Double-strand break repair: 53BP1 comes into focus

Nature Reviews Molecular Cell Biology

Volumn 15, Issue 1, 2014, Pages 7-18

  Panier, Stephanie ^a   Boulton, Simon J ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ATM PROTEIN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE H2A; HISTONE H4; P53 BINDING PROTEIN 1; PROTEIN; RNF168 PROTEIN; RNF8 PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BREAST CANCER; CHROMATIN; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FIBROBLAST; GENOMIC INSTABILITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHIZOSACCHAROMYCES POMBE; TELOMERE; UBIQUITINATION;

EID: 84891014338     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3719     Document Type: Review

References (121)

1. Bennett, C. B., Lewis, A. L., Baldwin, K. K. & Resnick, M. A. Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid. Proc. Natl Acad. Sci. USA 90, 5613-5617 (1993).
2. Sandell, L. L. & Zakian, V. A. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75, 729-739 (1993).
3. Jackson, S. P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071-1078 (2009).
4. Iwabuchi, K., Bartel, P. L., Li, B., Marraccino, R. & Fields, S. Two cellular proteins that bind to wild-type but not mutant p53. Proc. Natl Acad. Sci. USA 91, 6098-6102 (1994).
5. Adams, M. M. & Carpenter, P. B. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Division 1, 19 (2006).
6. Harrison, J. C. & Haber, J. E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40, 209-235 (2006).
7. Huen, M. S. Y. et al. Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1. Mol. Cell 37, 854-864 (2010).
8. Silverman, J., Takai, H., Buonomo, S. B. C., Eisenhaber, F. & de Lange, T. Human Rif1, ortholog of a yeast telomeric protein, is regulated by ATM and 53BP1 and functions in the S-phase checkpoint. Genes Dev. 18, 2108-2119 (2004).
9. Gong, Z., Cho, Y. W., Kim, J. E., Ge, K. & Chen, J. 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, 7284-7293 (2009).
10. Jowsey, P. A., Doherty, A. J. & Rouse, J. Human PTIP facilitates ATM-mediated activation of p53 and promotes cellular resistance to ionizing radiation. J. Biol. Chem. 279, 55562-55569 (2004).
11. Panier, S. et al. Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell 47, 383-395 (2012).
12. Munoz, I. M., Jowsey, P. A., Toth, R. & Rouse, J. Phospho-epitope binding by the BRCT domains of hPTIP controls multiple aspects of the cellular response to DNA damage. Nucleic Acids Res. 35, 5312-5322 (2007).
13. Callen, E. et al. 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell 153, 1266-1280 (2013).
14. Ditullio, R. A. et al. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nature Cell Biol. 4, 998-1002 (2002).
15. Fernandez-Capetillo, O. et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nature Cell Biol. 4, 993-997 (2002).
16. Mochan, T. A., Venere, M., DiTullio, R. A. Jr & Halazonetis, T. D. 53BP1, an activator of ATM in response to DNA damage. DNA Repair 3, 945-952 (2004).
17. Wang, B. 53BP1, a mediator of the DNA damage checkpoint. Science 298, 1435-1438 (2002).
18. Ward, I. M., Minn, K., van Deursen, J. and Chen, J. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23, 2556-2563 (2003).
19. Lee, J. -H. & Paull, T. T. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26, 7741-7748 (2007).
20. Bouwman, P. et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nature Struct. Mol. Biol. 17, 688-695 (2010).
21. Bunting, S. F. et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141, 243-254 (2010). References 20 and 21 show that 53BP1 is an inhibitor of DNA end-resection and homologous recombination.
22. Chapman, J. R., Sossick, A. J., Boulton, S. J. & Jackson, S. P. BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair. J. Cell Sci. 125, 3529-3534 (2012).
23. Lieber, M. R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181-211 (2010).
24. Heyer, W.-D., Ehmsen, K. T. & Liu, J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44, 113-139 (2010).
25. Chapman, J. R., Taylor, M. R. G. & Boulton, S. J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47, 497-510 (2012).
26. Dynan, W. S. & Yoo, S. Interaction of Ku protein and DNA-dependent protein kinase catalytic subunit with nucleic acids. Nucleic Acids Res. 26, 1551-1559 (1998).
27. Symington, L. S. & Gautier, J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271 (2011).
28. Difilippantonio, S. et al. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 456, 529-533 (2008).
29. Dimitrova, N., Chen, Y.-C. M., Spector, D. L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528 (2008).
30. Manis, J. P. et al. 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nature Immunol. 5, 481-487 (2004).
31. Reina-San-Martin, B., Chen, J., Nussenzweig, A. & Nussenzweig, M. C. Enhanced intra-switch region recombination during immunoglobulin class switch recombination in 53BP1-/- B cells. Eur. J. Immunol. 37, 235-239 (2007).
32. Ward, I. M. 53BP1 is required for class switch recombination. J. Cell Biol. 165, 459-464 (2004).
33. Anderson, L., Henderson, C. & Adachi, Y. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol. Cell. Biol. 21, 1719-1729 (2001).
34. Rappold, I., Iwabuchi, K., Date, T. & Chen, J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153, 613-620 (2001).
35. Schultz, L. B., Chehab, N. H., Malikzay, A. & Halazonetis, T. D. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151, 1381-1390 (2000).
36. 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).
37. Doil, C. et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446 (2009).
38. Huen, M. S. Y. et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901-914 (2007).
39. Kolas, N. K. et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637-1640 (2007).
40. Mailand, N. et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900 (2007).
41. Stewart, G. S. et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434 (2009). References 37 and 41 show that RNF168-mediated regulatory chromatin ubiquitylation is essential for the recruitment of 53BP1 to DSB sites.
42. Wang, B. & Elledge, S. J. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl Acad. Sci. 104, 20759-20763 (2007).
43. 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).
44. Mattiroli, F. et al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182-1195 (2012).
45. Goodarzi, A. A. & Jeggo, P. A. The repair and signaling responses to DNA double-strand breaks. Adv. Genet. 82, 1-45 (2013).
46. Chen, J., Feng, W., Jiang, J., Deng, Y. & Huen, M. S. Y. Ring finger protein RNF169 antagonises the ubiquitin-dependent signaling cascade at sites of DNA damage. J. Biol. Chem. 287, 27715-27722 (2012).
47. Huang, J. et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nature Cell Biol. 11, 592-603 (2009).
48. Poulsen, M., Lukas, C., Lukas, J., Bekker-Jensen, S. & Mailand, N. Human RNF169 is a negative regulator of the ubiquitin-dependent response to DNA double-strand breaks. J. Cell Biol. 197, 189-199 (2012).
49. Panier, S. & Durocher, D. Push back to respond better: regulatory inhibition of the DNA double-strand break response. Nature Rev. Mol. Cell Biol. 14, 661-672 (2013).
50. Bekker-Jensen, S. et al. HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nature Cell Biol. 12, 80-86 (2009).
51. Butler, L. R. et al. The proteasomal de-ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J. 31, 3918-3934 (2012).
52. Gudjonsson, T. et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150, 697-709 (2012).
53. Mosbech, A., Lukas, C., Bekker-Jensen, S. & Mailand, N. The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J. Biol. Chem. 7, 16579-16587 (2013).
54. Nakada, S. et al. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466, 941-946 (2010).
55. Shao, G. et al. The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8- Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc. Natl Acad. Sci. 106, 3166-3171 (2009).
56. Danielsen, J. R. et al. DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding zinc finger. J. Cell Biol. 197, 179-187 (2012).
57. Galanty, Y., Belotserkovskaya, R., Coates, J. & Jackson, S. P. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195 (2012).
58. Galanty, Y. et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939 (2009).
59. Luo, K., Zhang, H., Wang, L., Yuan, J. & Lou, Z. Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 31, 3008-3019 (2012).
60. Morris, J. R. et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890 (2009).
61. Yin, Y. et al. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196-1208 (2012).
62. Vyas, R. et al. RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ. 20, 490-502 (2013).
63. Celeste, A. et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nature Cell Biol. 5, 675-679 (2003).
64. Bekker-Jensen, S., Lukas, C., Melander, F., Bartek, J. & Lukas, J. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170, 201-211 (2005).
65. Lou, Z., Minter-Dykhouse, K., Wu, X. & Chen, J. MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421, 957-961 (2003).
66. Stewart, G. S., Wang, B., Bignell, C. R., Taylor, A. M. R. & Elledge, S. J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961-966 (2003).
67. Joo, H. -Y. et al. Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449, 1068-1072 (2007).
68. Morales, J. C. et al. Role for the BRCA1 C-terminal repeats (BRCT) protein 53BP1 in maintaining genomic stability. J. Biol. Chem. 278, 14971-14977 (2003).
69. Fradet-Turcotte, A. et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499, 50-54 (2013). Discovers that 53BP1 binds directly to RNF168-ubiquitylated H2A and that this binding is required for 53BP1 accumulation at damaged chromatin.
70. 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). Reveals the molecular mechanism through which the 53BP1 Tudor domain binds to dimethylated H4K20.
71. Zgheib, O., Pataky, K., Brugger, J. & Halazonetis, T. D. An oligomerized 53BP1 tudor domain suffices for recognition of DNA double-strand breaks. Mol. Cell. Biol. 29, 1050-1058 (2009).
72. Huyen, Y. et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406-411 (2004).
73. Pesavento, J. J., Yang, H., Kelleher, N. L. & Mizzen, C. A. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol. Cell. Biol. 28, 468-486 (2008).
74. Oda, H. et al. Regulation of the histone H4 monomethylase PR-Set7 by CRL4Cdt2-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 40, 364-376 (2010).
75. Pei, H. et al. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470, 124-128 (2011).
76. Hajdu, I., Ciccia, A., Lewis, S. M. & Elledge, S. J. Wolf-Hirschhorn syndrome candidate 1 is involved in the cellular response to DNA damage. Proc. Natl Acad. Sci. USA 108, 13130-13134 (2011).
77. Karachentsev, D., Sarma, K., Reinberg, D. & Steward, R. PR-Set7-dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. Genes Dev. 19, 431-435 (2005).
78. Schotta, G. et al. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22, 2048-2061 (2008).
79. Marango, J. et al. The MMSET protein is a histone methyltransferase with characteristics of a transcriptional corepressor. Blood 111, 3145-3154 (2008).
80. Nimura, K. et al. A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome. Nature 460, 287-291 (2009).
81. Hartlerode, A. J. et al. Impact of histone H4 lysine 20 methylation on 53BP1 responses to chromosomal double strand breaks. PLoS ONE 7, e49211 (2012).
82. Acs, K. et al. The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nature Struct. Mol. Biol. 18, 1345-1350 (2011).
83. Mallette, F. A. et al. RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J. 31, 1865-1878 (2012).
84. Lee, J., Thompson, J. R., Botuyan, M. V. & Mer, G. Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A- tudor. Nature Struct. Mol. Biol. 15, 109-111 (2008).
85. Min, J. et al. L3MBTL1 recognition of mono- and dimethylated histones. Nature Struct. Mol. Biol. 14, 1229-1230 (2007).
86. Meerang, M. et al. The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nature Cell Biol. 13, 1376-1382 (2011).
87. Smeenk, G. & van Attikum, H. The chromatin response to DNA breaks: leaving a mark on genome integrity. Annu. Rev. Biochem. 82, 55-80 (2013).
88. Hsiao, K. Y. & Mizzen, C. A. Histone H4 deacetylation facilitates 53BP1 DNA damage signaling and double-strand break repair. J. Mol. Cell Biol. 5, 157-165 (2013).
89. Tang, J. et al. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nature Struct. Mol. Biol. 20, 317-325 (2013). References 88 and 89 showed that the acetylation status of H4K16 regulates the association of 53BP1 with dimethylated H4K20 during DSB repair.
90. Miller, K. M. et al. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nature Struct. Mol. Biol. 17, 1144-1151 (2010).
91. Lee, M. J., Lee, B. -H., Hanna, J., King, R. W. & Finley, D. Trimming of ubiquitin chains by proteasome-associated deubiquitinating enzymes. Mol. Cell Proteomics 10, R110.003871- R110.003875 (2011).
92. Sanders, S. L. et al. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603-614 (2004).
93. Santos, M. A. et al. Class switching and meiotic defects in mice lacking the E3 ubiquitin ligase RNF8. J. Exp. Med. 207, 973-981 (2010).
94. Stucki, M. et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226 (2005).
95. Kilkenny, M. L. et al. Structural and functional analysis of the Crb2-BRCT2 domain reveals distinct roles in checkpoint signaling and DNA damage repair. Genes Dev. 22, 2034-2047 (2008).
96. Sanders, S. L., Arida, A. R. & Phan, F. P. Requirement for the phospho-H2AX binding module of Crb2 in double-strand break targeting and checkpoint activation. Mol. Cell. Biol. 30, 4722-4731 (2010).
97. Sofueva, S., Du, L.-L., Limbo, O., Williams, J. S. & Russell, P. BRCT domain interactions with phospho-histone H2A target Crb2 to chromatin at double-strand breaks and maintain the DNA damage checkpoint. Mol. Cell. Biol. 30, 4732-4743 (2010).
98. Du, L. L., Nakamura, T. M. & Russell, P. Histone modification- dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20, 1583-1596 (2006).
99. Iwabuchi, K. et al. 53BP1 contributes to survival of cells irradiated with X-ray during G1 without Ku70 or Artemis. Genes Cells11, 935-948 (2006).
100. Nakamura, K. et al. Genetic dissection of vertebrate 53BP1: a major role in non-homologous end joining of DNA double strand breaks. DNA Repair 5, 741-749 (2006).
101. Bothmer, A. et al. Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol. Cell 42, 319-329 (2011).
102. Rai, R. et al. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J. 29, 2598-2610 (2010).
103. Chapman, J. R. et al. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell 49, 858-871 (2013).
104. Escribano-Diaz, C. et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell 49, 872-883 (2013).
105. Zimmermann, M., Lottersberger, F., Buonomo, S. B., Sfeir, A. & de Lange, T. 53BP1 regulates repair using rif1 to control 5' end resection. Science 399, 700-704 (2013).
106. Di Virgilio, M. et al. rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science 399, 711-715 (2013).
107. Feng, L., Fong, K.-W., Wang, J., Wang, W. & Chen, J. RIF1 counteracts BRCA1-mediated end resection during DNA repair. J. Biol. Chem. 288, 11135-11143 (2013). References 103-107 identify RIF1 as a 53BP1 effector protein during DSB repair pathway choice.
108. Marcand, S., Wotton, D., Gilson, E. & Shore, D. Rap1p and telomere length regulation in yeast. Ciba Found. Symp. 211, 76-93; discussion 93-103 (1997).
109. Wotton, D. & Shore, D. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 11, 748-760 (1997).
110. Buonomo, S. B., Wu, Y., Ferguson, D. & de Lange, T. Mammalian Rif1 contributes to replication stress survival and homology-directed repair. J. Cell Biol. 187, 385-398 (2009).
111. Cornacchia, D. et al. Mouse Rif1 is a key regulator of the replication-timing programme in mammalian cells. EMBO J. 31, 3678-3690 (2012).
112. Yamazaki, S. et al. Rif1 regulates the replication timing domains on the human genome. EMBO J. 31, 3667-3677 (2012).
113. Xu, D. et al. Rif1 provides a new DNA-binding interface for the Bloom syndrome complex to maintain normal replication. EMBO J. 29, 3140-3155 (2010).
114. Rai, R. et al. The E3 ubiquitin ligase Rnf8 stabilizes Tpp1 to promote telomere end protection. Nature Struct. Mol. Biol. 18, 1400-1407 (2011).
115. Wang, X., Takenaka, K. & Takeda, S. PTIP promotes DNA double-strand break repair through homologous recombination. Genes Cells 15, 243-254 (2010).
116. Shi, T. et al. Rif1 and Rif2 shape telomere function and architecture through multivalent Rap1 interactions. Cell 153, 1340-1353 (2013).
117. Xie, A. et al. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell 28, 1045-1057 (2007).
118. Brzovic, P. S. et al. Binding and recognition in the assembly of an active BRCA1/BARD1 ubiquitin-ligase complex. Proc. Natl Acad. Sci. USA 100, 5646-5651 (2003).
119. Sartori, A. A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
120. Reczek, C. R., Szabolcs, M., Stark, J. M., Ludwig, T. & Baer, R. The interaction between CtIP and BRCA1 is not essential for resection-mediated DNA repair or tumor suppression. J. Cell Biol. 201, 693-707 (2013).
121. Boboila, C., Alt, F. W. & Schwer, B. Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA double-strand breaks. Adv. Immunol. 116, 1-49 (2012).