Structural insight into autoinhibition and histone H3-induced activation of DNMT3A

Nature

Volumn 517, Issue 7536, 2015, Pages 640-644

  Guo, Xue ^a,b   Wang, Ling ^a,b   Li, Jie ^a   Ding, Zhanyu ^c   Xiao, Jianxiong ^a   Yin, Xiaotong ^a   He, Shuang ^a   Shi, Pan ^c,d,e   Dong, Liping ^f,g   Li, Guohong ^f   Tian, Changlin ^c,d,e   Wang, Jiawei ^h   Cong, Yao ^c   Xu, Yanhui ^a,b  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b FUDAN UNIVERSITY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

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

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

^f INSTITUTE OF BIOPHYSICS   (China)

^g UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^h Peking University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3L; GLUTATHIONE TRANSFERASE; HISTONE H3; HYDROGEN; UNCLASSIFIED DRUG; DNA; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNMT3L PROTEIN, HUMAN; HISTONE;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA METHYLATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORINE NUCLEAR MAGNETIC RESONANCE; GEL MOBILITY SHIFT ASSAY; HUMAN; HYDROGEN BOND; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY; XENOPUS LAEVIS;

ANIMALS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENZYME ACTIVATION; HISTONES; HUMANS; MICE; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; XENOPUS LAEVIS;

EID: 84925511390     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13899     Document Type: Article

References (43)

1. Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genet. 33 (suppl.),245-254 (2003).
2. Smith, Z. D. & Meissner, A. DNA methylation: roles in mammalian development. Nature Rev. Genet. 14, 204-220 (2013).
3. Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11, 204-220 (2010).
4. Guibert, S., Forne, T. & Weber, M. Dynamic regulation of DNA methylation during mammalian development. Epigenomics 1, 81-98 (2009).
5. Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21 (2002).
6. Okano, M., Xie, S. & Li, E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nature Genet. 19, 219-220 (1998).
7. Okano, M., Bell, D. W., Haber, D. A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novomethylation andmammalian development. Cell 99, 247-257 (1999).
8. Bestor, T. H. The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395-2402 (2000).
9. Laurent, L. et al. Dynamic changes in the humanmethylome during differentiation. Genome Res. 20, 320-331 (2010).
10. Lister, R. et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322 (2009).
11. Bird, A. P. & Taggart, M. H. Variable patterns of total DNA and rDNA methylation in animals. Nucleic Acids Res. 8, 1485-1497 (1980).
12. Ehrlich, M. et al. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res. 10, 2709-2721 (1982).
13. Chedin, F., Lieber, M. R. & Hsieh, C. L. The DNA methyltransferase-like protein DNMT3L stimulates de novomethylation by Dnmt3a. Proc. Natl Acad. Sci. USA 99, 16916-16921 (2002).
14. Cedar, H. & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nature Rev. Genet. 10, 295-304 (2009).
15. Ooi, S. K. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717 (2007).
16. Otani, J. et al. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 10, 1235-1241 (2009).
17. Zhang, Y. et al. 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 (2010).
18. Li, B. Z. et al. Histone tails regulate DNA methylation by allosterically activating de novo methyltransferase. Cell Res. 21, 1172-1181 (2011).
19. Weber, M. et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nature Genet. 39, 457-466 (2007).
20. Meissner, A. et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770 (2008).
21. Chen, T., Ueda, Y., Xie, S. & Li, E. A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation. J. Biol. Chem. 277, 38746-38754 (2002).
22. Jia, D., Jurkowska, R. Z., Zhang, X., Jeltsch, A. & Cheng, X. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251 (2007).
23. Klimasauskas, S., Kumar, S., Roberts, R. J. & Cheng, X. HhaImethyltransferase flips its target base out of the DNA helix. Cell 76, 357-369 (1994).
24. Rajavelu, A., Jurkowska, R. Z., Fritz, J. & Jeltsch, A. Function and disruption of DNA methyltransferase 3a cooperative DNA binding and nucleoprotein filament formation. Nucleic Acids Res. 40, 569-580 (2012).
25. Shi, P. et al. Site-specific protein backbone and side-chainNMR chemical shift and relaxation analysis of human vinexin SH3 domain using a genetically encoded 15N/19F-labeled unnatural amino acid. Biochem. Biophys. Res. Commun. 402, 461-466 (2010).
26. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
27. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007).
28. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
29. Vagin, A. & Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 30, 1022-1025 (1997).
30. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
31. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. PROCHECK: a programto check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291 (1993).
32. DeLano, W. L. The PyMOL Molecular Graphics System. http://www.pymol.org (2002).
33. Roth, M.& Jeltsch, A. Biotin-avidin microplate assay for the quantitative analysis of enzymatic methylation of DNA by DNA methyltransferases. Biol. Chem. 381, 269-272 (2000).
34. Luger, K., Rechsteiner, T. J. & Richmond, T. J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119, 1-16 (1999).
35. Simon, M. D. et al. The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 128, 1003-1012 (2007).
36. Shi, P. et al. Site-specific (1)(9)F NMR chemical shift and side chain relaxation analysis of a membrane protein labeled with an unnatural amino acid. Protein Sci. 20, 224-228 (2011).
37. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
38. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
39. Ludtke, S. J., Jakana, J., Song, J. L., Chuang, D. T. & Chiu, W. A 11.5A° single particle reconstruction of GroEL using EMAN. JMB (2001).
40. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R. & Schatz, M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24 (1996).
41. Cong, Y.&Ludtke, S. J. Single particle analysis at high resolution.Methods Enzymol. 482, 211-235 (2010).
42. Cong, Y. et al. 4.0-A° resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement. Proc. Natl Acad. Sci. USA 107, 4967-4972 (2010).
43. Pettersen, E. F. et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).