Structural plasticity of methyllysine recognition by the tandem Tudor domain of 53BP1

Structure

Volumn 23, Issue 2, 2015, Pages 312-321

  Tong, Qiong ^a   Cui, Gaofeng ^b   Botuyan, Maria Victoria ^b   Rothbart, Scott B ^c   Hayashi, Ryo ^d   Musselman, Catherine A ^a   Singh, Namit ^b   Appella, Ettore ^d   Strahl, Brian D ^c   Mer, Georges ^b   Kutateladze, Tatiana G ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; HISTONE; PROTEIN; PROTEIN 53BP1; PROTEIN P53; UNCLASSIFIED DRUG; LYSINE; MULTIPROTEIN COMPLEX; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; DNA DAMAGE; FLUORESCENCE SPECTROSCOPY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROGEN BOND; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; OLIGOMERIZATION; PLASTICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; DNA METHYLATION; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; DNA METHYLATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSINE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PROTEIN STRUCTURE, TERTIARY;

EID: 84930189683     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.11.013     Document Type: Article

References (51)

1. M.V. Botuyan, J. Lee, I.M. Ward, J.E. Kim, J.R. Thompson, J. Chen, and G. Mer Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair Cell 127 2006 1361 1373
2. R. Brosh, and V. Rotter When mutants gain new powers: news from the mutant p53 field Nat. Rev. Cancer 9 2009 701 713
3. S.M. Carr, S. Munro, L.P. Zalmas, O. Fedorov, C. Johansson, T. Krojer, C.A. Sagum, M.T. Bedford, U. Oppermann, and N.B. La Thangue Lysine methylation-dependent binding of 53BP1 to the pRb tumor suppressor Proc. Natl. Acad. Sci. USA 111 2014 11341 11346
4. D.A. Case, T.E. Cheatham 3rd, T. Darden, H. Gohlke, R. Luo, K.M. Merz Jr.; A. Onufriev, C. Simmerling, B. Wang, and R.J. Woods The Amber biomolecular simulation programs J. Comput. Chem. 26 2005 1668 1688
5. G. Charier, J. Couprie, B. Alpha-Bazin, V. Meyer, E. Quemeneur, R. Guerois, I. Callebaut, B. Gilquin, and S. Zinn-Justin The Tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding Structure 12 2004 1551 1562
6. C.F. Cheok, C.S. Verma, J. Baselga, and D.P. Lane Translating p53 into the clinic Nat. Rev. Clin. Oncol. 8 2011 25 37
7. S. Chuikov, J.K. Kurash, J.R. Wilson, B. Xiao, N. Justin, G.S. Ivanov, K. McKinney, P. Tempst, C. Prives, and S.J. Gamblin Regulation of p53 activity through lysine methylation Nature 432 2004 353 360
8. G. Cornilescu, F. Delaglio, and A. Bax Protein backbone angle restraints from searching a database for chemical shift and sequence homology J. Biomol. NMR 13 1999 289 302
9. G. Cui, M.V. Botuyan, and G. Mer Preparation of recombinant peptides with site- and degree-specific lysine (13)C-methylation Biochemistry 48 2009 3798 3800
10. G. Cui, S. Park, A.I. Badeaux, D. Kim, J. Lee, J.R. Thompson, F. Yan, S. Kaneko, Z. Yuan, and M.V. Botuyan PHF20 is an effector protein of p53 double lysine methylation that stabilizes and activates p53 Nat. Struct. Mol. Biol. 19 2012 916 924
11. C. Dai, and W. Gu p53 post-translational modification: deregulated in tumorigenesis Trends Mol. Med. 16 2010 528 536
12. C.J. DeHart, J.S. Chahal, S.J. Flint, and D.H. Perlman Extensive post-translational modification of active and inactivated forms of endogenous p53 Mol. Cell Proteomics 13 2014 1 17
13. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
14. B.M. Duggan, G.B. Legge, H.J. Dyson, and P.E. Wright SANE (Structure Assisted NOE Evaluation): an automated model-based approach for NOE assignment J. Biomol. NMR 19 2001 321 329
15. O. Fernandez-Capetillo, H.T. Chen, A. Celeste, I. Ward, P.J. Romanienko, J.C. Morales, K. Naka, Z. Xia, R.D. Camerini-Otero, and N. Motoyama DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1 Nat. Cell Biol. 4 2002 993 997
16. S. Fnu, E.A. Williamson, L.P. De Haro, M. Brenneman, J. Wray, M. Shaheen, K. Radhakrishnan, S.H. Lee, J.A. Nickoloff, and R. Hromas Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining Proc. Natl. Acad. Sci. USA 108 2011 540 545
17. A. Fradet-Turcotte, M.D. Canny, C. Escribano-Diaz, A. Orthwein, C.C. Leung, H. Huang, M.C. Landry, J. Kitevski-LeBlanc, S.M. Noordermeer, F. Sicheri, and D. Durocher 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark Nature 499 2013 50 54
18. J. Gatchalian, A. Futterer, S.B. Rothbart, Q. Tong, H. Rincon-Arano, A. Sanchez de Diego, M. Groudine, B.D. Strahl, A.C. Martinez, K.H. van Wely, and T.G. Kutateladze Dido3 PHD modulates cell differentiation and division Cell Rep. 4 2013 148 158
19. P. Güntert Automated NMR structure calculation with CYANA Methods Mol. Biol. 278 2004 353 378
20. J. Huang, and S.L. Berger The emerging field of dynamic lysine methylation of non-histone proteins Curr. Opin. Genet. Dev. 18 2008 152 158
21. J. Huang, L. Perez-Burgos, B.J. Placek, R. Sengupta, M. Richter, J.A. Dorsey, S. Kubicek, S. Opravil, T. Jenuwein, and S.L. Berger Repression of p53 activity by Smyd2-mediated methylation Nature 444 2006 629 632
22. J. Huang, R. Sengupta, A.B. Espejo, M.G. Lee, J.A. Dorsey, M. Richter, S. Opravil, R. Shiekhattar, M.T. Bedford, T. Jenuwein, and S.L. Berger p53 is regulated by the lysine demethylase LSD1 Nature 449 2007 105 108
23. J. Huang, J. Dorsey, S. Chuikov, X. Zhang, T. Jenuwein, D. Reinberg, and S.L. Berger G9a and Glp methylate lysine 373 in the tumor suppressor p53 J. Biol. Chem. 285 2010 9636 9641
24. Y. Huyen, O. Zgheib, R.A. Ditullio Jr.; V.G. Gorgoulis, P. Zacharatos, T.J. Petty, E.A. Sheston, H.S. Mellert, E.S. Stavridi, and T.D. Halazonetis Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks Nature 432 2004 406 411
25. D.K. Jha, and B.D. Strahl An RNA polymerase II-coupled function for histone H3K36 methylation in checkpoint activation and DSB repair Nat. Commun. 5 2014 3965
26. B.A. Johnson, and R.A. Blevins NMR View: a computer program for visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
27. I. Kachirskaia, X. Shi, H. Yamaguchi, K. Tanoue, H. Wen, E.W. Wang, E. Appella, and O. Gozani Role for 53BP1 Tudor domain recognition of p53 dimethylated at lysine 382 in DNA damage signaling J. Biol. Chem. 283 2008 34660 34666
28. J. Kim, J. Daniel, A. Espejo, A. Lake, M. Krishna, L. Xia, Y. Zhang, and M.T. Bedford Tudor, MBT and chromo domains gauge the degree of lysine methylation EMBO Rep. 7 2006 397 403
29. J. Lee, J.R. Thompson, M.V. Botuyan, and G. Mer Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor Nat. Struct. Mol. Biol. 15 2008 109 111
30. A.J. Levine, and M. Oren The first 30 years of p53: growing ever more complex Nat. Rev. Cancer 9 2009 749 758
31. G. Mer, A. Bochkarev, R. Gupta, E. Bochkareva, L. Frappier, C.J. Ingles, A.M. Edwards, and W.J. Chazin Structural basis for the recognition of DNA repair proteins UNG2, XPA, and RAD52 by replication factor RPA Cell 103 2000 449 456
32. S. Mujtaba, Y. He, L. Zeng, S. Yan, O. Plotnikova, Sachchidanand, R. Sanchez, N.J. Zeleznik-Le, Z. Ronai, and M.M. Zhou Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation Mol. Cell 13 2004 251 263
33. P.A. Muller, and K.H. Vousden p53 mutations in cancer Nat. Cell Biol. 15 2013 2 8
34. C.A. Musselman, R.E. Mansfield, A.L. Garske, F. Davrazou, A.H. Kwan, S.S. Oliver, H. O'Leary, J.M. Denu, J.P. Mackay, and T.G. Kutateladze Binding of the CHD4 PHD2 finger to histone H3 is modulated by covalent modifications Biochem. J. 423 2009 179 187
35. C.A. Musselman, N. Avvakumov, R. Watanabe, C.G. Abraham, M.E. Lalonde, Z. Hong, C. Allen, S. Roy, J.K. Nunez, and J. Nickoloff Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1 Nat. Struct. Mol. Biol. 19 2012 1266 1272
36. C.A. Musselman, J. Ramirez, J.K. Sims, R.E. Mansfield, S.S. Oliver, J.M. Denu, J.P. Mackay, P.A. Wade, J. Hagman, and T.G. Kutateladze Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression Proc. Natl. Acad. Sci. USA 109 2012 787 792
37. C.C. Pai, R.S. Deegan, L. Subramanian, C. Gal, S. Sarkar, E.J. Blaikley, C. Walker, L. Hulme, E. Bernhard, and S. Codlin A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice Nat. Commun. 5 2014 4091
38. S. Panier, and S.J. Boulton Double-strand break repair: 53BP1 comes into focus Nat. Rev. Mol. Cell Biol. 15 2014 7 18
39. I. Rappold, K. Iwabuchi, T. Date, and J. Chen Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways J. Cell Biol. 153 2001 613 620
40. S. Roy, C.A. Musselman, I. Kachirskaia, R. Hayashi, K.C. Glass, J.C. Nix, O. Gozani, E. Appella, and T.G. Kutateladze Structural insight into p53 recognition by the 53BP1 tandem Tudor domain J. Mol. Biol. 398 2010 489 496
41. X. Shi, I. Kachirskaia, H. Yamaguchi, L.E. West, H. Wen, E.W. Wang, S. Dutta, E. Appella, and O. Gozani Modulation of p53 function by SET8-mediated methylation at lysine 382 Mol. Cell 27 2007 636 646
42. B.D. Strahl, and C.D. Allis The language of covalent histone modifications Nature 403 2000 41 45
43. J. Tang, N.W. Cho, G. Cui, E.M. Manion, N.M. Shanbhag, M.V. Botuyan, G. Mer, and R.A. Greenberg Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination Nat. Struct. Mol. Biol. 20 2013 317 325
44. V. Tsui, and D.A. Case Theory and applications of the generalized Born solvation model in macromolecular simulations Biopolymers 56 2000 275 291
45. K.H. Vousden, and D.P. Lane p53 in health and disease Nat. Rev. Mol. Cell Biol. 8 2007 275 283
46. I. Ward, J.E. Kim, K. Minn, C.C. Chini, G. Mer, and J. Chen The tandem BRCT domain of 53BP1 is not required for its repair function J. Biol. Chem. 281 2006 38472 38477
47. L.E. West, S. Roy, K. Lachmi-Weiner, R. Hayashi, X. Shi, E. Appella, T.G. Kutateladze, and O. Gozani The MBT repeats of L3MBTL1 link SET8-mediated p53 methylation at lysine 382 to target gene repression J. Biol. Chem. 285 2010 37725 37732
48. D.S. Wishart, and B.D. Sykes The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data J. Biomol. NMR 4 1994 171 180
49. O. Zgheib, K. Pataky, J. Brugger, and T.D. Halazonetis An oligomerized 53BP1 tudor domain suffices for recognition of DNA double-strand breaks Mol. Cell Biol. 29 2009 1050 1058
50. X. Zhang, H. Wen, and X. Shi Lysine methylation: beyond histones Acta Biochim. Biophys. Sin. (Shanghai) 44 2012 14 27
51. C. Zwahlen, P. Legault, S.J.F. Vincent, J. Greenblat, R. Konrat, and L.E. Kay Methods of measurements of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage N-peptide/box B RNA complex J. Am. Chem. Soc. 119 1997 6711 6721