53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions

Cell

Volumn 153, Issue 6, 2013, Pages 1266-1280

  Callen, Elsa ^a   Di Virgilio, Michela ^b   Kruhlak, Michael J ^a   Nieto Soler, Maria ^c   Wong, Nancy ^a   Chen, Hua Tang ^a   Faryabi, Robert B ^a   Polato, Federica ^a   Santos, Margarida ^a   Starnes, Linda M ^d   Wesemann, Duane R ^e   Lee, Ji Eun ^f   Tubbs, Anthony ^g   Sleckman, Barry P ^g   Daniel, Jeremy A ^d   Ge, Kai ^f   Alt, Frederick W ^e   Fernandez Capetillo, Oscar ^c   Nussenzweig, Michel C ^b   Nussenzweig, André ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

^d University of Copenhagen   (Denmark)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CAMPTOTHECIN; CISPLATIN; DNA DAMAGE RESPONSE PROTEIN; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; MUTANT PROTEIN; PHOSPHOPROTEIN; PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ALLELE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL SURVIVAL; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CHROMOSOME DAMAGE; CONTROLLED STUDY; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; GENOMIC INSTABILITY; HISTONE MODIFICATION; HOMOLOGOUS RECOMBINATION; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PHOSPHORYLATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN INTERACTION; TRANSCRIPTION INITIATION; WILD TYPE;

EID: 84878893538     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.05.023     Document Type: Article

References (53)

1. J.H. Barlow, R.B. Faryabi, E. Callén, N. Wong, A. Malhowski, H.T. Chen, G. Gutierrez-Cruz, H.W. Sun, P. McKinnon, and G. Wright Identification of early replicating fragile sites that contribute to genome instability Cell 152 2013 620 632
2. A. Bhattacharyya, U.S. Ear, B.H. Koller, R.R. Weichselbaum, and D.K. Bishop The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin J. Biol. Chem. 275 2000 23899 23903
3. C. Boboila, M. Jankovic, C.T. Yan, J.H. Wang, D.R. Wesemann, T. Zhang, A. Fazeli, L. Feldman, A. Nussenzweig, M. Nussenzweig, and F.W. Alt Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70 Proc. Natl. Acad. Sci. USA 107 2010 3034 3039
4. A. Bothmer, D.F. Robbiani, N. Feldhahn, A. Gazumyan, A. Nussenzweig, and M.C. Nussenzweig 53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination J. Exp. Med. 207 2010 855 865
5. A. Bothmer, D.F. Robbiani, M. Di Virgilio, S.F. Bunting, I.A. Klein, N. Feldhahn, J. Barlow, H.T. Chen, D. Bosque, and E. Callen Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1 Mol. Cell 42 2011 319 329
6. P. Bouwman, A. Aly, J.M. Escandell, M. Pieterse, J. Bartkova, H. van der Gulden, S. Hiddingh, M. Thanasoula, A. Kulkarni, and Q. Yang 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers Nat. Struct. Mol. Biol. 17 2010 688 695
7. C. Bowman-Colin, B. Xia, S. Bunting, C. Klijn, R. Drost, P. Bouwman, L. Fineman, X. Chen, A.C. Culhane, and H. Cai Palb2 synergizes with Trp53 to suppress mammary tumor formation in a model of inherited breast cancer Proc. Natl. Acad. Sci. USA 2013 10.1073/pnas.1305362110 Published online May 8, 2013
8. H.E. Bryant, N. Schultz, H.D. Thomas, K.M. Parker, D. Flower, E. Lopez, S. Kyle, M. Meuth, N.J. Curtin, and T. Helleday Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase Nature 434 2005 913 917
9. S.F. Bunting, E. Callén, N. Wong, H.T. Chen, F. Polato, A. Gunn, A. Bothmer, N. Feldhahn, O. Fernandez-Capetillo, and L. Cao 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks Cell 141 2010 243 254
10. S.F. Bunting, E. Callén, M.L. Kozak, J.M. Kim, N. Wong, A.J. López-Contreras, T. Ludwig, R. Baer, R.B. Faryabi, and A. Malhowski BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair Mol. Cell 46 2012 125 135
11. S.B. Buonomo, Y. Wu, D. Ferguson, and T. de Lange Mammalian Rif1 contributes to replication stress survival and homology-directed repair J. Cell Biol. 187 2009 385 398
12. E. Callén, M. Jankovic, S. Difilippantonio, J.A. Daniel, H.T. Chen, A. Celeste, M. Pellegrini, K. McBride, D. Wangsa, and A.L. Bredemeyer ATM prevents the persistence and propagation of chromosome breaks in lymphocytes Cell 130 2007 63 75
13. E. Callén, M.C. Nussenzweig, and A. Nussenzweig Breaking down cell cycle checkpoints and DNA repair during antigen receptor gene assembly Oncogene 26 2007 7759 7764
14. E. Callen, R.B. Faryabi, M. Luckey, B. Hao, J.A. Daniel, W. Yang, H.W. Sun, G. Dressler, W. Peng, and H. Chi The DNA damage- and transcription- associated protein paxip1 controls thymocyte development and emigration Immunity 37 2012 971 985
15. L. Cao, X. Xu, S.F. Bunting, J. Liu, R.H. Wang, L.L. Cao, J.J. Wu, T.N. Peng, J. Chen, and A. Nussenzweig A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency Mol. Cell 35 2009 534 541
16. A. Celeste, O. Fernandez-Capetillo, M.J. Kruhlak, D.R. Pilch, D.W. Staudt, A. Lee, R.F. Bonner, W.M. Bonner, and A. Nussenzweig Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks Nat. Cell Biol. 5 2003 675 679
17. G.B. Celli, E.L. Denchi, and T. de Lange Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination Nat. Cell Biol. 8 2006 885 890
18. J.R. Chapman, P. Barral, J.B. Vannier, V. Borel, M. Steger, A. Tomas-Loba, A.A. Sartori, I.R. Adams, F.D. Batista, and S.J. Boulton RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection Mol. Cell 49 2013 858 871
19. Y.W. Cho, T. Hong, S. Hong, H. Guo, H. Yu, D. Kim, T. Guszczynski, G.R. Dressler, T.D. Copeland, M. Kalkum, and K. Ge PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex J. Biol. Chem. 282 2007 20395 20406
20. Y.W. Cho, S. Hong, Q. Jin, L. Wang, J.E. Lee, O. Gavrilova, and K. Ge Histone methylation regulator PTIP is required for PPARgamma and C/EBPalpha expression and adipogenesis Cell Metab. 10 2009 27 39
21. J.A. Daniel, M.A. Santos, Z. Wang, C. Zang, K.R. Schwab, M. Jankovic, D. Filsuf, H.T. Chen, A. Gazumyan, and A. Yamane PTIP promotes chromatin changes critical for immunoglobulin class switch recombination Science 329 2010 917 923
22. M. Di Virgilio, E. Callen, A. Yamane, W. Zhang, M. Jankovic, A.D. Gitlin, N. Feldhahn, W. Resch, T.Y. Oliveira, and B.T. Chait Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching Science 339 2013 711 715
23. S. Difilippantonio, E. Gapud, N. Wong, C.Y. Huang, G. Mahowald, H.T. Chen, M.J. Kruhlak, E. Callen, F. Livak, and M.C. Nussenzweig 53BP1 facilitates long-range DNA end-joining during V(D)J recombination Nature 456 2008 529 533
24. N. Dimitrova, Y.C. Chen, D.L. Spector, and T. de Lange 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility Nature 456 2008 524 528
25. C. Escribano-Díaz, A. Orthwein, A. Fradet-Turcotte, M. Xing, J.T. Young, J. Tkáč, M.A. Cook, A.P. Rosebrock, M. Munro, and M.D. Canny A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice Mol. Cell 49 2013 872 883
26. H. Farmer, N. McCabe, C.J. Lord, A.N. Tutt, D.A. Johnson, T.B. Richardson, M. Santarosa, K.J. Dillon, I. Hickson, and C. Knights Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy Nature 434 2005 917 921
27. L. Feng, K.W. Fong, J. Wang, W. Wang, and J. Chen RIF1 counteracts BRCA1-mediated end resection during DNA repair J. Biol. Chem. 288 2013 11135 11143
28. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, and J. Gentry Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
29. Z. Gong, Y.W. Cho, J.E. Kim, K. Ge, and J. Chen Accumulation of Pax2 transactivation domain interaction protein (PTIP) at sites of DNA breaks via RNF8-dependent pathway is required for cell survival after DNA damage J. Biol. Chem. 284 2009 7284 7293
30. J.E. Jaspers, A. Kersbergen, U. Boon, W. Sol, L. van Deemter, S.A. Zander, R. Drost, E. Wientjens, J. Ji, and A. Aly Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors Cancer Discov 3 2013 68 81
31. P.A. Jowsey, A.J. Doherty, and J. Rouse Human PTIP facilitates ATM-mediated activation of p53 and promotes cellular resistance to ionizing radiation J. Biol. Chem. 279 2004 55562 55569
32. A.J. López-Contreras, P. Gutierrez-Martinez, J. Specks, S. Rodrigo-Perez, and O. Fernandez-Capetillo An extra allele of Chk1 limits oncogene-induced replicative stress and promotes transformation J. Exp. Med. 209 2012 455 461
33. Lottersberger, F., Bothmer, A., Robbiani, D.F., Nussenzweig, M.C., and de Lange, T. (2013). Role of 53BP1 oligomerization in regulating double-strand break repair. Proceedings of the National Academy of Sciences of the United States of America.
34. I.A. Manke, D.M. Lowery, A. Nguyen, and M.B. Yaffe BRCT repeats as phosphopeptide-binding modules involved in protein targeting Science 302 2003 636 639
35. M.E. Moynahan, J.W. Chiu, B.H. Koller, and M. Jasin Brca1 controls homology-directed DNA repair Mol. Cell 4 1999 511 518
36. I.M. Munoz, P.A. Jowsey, R. Toth, and J. Rouse Phospho-epitope binding by the BRCT domains of hPTIP controls multiple aspects of the cellular response to DNA damage Nucleic Acids Res. 35 2007 5312 5322
37. S.R. Patel, D. Kim, I. Levitan, and G.R. Dressler The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex Dev. Cell 13 2007 580 592
38. R. Rai, H. Zheng, H. He, Y. Luo, A. Multani, P.B. Carpenter, and S. Chang The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres EMBO J. 29 2010 2598 2610
39. B. Reina-San-Martin, J. Chen, A. Nussenzweig, and M.C. Nussenzweig Enhanced intra-switch region recombination during immunoglobulin class switch recombination in 53BP1-/- B cells Eur. J. Immunol. 37 2007 235 239
40. K.R. Schwab, S.R. Patel, and G.R. Dressler Role of PTIP in class switch recombination and long-range chromatin interactions at the immunoglobulin heavy chain locus Mol. Cell. Biol. 31 2011 1503 1511
41. R. Scully, J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, T. Ashley, and D.M. Livingston Association of BRCA1 with Rad51 in mitotic and meiotic cells Cell 88 1997 265 275
42. A. Sfeir, and T. de Lange Removal of shelterin reveals the telomere end-protection problem Science 336 2012 593 597
43. J. Silverman, H. Takai, S.B. Buonomo, F. Eisenhaber, and T. de Lange Human Rif1, ortholog of a yeast telomeric protein, is regulated by ATM and 53BP1 and functions in the S-phase checkpoint Genes Dev. 18 2004 2108 2119
44. E. Sonoda, H. Hochegger, A. Saberi, Y. Taniguchi, and S. Takeda Differential usage of non-homologous end-joining and homologous recombination in double strand break repair DNA Repair (Amst.) 5 2006 1021 1029
45. L.S. Symington, and J. Gautier Double-strand break end resection and repair pathway choice Annu. Rev. Genet. 45 2011 247 271
46. L.I. Toledo, M. Murga, R. Zur, R. Soria, A. Rodriguez, S. Martinez, J. Oyarzabal, J. Pastor, J.R. Bischoff, and O. Fernandez-Capetillo A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations Nat. Struct. Mol. Biol. 18 2011 721 727
47. X. Wang, K. Takenaka, and S. Takeda PTIP promotes DNA double-strand break repair through homologous recombination Genes Cells. 2010 10.1111/j.1365-2443. 2009.01379.x Published online January 19, 2013
48. I.M. Ward, B. Reina-San-Martin, A. Olaru, K. Minn, K. Tamada, J.S. Lau, M. Cascalho, L. Chen, A. Nussenzweig, and F. Livak 53BP1 is required for class switch recombination J. Cell Biol. 165 2004 459 464
49. 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
50. D.R. Wesemann, J.M. Magee, C. Boboila, D.P. Calado, M.P. Gallagher, A.J. Portuguese, J.P. Manis, X. Zhou, M. Recher, and K. Rajewsky Immature B cells preferentially switch to IgE with increased direct Sμ to Sε recombination J. Exp. Med. 208 2011 2733 2746
51. A. Yamane, D.F. Robbiani, W. Resch, A. Bothmer, H. Nakahashi, T. Oliveira, P.C. Rommel, E.J. Brown, A. Nussenzweig, M.C. Nussenzweig, and R. Casellas RPA accumulation during class switch recombination represents 5′-3′ DNA-end resection during the S-G2/M phase of the cell cycle Cell Rep 3 2013 138 147
52. X. Yu, C.C. Chini, M. He, G. Mer, and J. Chen The BRCT domain is a phospho-protein binding domain Science 302 2003 639 642
53. M. Zimmermann, F. Lottersberger, S.B. Buonomo, A. Sfeir, and T. de Lange 53BP1 regulates DSB repair using Rif1 to control 5′ end resection Science 339 2013 700 704