An oligomerized 53BP1 tudor domain suffices for recognition of DNA double-strand breaks

Molecular and Cellular Biology

Volumn 29, Issue 4, 2009, Pages 1050-1058

  Zgheib, Omar ^a,b   Pataky, Kristopher ^c   Brugger, Juergen ^c   Halazonetis, Thanos D ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HISTONE H2AX; HYBRID PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN 53BP1; TRANSCRIPTION FACTOR GCN4; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; NUCLEAR LOCALIZATION SIGNAL; OLIGOMERIZATION; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; UBIQUITINATION;

AMINO ACID SEQUENCE; CELL COMPARTMENTATION; CELL LINE, TUMOR; CELL NUCLEUS; CONSERVED SEQUENCE; DNA BREAKS, DOUBLE-STRANDED; GREEN FLUORESCENT PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RADIATION, IONIZING; RECOMBINANT FUSION PROTEINS; REPRODUCIBILITY OF RESULTS; STRUCTURE-ACTIVITY RELATIONSHIP;

SACCHAROMYCETALES; SCHIZOSACCHAROMYCETACEAE; VERTEBRATA;

EID: 59449094470     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01011-08     Document Type: Article

References (46)

1. Adams, M. M., and P. B. Carpenter. 2006. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div. 1:19.
2. Adams, M. M., B. Wang, Z. Xia, J. C. Morales, X. Lu, L. A. Donehower, D. A. Bochar, S. J. Elledge, and P. B. Carpenter. 2005. 53BP1 oligomerization is independent of its methylation by PRMT1. Cell Cycle 4:1854-1861.
3. Alpha-Bazin, B., A. Lorphelin, N. Nozerand, G. Charier, C. Marchetti, F. Berenguer, J. Couprie, B. Gilquin, S. Zinn-Justin, and E. Quemeneur. 2005. Boundaries and physical characterization of a new domain shared between mammalian 53BP1 and yeast Rad9 checkpoint proteins. Protein Sci. 14: 1827-1839.
4. Anderson, L., C. Henderson, and Y. Adachi. 2001. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol. Cell. Biol. 21:1719-1729.
5. Bekker-Jensen, S., C. Lukas, F. Melander, J. Bartek, and J. Lukas. 2005. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170:201-211.
6. Botuyan, M. V., J. Lee, I. M. Ward, J. E. Kim, J. R. Thompson, J. Chen, and G. Mer. 2006. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127:1361-1373.
7. Charier, G., J. Couprie, B. Alpha-Bazin, V. Meyer, E. Quemeneur, R. Guerois, I. Callebaut, B. Gilquin, and S. Zinn-Justin. 2004. The Tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding. Structure 12:1551-1562.
8. Costes, S. V., A. Ponomarev, J. L. Chen, D. Nguyen, F. A. Cucinotta, and M. H. Barcellos-Hoff. 2007. Image-based modeling reveals dynamic redistribution of DNA damage into nuclear sub-domains. PLoS Comput. Biol. 3:e155.
9. Du, L. L., B. A. Moser, and P. Russell. 2004. Homo-oligomerization is the essential function of the tandem BRCT domains in the checkpoint protein Crb2. J. Biol. Chem. 279:38409-38414.
10. Du, L. L., T. M. Nakamura, and P. Russell. 2006. Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20:1583-1596.
11. Falck, J., J. Coates, and S. P. Jackson. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605-611.
12. Fernandez-Capetillo, O., H. T. Chen, A. Celeste, I. Ward, P. J. Romanienko, J. C. Morales, K Naka, Z. Xia, R. D. Camerini-Otero, N. Motoyama, P. B. Carpenter, W. M. Bonner, J. Chen, and A. Nussenzweig. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993-997.
13. Grenon, M., T. Costelloe, S. Jimeno, A. O'Shaughnessy, J. Fitzgerald, O. Zgheib, L. Degerth, and N. F. Lowndes. 2007. Docking onto chromatin via the Saccharomyces cerevisiae Rad9 Tudor domain. Yeast 24:105-119.
14. Hammet, A., C. Magill, J. Heierhorst, and S. P. Jackson. 2007. Rad9 BRCT domain interaction with phosphorylated H2AX regulates the G1 checkpoint in budding yeast. EMBO Rep. 8:851-857.
15. Harbury, P. B., T. Zhang, P. S. Kim, and T. Alber. 1993. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262:1401-1407.
16. Harrison, J. C., and J. E. Haber. 2006. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40:209-235.
17. Huen, M. S., R. Grant, I. Manke, K Minn, X. Yu, M. B. Yaffe, and J. Chen. 2007. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131:901-914.
18. Huyen, Y., 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. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406-411.
19. Iwabuchi, K., B. P. Basu, B. Kysela, T. Kurihara, M. Shibata, D. Guan, Y. Cao, T. Hamada, K. Imamura, P. A. Jeggo, T. Date, and A. J. Doherty. 2003. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J. Biol. Chem. 278:36487-36495.
20. Jullien, D., P. Vagnarelli, W. C. Earnshaw, and Y. Adachi. 2002. Kinetochore localisation of the DNA damage response component 53BP1 during mitosis. J. Cell Sci. 115:71-79.
21. Kim, H., J. Chen, and X. Yu. 2007. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316:1202-1205.
22. Kolas, N. K., J. R. Chapman, S. Nakada, J. Ylanko, R. Chahwan, F. D. Sweeney, S. Panier, M. Mendez, J. Wildenhain, T. M. Thomson, L. Pelletier, S. P. Jackson, and D. Durocher. 2007. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318:1637-1640.
23. Lancelot, N., G. Charier, J. Couprie, I. Duband-Goulet, B. Alpha-Bazin, E. Quemeneur, E. Ma, M. C. Marsolier-Kergoat, V. Ropars, J. B. Charbonnier, S. Miron, C. T. Craescu, I. Callebaut, B. Gilquin, and S. Zinn-Justin. 2007. The checkpoint Saccharomyces cerevisiae Rad9 protein contains a tandem tudor domain that recognizes DNA. Nucleic Acids Res. 35:5898-5912.
24. Mailand, N., S. Bekker-Jensen, H. Faustrup, F. Melander, J. Bartek, C. Lukas, and J. Lukas. 2007. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131:887-900.
25. Mochan, T. A., M. Venere, R. A. DiTullio, Jr., and T. D. Halazonetis. 2004. 53BP1, an activator of ATM in response to DNA damage. DNA Repair 3:945-952.
26. Nakamura, T. M., L. L. Du, C. Redon, and P. Russell. 2004. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol. Cell. Biol. 24:6215-6230.
27. O'Shea, E. K., J. D. Klemm, P. S. Kim, and T. Alber. 1991. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254:539-544.
28. Pataky, K., G. Villanueva, A. Liani, O. Zgheib, N. Jenkins, D. J. Halazonetis, T. D. Halazonetis, and J. Brugger. Microcollimator for micron-wide stripe irradiation of cells using 20-30 keV X-rays. Radiat. Res., in press.
29. Pryde, F., S. Khalili, K. Robertson, J. Selfridge, A. M. Ritchie, D. W. Melton, D. Jullien, and Y. Adachi. 2005. 53BP1 exchanges slowly at the sites of DNA damage and appears to require RNA for its association with chromatin. J. Cell Sci. 118:2043-2055.
30. Rappold, I., K. Iwabuchi, T. Date, and J. Chen. 2001. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153:613-620.
31. Sanders, S. L., M. Portoso, J. Mata, J. Bahler, R. C. Allshire, and T. Kouzarides. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-614.
32. Schotta, G., R. Sengupta, S. Kubicek, S. Malin, M. Kauer, E. Callen, A. Celeste, M. Pagani, S. Opravil, I. A. De La Rosa-Velazquez, A. Espejo, M. T. Bedford, A. Nussenzweig, M. Busslinger, and T. Jenuwein. 2008. A chroma-tin-wide transition to H4K20 monomethylation impairs genome integrityand programmed DNA rearrangements in the mouse. Genes Dev. 22:2048-2061.
33. Schultz, L. B., N. H. Chehab, A. Malikzay, and T. D. Halazonetis. 2000. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151:1381-1390.
34. Sobhian, B., G. Shao, D. R. Lilli, A. C. Culhane, L. A. Moreau, B. Xia, D. M. Livingston, and R. A. Greenberg. 2007. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316:1198-1202.
35. Soulier, J., and N. F. Lowndes. 1999. The BRCT domain of the S. cerevisiae checkpoint protein Rad9 mediates a Rad9-Rad9 interaction after DNA damage. Curr. Biol. 9:551-554.
36. Stucki, M., J. A. Clapperton, D. Mohammad, M. B. Yaffe, S. J. Smerdon, and S. P. Jackson. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213-1226.
37. Swanson, K. A., R. S. Kang, S. D. Stamenova, L. Hicke, and I. Radhakrishnan. 2003. Solution structure of Vps27 UIM-ubiquitin complex important for endosomal sorting and receptor downregulation. EMBO J. 22:4597-4606.
38. Toh, G. W., A. M. O'Shaughnessy, S. Jimeno, I. M. Dobbie, M. Grenon, S. Maffini, A. O'Rorke, and N. F. Lowndes. 2006. Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Repair 5:693-703.
39. Wang, B., S. Matsuoka, B. A. Ballif, D. Zhang, A. Smogorzewska, S. P. Gygi, and S. J. Elledge. 2007. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316:1194-1198.
40. Ward, I. M., K. Minn, K. G. Jorda, and J. Chen. 2003. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278:19579-19582.
41. Ward, I., J. E. Kim, K. Minn, C. C. Chini, G. Mer, and J. Chen. 2006. The tandem BRCT domain of 53BP1 is not required for its repair function. J. Biol. Chem. 281:38472-38477.
42. Waterman, M. J., J. L. Waterman, and T. D. Halazonetis. 1996. An engineered four-stranded coiled coil substitutes for the tetramerization domain of wild-type p53 and alleviates transdominant inhibition by tumor-derived p53 mutants. Cancer Res. 56:158-163.
43. 1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25:8430-8443.
44. Xia, Z., J. C. Morales, W. G. Dunphy, and P. B. Carpenter. 2001. Negative cell cycle regulation and DNA damage-inducible phosphorylation of the BRCT protein 53BP1. J. Biol. Chem. 276:2708-2718.
45. Yan, J., Y. S. Kim, X. P. Yang, L. P. Li, G. Liao, F. Xia, and A. M. Jetten. 2007. The ubiquitin-interacting motif containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. Cancer Res. 67:6647-6656.
46. Yang, H., J. J. Pesavento, T. W. Starnes, D. E. Cryderman, L. L. Wallrath, N. L. Kelleher, and C. A. Mizzen. 2008. Preferential dimethylation of histone H4 lysine 20 by Suv4-20. J. Biol. Chem. 283:12085-12092.