 10-18 (2008).
18. Wysocka, J. et al. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121, 859-872 (2005).
19. Cao, F. et al. An Ash2L/RbBP5 heterodimer stimulates the MLL1 methyltransferase activity through coordinated substrate interactions with the MLL1 SET domain. PLoS ONE 5, e14102 (2010).
20. Shinsky, S. A., Monteith, K. E., Viggiano, S., Cosgrove, M. S. Biochemical reconstitution and phylogenetic comparison of human SET1 family core complexes involved in histone methylation. J. Biol. Chem. 290, 6361-6375 (2015).
21. Shinsky, S. A., Cosgrove, M. S. Unique role of the WD-40 repeat protein 5 (WDR5) subunit within the mixed lineage leukemia 3 (MLL3) histone methyltransferase complex. J. Biol. Chem. 290, 25819-25833 (2015).
22. Zhang, P., Lee, H., Brunzelle, J. S., Couture, J. F. The plasticity of WDR5 peptide-binding cleft enables the binding of the SET1 family of histone methyltransferases. Nucleic Acids Res. 40, 4237-4246 (2012).
23. Zhang, P. et al. A phosphorylation switch on RBBP5 regulates histone H3 Lys4 methylation. Genes Dev. 29, 123-128 (2015).
24. Chen, Y., Cao, F., Wan, B., Dou, Y., Lei, M. Structure of the SPRY domain of human Ash2L and its interactions with RbBP5 and DPY30. Cell Res. 22, 598-602 (2012).
25. Odho, Z., Southall, S. M., Wilson, J. R. 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, 32967-32976 (2010).
26. Zhang, Y. et al. evolving catalytic properties of the MLL family set domain. Structure 23, 1921-1933 (2015).
27. Cheng, X., Collins, R. E., Zhang, X. Structural and sequence motifs of protein (histone) methylation enzymes. Annu. Rev. Biophys. Biomol. Struct. 34, 267-294 (2005).
28. Zhang, X. et al. Structural basis for the product specificity of histone lysine methyltransferases. Mol. Cell 12, 177-185 (2003).
29. Sirinupong, N., Brunzelle, J., Doko, E., Yang, Z. Structural insights into the autoinhibition and posttranslational activation of histone methyltransferase SmyD3. J. Mol. Biol. 406, 149-159 (2011).
30. Wang, K. C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120-124 (2011).
31. Ang, Y. S. et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145, 183-197 (2011).
32. Gan, Q. et al. WD repeat-containing protein 5, a ubiquitously expressed histone methyltransferase adaptor protein, regulates smooth muscle cell-selective gene activation through interaction with pituitary homeobox 2. J. Biol. Chem. 286, 21853-21864 (2011).
33. Dou, Y. et al. Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121, 873-885 (2005).
34. Thompson, B. A., Tremblay, V., Lin, G., Bochar, D. A. CHD8 is an ATPdependent chromatin remodeling factor that regulates ?-catenin target genes. Mol. Cell. Biol. 28, 3894-3904 (2008).
35. Otwinowski, Z., Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
36. Vonrhein, C., Blanc, E., Roversi, P., Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
37. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
38. Emsley, P., Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
39. Storoni, L. C., McCoy, A. J., Read, R. J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D 60, 432-438 (2004).
40. Shi, P. et al. Site-specific 19F NMR chemical shift and side chain relaxation analysis of a membrane protein labeled with an unnatural amino acid. Protein Sci. 20, 224-228 (2011).
41. Lindahl, E., Azuara, C., Koehl, P., Delarue, M. NOMAD-Ref: visualization, deformation and refinement of macromolecular structures based on all-atom normal mode analysis. Nucleic Acids Res. 34, W52-W56 (2006).