Polo-like kinase 3 regulates CtIP during DNA double-strand break repair in G1

Journal of Cell Biology

Volumn 206, Issue 7, 2014, Pages 877-894

  Barton, Olivia ^a   Naumann, Steffen C ^a   Diemer Biehs, Ronja ^a   Künzel, Julia ^a   Steinlage, Monika ^a   Conrad, Sandro ^a   Makharashvili, Nodar ^b   Wang, Jiadong ^c   Feng, Lin ^c   Lopez, Bernard S ^d   Paull, Tanya T ^b   Chen, Junjie ^c   Jeggo, Penny A ^e   Löbrich, Markus ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d Gustave Roussy Comprehensive Cancer Institute   (France)

^e UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINAL BINDING PROTEIN INTERACTING PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; DNA; NOCODAZOLE; POLO LIKE KINASE 3; UNCLASSIFIED DRUG; CARRIER PROTEIN; H2AFX PROTEIN, HUMAN; HISTONE; NUCLEAR PROTEIN; PLK3 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; RBBP8 PROTEIN, HUMAN; REPLICATION FACTOR A; RPA2 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA CONTENT; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; GENETIC TRANSFECTION; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PREMATURE CHROMOSOME CONDENSATION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; DNA END JOINING REPAIR; G1 PHASE CELL CYCLE CHECKPOINT; GENE TRANSLOCATION; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN PROCESSING;

ANIMALS; CARRIER PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; G1 PHASE CELL CYCLE CHECKPOINTS; HEK293 CELLS; HELA CELLS; HISTONES; HUMANS; MICE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A; TRANSLOCATION, GENETIC;

EID: 84907801263     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201401146     Document Type: Article

References (71)

1. Anantha, R.W., V.M. Vassin, and J.A. Borowiec. 2007. Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem. 282:35910-35923. http://dx.doi.org/10.1074/jbc .M704645200
2. Anger, M., W.A. Kues, J. Klima, M. Mielenz, M. Kubelka, J. Motlik, M. Esner, P. Dvorak, J.W. Carnwath, and H. Niemann. 2003. Cell cycle dependent expression of Plk1 in synchronized porcine fetal fibroblasts. Mol. Reprod. Dev. 65:245-253. http://dx.doi.org/10.1002/mrd.10289
3. Bahassi, M., C.W. Conn, D.L. Myer, R.F. Hennigan, C.H. McGowan, Y. Sanchez, and P.J. Stambrook. 2002. Mammalian Polo-like kinase 3 (Plk3) is a multifunctional protein involved in stress response pathways. Oncogene. 21:6633-6640. http://dx.doi.org/10.1038/sj.onc.1205850
4. Beausoleil, S.A., J. Villén, S.A. Gerber, J. Rush, and S.P. Gygi. 2006. A probability- based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24:1285-1292. http://dx.doi .org/10.1038/nbt1240
5. Beucher, A., J. Birraux, L. Tchouandong, O. Barton, A. Shibata, S. Conrad, A.A. Goodarzi, A. Krempler, P.A. Jeggo, and M. Löbrich. 2009. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J. 28:3413-3427. http://dx.doi .org/10.1038/emboj.2009.276
6. Boboila, C., 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. 2010. Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proc. Natl. Acad. Sci. USA. 107:3034-3039. http://dx.doi.org/10.1073/pnas.0915067107
7. Bunting, S.F., and A. Nussenzweig. 2013. End-joining, translocations and cancer. Nat. Rev. Cancer. 13:443-454. http://dx.doi.org/10.1038/nrc3537
8. Chapman, J.R., M.R. Taylor, and S.J. Boulton. 2012. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell. 47:497-510. http://dx.doi.org/10.1016/j.molcel.2012.07.029
9. Chapman, J.R., 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. 2013. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell. 49:858-871. http://dx.doi .org/10.1016/j.molcel.2013.01.002
10. Chen, F., A. Nastasi, Z. Shen, M. Brenneman, H. Crissman, and D.J. Chen. 1997. Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52. Mutat . Res. 384:205-211. http://dx.doi.org/10.1016/S0921-8777(97)00020-7
11. Darroudi, F., J. Fomina, M. Meijers, and A.T. Natarajan. 1998. Kinetics of the formation of chromosome aberrations in X-irradiated human lymphocytes, using PCC and FISH. Mutat. Res. 404:55-65. http://dx.doi .org/10.1016/S0027-5107(98)00095-5
12. Davis, A.J., and D.J. Chen. 2013. DNA double strand break repair via nonhomologous end-joining. Transl. Cancer Res. 2:130-143.
13. de Cárcer, G., G. Manning, and M. Malumbres. 2011. From Plk1 to Plk5: functional evolution of polo-like kinases. Cell Cycle. 10:2255-2262. http:// dx.doi.org/10.4161/cc.10.14.16494
14. Deckbar, D., T. Stiff, B. Koch, C. Reis, M. Löbrich, and P.A. Jeggo. 2010. The limitations of the G1-S checkpoint. Cancer Res. 70:4412-4421. http:// dx.doi.org/10.1158/0008-5472.CAN-09-3198
15. Di Virgilio, M., E. Callen, A. Yamane, W. Zhang, M. Jankovic, A.D. Gitlin, N. Feldhahn, W. Resch, T.Y. Oliveira, B.T. Chait, et al. 2013. Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science. 339:711-715. http://dx.doi.org/10.1126/science.1230624
16. Donnianni, R.A., M. Ferrari, F. Lazzaro, M. Clerici, B. Tamilselvan Nachimuthu, P. Plevani, M. Muzi-Falconi, and A. Pellicioli. 2010. Elevated levels of the polo kinase Cdc5 override the Mec1/ATR checkpoint in budding yeast by acting at different steps of the signaling pathway. PLoS Genet. 6:e1000763. http://dx.doi.org/10.1371/journal.pgen.1000763
17. Elia, A.E.H., P. Rellos, L.F. Haire, J.W. Chao, F.J. Ivins, K. Hoepker, D. Mohammad, L.C. Cantley, S.J. Smerdon, and M.B. Yaffe. 2003. The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain. Cell. 115:83-95. http://dx.doi .org/10.1016/S0092-8674(03)00725-6
18. Escribano-Díaz, C., A. Orthwein, A. Fradet-Turcotte, M. Xing, J.T. Young, J. Tkác, M.A. Cook, A.P. Rosebrock, M. Munro, M.D. Canny, et al. 2013. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell. 49:872- 883. http://dx.doi.org/10.1016/j.molcel.2013.01.001
19. Feng, L., K.W. Fong, J. Wang, W. Wang, and J. Chen. 2013. RIF1 counteracts BRCA1-mediated end resection during DNA repair. J. Biol. Chem. 288: 11135-11143. http://dx.doi.org/10.1074/jbc.M113.457440
20. Golsteyn, R.M., K.E. Mundt, A.M. Fry, and E.A. Nigg. 1995. Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. J. Cell Biol. 129:1617- 1628. http://dx.doi.org/10.1083/jcb.129.6.1617
21. Gotoh, E., and M. Durante. 2006. Chromosome condensation outside of mitosis: mechanisms and new tools. J. Cell. Physiol. 209:297-304. http://dx.doi .org/10.1002/jcp.20720
22. Helmink, B.A., A.T. Tubbs, Y. Dorsett, J.J. Bednarski, L.M. Walker, Z. Feng, G.G. Sharma, P.J. McKinnon, J. Zhang, C.H. Bassing, and B.P. Sleckman. 2011. H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes. Nature. 469:245-249. http://dx.doi.org/ 10.1038/nature09585
23. Huertas, P., and S.P. Jackson. 2009. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 284: 9558-9565. http://dx.doi.org/10.1074/jbc.M808906200
24. Huertas, P., F. Cortés-Ledesma, A.A. Sartori, A. Aguilera, and S.P. Jackson. 2008. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature. 455:689-692. http://dx.doi.org/10.1038/nature07215
25. Jackman, J., and P.M. O'Connor. 2001. Methods for synchronizing cells at specific stages of the cell cycle. Curr. Protoc. Cell Biol. Chapter 8:Unit 8.3.
26. Jackson, S.P., and J. Bartek. 2009. The DNA-damage response in human biology and disease. Nature. 461:1071-1078. http://dx.doi.org/10.1038/ nature08467
27. Kim, S.T., D.S. Lim, C.E. Canman, and M.B. Kastan. 1999. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274:37538-37543. http://dx.doi.org/10.1074/jbc.274.53.37538
28. Kühne, M., K. Rothkamm, and M. Löbrich. 2000. No dose-dependence of DNA double-strand break misrejoining following ?-particle irradiation. Int. J. Radiat. Biol. 76:891-900. http://dx.doi.org/10.1080/09553000050050909
29. Lansing, T.J., R.T. McConnell, D.R. Duckett, G.M. Spehar, V.B. Knick, D.F. Hassler, N. Noro, M. Furuta, K.A. Emmitte, T.M. Gilmer, et al. 2007. In vitro biological activity of a novel small-molecule inhibitor of polo-like kinase 1. Mol. Cancer Ther. 6:450-459. http://dx.doi.org/10.1158/1535- 7163.MCT-06-0543
30. Lee, K.S., J.E. Park, Y.H. Kang, T.S. Kim, and J.K. Bang. 2014. Mechanisms underlying Plk1 polo-box domain-mediated biological processes and their physiological significance. Mol. Cells. 37:286-294. http://dx.doi .org/10.14348/molcells.2014.0002
31. Lee-Theilen, M., A.J. Matthews, D. Kelly, S. Zheng, and J. Chaudhuri. 2011. CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat. Struct. Mol. Biol. 18:75-79. http://dx.doi .org/10.1038/nsmb.1942
32. Li, S., N.S. Ting, L. Zheng, P.L. Chen, Y. Ziv, Y. Shiloh, E.Y. Lee, and W.H. Lee. 2000. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature. 406:210-215. http://dx.doi .org/10.1038/35018134
33. Löbrich, M., A. Shibata, A. Beucher, A. Fisher, M. Ensminger, A.A. Goodarzi, O. Barton, and P.A. Jeggo. 2010. gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle. 9:662-669. http://dx.doi.org/10.4161/cc.9.4.10764
34. Lukas, C., V. Savic, S. Bekker-Jensen, C. Doil, B. Neumann, R.S. Pedersen, M. Grøfte, K.L. Chan, I.D. Hickson, J. Bartek, and J. Lukas. 2011a. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13:243-253. http://dx.doi.org/10.1038/ncb2201
35. Lukas, J., C. Lukas, and J. Bartek. 2011b. More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat. Cell Biol. 13:1161-1169. http://dx.doi.org/10.1038/ncb2344
36. Mansour, W.Y., S. Schumacher, R. Rosskopf, T. Rhein, F. Schmidt-Petersen, F. Gatzemeier, F. Haag, K. Borgmann, H. Willers, and J. Dahm-Daphi. 2008. Hierarchy of nonhomologous end-joining, single-strand annealing and gene conversion at site-directed DNA double-strand breaks. Nucleic Acids Res. 36:4088-4098. http://dx.doi.org/10.1093/nar/gkn347
37. Mladenov, E., B. Anachkova, and I. Tsaneva. 2006. Sub-nuclear localization of Rad51 in response to DNA damage. Genes Cells. 11:513-524. http://dx .doi.org/10.1111/j.1365-2443.2006.00958.x
38. Mosesso, P., E. Fonti, L. Bassi, C. Lorenti Garcia, and F. Palitti. 1999. The involvement of chromatin condensation in camptothecin-induced chromosome breaks in G0 human lymphocytes. Mutagenesis. 14:103-105. http://dx.doi.org/10.1093/mutage/14.1.103
39. Moynahan, M.E., and M. Jasin. 2010. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 11:196-207. http://dx.doi.org/10.1038/nrm2851
40. Naim, V., T. Wilhelm, M. Debatisse, and F. Rosselli. 2013. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat . Cell Biol. 15:1008-1015. http://dx.doi.org/10.1038/ncb2793
41. Nakamura, K., T. Kogame, H. Oshiumi, A. Shinohara, Y. Sumitomo, K. Agama, Y. Pommier, K.M. Tsutsui, K. Tsutsui, E. Hartsuiker, et al. 2010. Collaborative action of Brca1 and CtIP in elimination of covalent modifications from double-strand breaks to facilitate subsequent break repair. PLoS Genet. 6:e1000828. http://dx.doi.org/10.1371/journal.pgen.1000828
42. Nussenzweig, A., and M.C. Nussenzweig. 2007. A backup DNA repair pathway moves to the forefront. Cell. 131:223-225. http://dx.doi.org/10.1016/j .cell.2007.10.005
43. Nussenzweig, A., and M.C. Nussenzweig. 2010. Origin of chromosomal translocations in lymphoid cancer. Cell. 141:27-38. http://dx.doi.org/10 .1016/j.cell.2010.03.016
44. Panier, S., and D. Durocher. 2013. Push back to respond better: regulatory inhibition of the DNA double-strand break response. Nat. Rev. Mol. Cell Biol. 14:661-672. http://dx.doi.org/10.1038/nrm3659
45. Pearce, M.S., J.A. Salotti, M.P. Little, K. McHugh, C. Lee, K.P. Kim, N.L. Howe, C.M. Ronckers, P. Rajaraman, A.W. Sir Craft, et al. 2012. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet. 380:499-505. http://dx.doi.org/10.1016/S0140-6736(12)60815-0
46. Peterson, S.E., Y. Li, F. Wu-Baer, B.T. Chait, R. Baer, H. Yan, M.E. Gottesman, and J. Gautier. 2013. Activation of DSB processing requires phosphorylation of CtIP by ATR. Mol. Cell. 49:657-667. http://dx.doi.org/10.1016/j .molcel.2012.11.020
47. Polo, S.E., and S.P. Jackson. 2011. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25:409- 433. http://dx.doi.org/10.1101/gad.2021311
48. Quennet, V., A. Beucher, O. Barton, S. Takeda, and M. Löbrich. 2011. CtIP and MRN promote non-homologous end-joining of etoposide-induced DNA double-strand breaks in G1. Nucleic Acids Res. 39:2144-2152. http:// dx.doi.org/10.1093/nar/gkq1175
49. Rass, E., A. Grabarz, I. Plo, J. Gautier, P. Bertrand, and B.S. Lopez. 2009. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 16:819-824. http://dx.doi.org/10 .1038/nsmb.1641
50. Reczek, C.R., M. Szabolcs, J.M. Stark, T. Ludwig, and R. Baer. 2013. The interaction between CtIP and BRCA1 is not essential for resection-mediated DNA repair or tumor suppression. J. Cell Biol. 201:693-707. http:// dx.doi.org/10.1083/jcb.201302145
51. Reinhardt, H.C., and M.B. Yaffe. 2013. Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Nat. Rev. Mol. Cell Biol. 14:563-580. http://dx.doi.org/10.1038/nrm3640
52. Rief, N., and M. Löbrich. 2002. Efficient rejoining of radiation-induced DNA double-strand breaks in centromeric DNA of human cells. J. Biol. Chem. 277:20572-20582. http://dx.doi.org/10.1074/jbc.M200265200
53. Rothkamm, K., I. Krüger, L.H. Thompson, and M. Löbrich. 2003. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23:5706-5715. http://dx.doi.org/10.1128/MCB.23.16.5706- 5715.2003
54. Sartori, A.A., C. Lukas, J. Coates, M. Mistrik, S. Fu, J. Bartek, R. Baer, J. Lukas, and S.P. Jackson. 2007. Human CtIP promotes DNA end resection. Nature. 450:509-514. http://dx.doi.org/10.1038/nature06337
55. Shibata, A., S. Conrad, J. Birraux, V. Geuting, O. Barton, A. Ismail, A. Kakarougkas, K. Meek, G. Taucher-Scholz, M. Löbrich, and P.A. Jeggo. 2011. Factors determining DNA double-strand break repair pathway choice in G2 phase. EMBO J. 30:1079-1092. http://dx.doi.org/10 .1038/emboj.2011.27
56. Stephan, H., C. Concannon, E. Kremmer, M.P. Carty, and H.P. Nasheuer. 2009. Ionizing radiation-dependent and independent phosphorylation of the 32-kDa subunit of replication protein A during mitosis. Nucleic Acids Res. 37:6028-6041. http://dx.doi.org/10.1093/nar/gkp605
57. van Gent, D.C., and M. van der Burg. 2007. Non-homologous end-joining, a sticky affair. Oncogene. 26:7731-7740. http://dx.doi.org/10.1038/sj.onc.1210871
58. van Gent, D.C., J.H. Hoeijmakers, and R. Kanaar. 2001. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2:196-206. http://dx.doi.org/10.1038/35056049
59. Wang, H., B. Rosidi, R. Perrault, M. Wang, L. Zhang, F. Windhofer, and G. Iliakis. 2005. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 65:4020-4030. http://dx.doi.org/10.1158/0008-5472.CAN-04-3055
60. Wang, H., L.Z. Shi, C.C. Wong, X. Han, P.Y. Hwang, L.N. Truong, Q. Zhu, Z. Shao, D.J. Chen, M.W. Berns, et al. 2013. The interaction of CtIP and Nbs1 connects CDK and ATM to regulate HR-mediated double-strand break repair. PLoS Genet. 9:e1003277. http://dx.doi.org/10.1371/journal .pgen.1003277
61. Wang, M., W. Wu, W. Wu, B. Rosidi, L. Zhang, H. Wang, and G. Iliakis. 2006. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 34:6170-6182. http://dx.doi .org/10.1093/nar/gkl840
62. Weichert, W., C. Denkert, M. Schmidt, V. Gekeler, G. Wolf, M. Köbel, M. Dietel, and S. Hauptmann. 2004. Polo-like kinase isoform expression is a prognostic factor in ovarian carcinoma. Br. J. Cancer. 90:815-821. http:// dx.doi.org/10.1038/sj.bjc.6601610
63. Weichert, W., G. Kristiansen, K.J. Winzer, M. Schmidt, V. Gekeler, A. Noske, B.M. Müller, S. Niesporek, M. Dietel, and C. Denkert. 2005. Polo-like kinase isoforms in breast cancer: expression patterns and prognostic implications. Virchows Arch. 446:442-450. http://dx.doi.org/10.1007/s00428-005-1212-8
64. Weinstock, D.M., E. Brunet, and M. Jasin. 2007. Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol. 9:978-981.
65. Ying, S., S. Minocherhomji, K.L. Chan, T. Palmai-Pallag, W.K. Chu, T. Wass, H.W. Mankouri, Y. Liu, and I.D. Hickson. 2013. MUS81 promotes common fragile site expression. Nat. Cell Biol. 15:1001-1007. http://dx.doi .org/10.1038/ncb2773
66. Yu, X., and J. Chen. 2004. DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24:9478-9486. http://dx.doi.org/10 .1128/MCB.24.21.9478-9486.2004
67. Yu, X., S. Fu, M. Lai, R. Baer, and J. Chen. 2006. BRCA1 ubiquitinates its phosphorylation- dependent binding partner CtIP. Genes Dev. 20:1721-1726. http://dx.doi.org/10.1101/gad.1431006
68. Yun, M.H., and K. Hiom. 2009. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature . 459:460-463. http://dx.doi.org/10.1038/nature07955
69. Zhang, Y., and M. Jasin. 2011. An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat. Struct. Mol. Biol. 18:80-84. http://dx.doi.org/10.1038/nsmb.1940
70. Zimmerman, W.C., and R.L. Erikson. 2007. Polo-like kinase 3 is required for entry into S phase. Proc. Natl. Acad. Sci. USA. 104:1847-1852. http:// dx.doi.org/10.1073/pnas.0610856104
71. Zimmermann, M., F. Lottersberger, S.B. Buonomo, A. Sfeir, and T. de Lange. 2013. 53BP1 regulates DSB repair using Rif1 to control 5? end resection. Science. 339:700-704. http://dx.doi.org/10.1126/science.1231573