The structural basis of modified nucleosome recognition by 53BP1

Nature

Volumn 536, Issue 7614, 2016, Pages 100-103

  Wilson, Marcus D ^a   Benlekbir, Samir ^b   Fradet Turcotte, Amélie ^a,d,e   Sherker, Alana ^a,c   Julien, Jean Philippe ^b,c   McEwan, Andrea ^a   Noordermeer, Sylvie M ^a   Sicheri, Frank ^a,c   Rubinstein, John L ^b,c   Durocher, Daniel ^a,c  

^a MOUNT SINAI HOSPITAL   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d Université Laval   (Canada)

^e UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

53BP1 PROTEIN; ALANINE; ARGININE; BINDING PROTEIN; GLUTAMIC ACID; GLUTATHIONE TRANSFERASE; HISTONE H4; LYSINE; UBIQUITIN; UNCLASSIFIED DRUG; HISTONE; NUCLEOSOME; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN;

CHROMOSOME; DNA; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; PEPTIDE; PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MUTATION; NUCLEOSOME; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIZE EXCLUSION CHROMATOGRAPHY; STOICHIOMETRY; SURFACE PROPERTY; CHEMICAL STRUCTURE; CHEMISTRY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME SPECIFICITY; GENETICS; METABOLISM; METHYLATION; PLIABILITY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; UBIQUITINATION; ULTRASTRUCTURE;

CRYOELECTRON MICROSCOPY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; METHYLATION; MODELS, MOLECULAR; NUCLEOSOMES; PLIABILITY; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITINATION;

EID: 84982791184     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18951     Document Type: Article

References (48)

1. Lukas, J., Lukas, C., Bartek, J. More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nature Cell Biol. 13, 1161-1169 (2011).
2. Dantuma, N. P., van Attikum, H. Spatiotemporal regulation of posttranslational modifications in the DNA damage response. EMBO J. 35, 6-23 (2016).
3. Jackson, S. P., Durocher, D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795-807 (2013).
4. Thorslund, T. et al. Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527, 389-393 (2015).
5. Stewart, G. S. et al. The RIDDLE syndrome protein mediates a ubiquitindependent signaling cascade at sites of DNA damage. Cell 136, 420-434 (2009).
6. Doil, C. et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446 (2009).
7. Mattiroli, F. et al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182-1195 (2012).
8. Gatti, M. et al. A novel ubiquitin mark at the N-terminal tail of histone H2As targeted by RNF168 ubiquitin ligase. Cell Cycle 11, 2538-2544 (2012).
9. Panier, S., Boulton, S. J. Double-strand break repair: 53BP1 comes into focus. Nature Rev. Mol. Cell Biol. 15, 7-18 (2014).
10. Fradet-Turcotte, A. et al. 53BP1 is a reader of the DNA-damage-induced H2A lys 15 ubiquitin mark. Nature 499, 50-54 (2013).
11. Botuyan, M. V. et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373 (2006).
12. Simon, M. D. et al. The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 128, 1003-1012 (2007).
13. Mattiroli, F., Uckelmann, M., Sahtoe, D. D., van Dijk, W. J., Sixma, T. K. The nucleosome acidic patch plays a critical role in RNF168-dependent ubiquitination of histone H2A. Nature Commun. 5, 3291 (2014).
14. Vasudevan, D., Chua, E. Y., Davey, C. A. Crystal structures of nucleosome core particles containing the '601' strong positioning sequence. J. Mol. Biol. 403, 1-10 (2010).
15. McGinty, R. K., Henrici, R. C., Tan, S. Crystal structure of the PRC1 ubiquitylation module bound to the nucleosome. Nature 514, 591-596 (2014).
16. Armache, K. J., Garlick, J. D., Canzio, D., Narlikar, G. J., Kingston, R. E. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution. Science 334, 977-982 (2011).
17. Arnaudo, N. et al. The N-terminal acetylation of Sir3 stabilizes its binding to the nucleosome core particle. Nature Struct. Mol. Biol. 20, 1119-1121 (2013).
18. Makde, R. D., England, J. R., Yennawar, H. P., Tan, S. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467, 562-566 (2010).
19. Barbera, A. J. et al. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311, 856-861 (2006).
20. Davey, C. A., Sargent, D. F., Luger, K., Maeder, A. W., Richmond, T. J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319, 1097-1113 (2002).
21. Long, L., Furgason, M., Yao, T. Generation of nonhydrolyzable ubiquitinhistone mimics. Methods 70, 134-138 (2014).
22. Baarends, W. M. et al. Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with derepression of the X chromosome. J. Cell Sci. 120, 1841-1851 (2007).
23. Pavri, R. et al. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125, 703-717 (2006).
24. Nakamura, K. et al. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol. Cell 41, 515-528 (2011).
25. Zeng, M. et al. CRL4(Wdr70) regulates H2B monoubiquitination and facilitates Exo1-dependent resection. Nature Commun. 7, 11364 (2016).
26. Iwasaki, W. et al. Comprehensive structural analysis of mutant nucleosomes containing lysine to glutamine (KQ) substitutions in the H3 and H4 histonefold domains. Biochemistry 50, 7822-7832 (2011).
27. Leung, J. W. et al. Nucleosome acidic patch promotes RNF168-and RING1B/BMI1-dependent H2AX and H2A ubiquitination and DNA damage signaling. PLoS Genet. 10, e1004178 (2014).
28. Morgan, M. T. et al. Structural basis for histone H2B deubiquitination by the SAGA DUB module. Science 351, 725-728 (2016).
29. Adkins, N. L., Niu, H., Sung, P., Peterson, C. L. Nucleosome dynamics regulates DNA processing. Nature Struct. Mol. Biol. 20, 836-842 (2013).
30. Kucukelbir, A., Sigworth, F. J., Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
31. Juang, Y. C. et al. OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol. Cell 45, 384-397 (2012).
32. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44 (2004).
33. Simon, T. W. et al. The use of mode of action information in risk assessment: quantitative key events/dose-response framework for modeling the dose-response for key events. Crit. Rev. Toxicol. 44 (Suppl 3), 17-43 (2014).
34. Orthwein, A. et al. A mechanism for the suppression of homologous recombination in G1 cells. Nature 528, 422-426 (2015).
35. Marr, C. R., Benlekbir, S., Rubinstein, J. L. Fabrication of carbon films with ? 500nm holes for cryo-EM with a direct detector device. J. Struct. Biol. 185, 42-47 (2014).
36. Tivol, W. F., Briegel, A., Jensen, G. J. An improved cryogen for plunge freezing. Microsc. Microanal. 14, 375-379 (2008).
37. Rubinstein, J. L., Brubaker, M. A. Alignment of cryo-EM movies of individual particles by optimization of image translations. J. Struct. Biol. 192, 188-195 (2015).
38. Mindell, J. A., Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
39. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
40. Zhao, J., Brubaker, M. A., Benlekbir, S., Rubinstein, J. L. Description and comparison of algorithms for correcting anisotropic magnification in cryo-EM images. J. Struct. Biol. 192, 209-215 (2015).
41. Rosenthal, P. B., Henderson, R. Optimal determination of particle orientation, absolute hand, contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721-745 (2003).
42. Ramage, R. et al. Synthetic, structural and biological studies of the ubiquitin system: the total chemical synthesis of ubiquitin. Biochem. J. 299, 151-158 (1994).
43. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
44. Emsley, P., Lohkamp, B., Scott, W. G., Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
45. Kim, D. E., Chivian, D., Baker, D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32, W526-W531 (2004).
46. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
47. Rufer, A. C., Thiebach, L., Baer, K., Klein, H. W., Hennig, M. X-ray structure of glutathione S-transferase from Schistosoma japonicum in a new crystal form reveals flexibility of the substrate-binding site. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 263-265 (2005).
48. Weeks, S. D., Grasty, K. C., Hernandez-Cuebas, L., Loll, P. J. Crystal structures of Lys-63-linked tri-and di-ubiquitin reveal a highly extended chain architecture. Proteins 77, 753-759 (2009).