Replication stress induces 53BP1-containing OPT domains in G1 cells

Journal of Cell Biology

Volumn 193, Issue 1, 2011, Pages 97-108

  Harrigan, Jeanine A ^a   Belotserkovskaya, Rimma ^a   Coates, Julia ^a   Dimitrova, Daniela S ^b   Polo, Sophie E ^a   Bradshaw, Charles R ^a   Fraser, Peter ^b   Jackson, Stephen P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; BINDING PROTEIN; HISTONE H2AX; OCTAMER TRANSCRIPTION FACTOR 1; P53 BINDING PROTEIN 1; PROTEIN P53; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL NUCLEUS INCLUSION BODY; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME FRAGILE SITE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ANALYSIS;

CELLS, CULTURED; DNA REPLICATION; G1 PHASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; OCTAMER TRANSCRIPTION FACTOR-1; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 79955490586     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201011083     Document Type: Article

References (46)

1. Ahel, D., Z. Horejsí, N. Wiechens, S.E. Polo, E. Garcia-Wilson, I. Ahel, H. Flynn, M. Skehel, S.C. West, S.P. Jackson, et al. 2009. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science. 325:1240-1243. doi:10.1126/science.1177321
2. Bouwman, P., A. Aly, J.M. Escandell, M. Pieterse, J. Bartkova, H. van der Gulden, S. Hiddingh, M. Thanasoula, A. Kulkarni, Q. Yang, et al. 2010. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17:688-695. doi:10.1038/nsmb.1831
3. Branzei, D., and M. Foiani. 2010. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11:208-219. doi:10.1038/nrm2852
4. Bunting, S.F., E. Callén, N. Wong, H.T. Chen, F. Polato, A. Gunn, A. Bothmer, N. Feldhahn, O. Fernandez-Capetillo, L. Cao, et al. 2010. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 141:243-254. doi:10.1016/j.cell.2010.03.012
5. Celeste, A., O. Fernandez-Capetillo, M.J. Kruhlak, D.R. Pilch, D.W. Staudt, A. Lee, R.F. Bonner, W.M. Bonner, and A. Nussenzweig. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675-679. doi:10.1038/ncb1004
6. Chan, K.L., P.S. North, and I.D. Hickson. 2007. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 26:3397-3409. doi:10.1038/sj.emboj.7601777
7. Chan, K.L., T. Palmai-Pallag, S. Ying, and I.D. Hickson. 2009. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11:753-760. doi:10.1038/ncb1882
8. Chapman, J.R., and S.P. Jackson. 2008. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 9:795-801. doi:10.1038/embor.2008.103
9. Ciccia, A., and S.J. Elledge. 2010. The DNA damage response: making it safe to play with knives. Mol. Cell. 40:179-204. doi:10.1016/j.molcel.2010.09.019
10. Cremer, M., F. Grasser, C. Lanctôt, S. Müller, M. Neusser, R. Zinner, I. Solovei, and T. Cremer. 2008. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods Mol. Biol. 463:205-239. doi:10.1007/978-1-59745-406-3_15
11. Doil, C., N. Mailand, S. Bekker-Jensen, P. Menard, D.H. Larsen, R. Pepperkok, J. Ellenberg, S. Panier, D. Durocher, J. Bartek, et al. 2009. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell. 136:435-446. doi:10.1016/j.cell.2008.12.041
12. Difilippantonio, S., E. Gapud, N. Wong, C.Y. Huang, G. Mahowald, H.T. Chen, M.J. Kruhlak, E. Callen, F. Livak, M.C. Nussenzweig, et al. 2008. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature. 456:529-533. doi:10.1038/nature07476
13. Dimitrova, D.S. 2009. Visualization of DNA replication sites in mammalian nuclei. Methods Mol. Biol. 521:413-436.
14. Dimitrova, N., Y.C. Chen, D.L. Spector, and T. de Lange. 2008. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature. 456:524-528. doi:10.1038/nature07433
15. Durkin, S.G., and T.W. Glover. 2007. Chromosome fragile sites. Annu. Rev. Genet. 41:169-192. doi:10.1146/annurev.genet.41.042007.165900
16. Galanty, Y., R. Belotserkovskaya, J. Coates, S. Polo, K.M. Miller, and S.P. Jackson. 2009. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature. 462:935-939. doi:10.1038/nature08657
17. Glover, T.W., C. Berger, J. Coyle, and B. Echo. 1984. DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum. Genet. 67:136-142. doi:10.1007/BF00272988
18. Hickson, I., Y. Zhao, C.J. Richardson, S.J. Green, N.M. Martin, A.I. Orr, P.M. Reaper, S.P. Jackson, N.J. Curtin, and G.C. Smith. 2004. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64:9152-9159. doi:10.1158/0008-5472.CAN-04-2727
19. Howlett, N.G., T. Taniguchi, S.G. Durkin, A.D. D'Andrea, and T.W. Glover. 2005. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum. Mol. Genet. 14:693-701. doi:10.1093/hmg/ddi065
20. Iacovoni, J.S., P. Caron, I. Lassadi, E. Nicolas, L. Massip, D. Trouche, and G. Legube. 2010. High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29:1446-1457. doi:10.1038/emboj.2010.38
21. Kent, W.J., C.W. Sugnet, T.S. Furey, K.M. Roskin, T.H. Pringle, A.M. Zahler, and D. Haussler. 2002. The human genome browser at UCSC. Genome Res. 12:996-1006.
22. Lempiäinen, H., and T.D. Halazonetis. 2009. Emerging common themes in regulation of PIKKs and PI3Ks. EMBO J. 28:3067-3073. doi:10.1038/emboj.2009.281
23. Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754-1760. doi:10.1093/bioinformatics/btp324
24. Li, L., K. Roy, S. Katyal, X. Sun, S. Bléoo, and R. Godbout. 2006. Dynamic nature of cleavage bodies and their spatial relationship to DDX1 bodies, Cajal bodies, and gems. Mol. Biol. Cell. 17:1126-1140. doi:10.1091/mbc.E05-08-0768
25. Li, L., E.A. Monckton, and R. Godbout. 2008. A role for DEAD box 1 at DNA double-strand breaks. Mol. Cell. Biol. 28:6413-6425. doi:10.1128/MCB.01053-08
26. Lovejoy, C.A., and D. Cortez. 2009. Common mechanisms of PIKK regulation. DNA Repair (Amst.). 8:1004-1008. doi:10.1016/j.dnarep.2009.04.006
27. Manis, J.P., J.C. Morales, Z. Xia, J.L. Kutok, F.W. Alt, and P.B. Carpenter. 2004. 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat. Immunol. 5:481-487. doi:10.1038/ni1067
28. Morales, J.C., Z. Xia, T. Lu, M.B. Aldrich, B. Wang, C. Rosales, R.E. Kellems, W.N. Hittelman, S.J. Elledge, and P.B. Carpenter. 2003. Role for the BRCA1 C-terminal repeats (BRCT) protein 53BP1 in maintaining genomic stability. J. Biol. Chem. 278:14971-14977. doi:10.1074/jbc.M212484200
29. Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods. 11:205-214. doi:10.1006/meth.1996.0407
30. Palm, W., and T. de Lange. 2008. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42:301-334. doi:10.1146/annurev.genet.41.110306.130350
31. Pombo, A., P. Cuello, W. Schul, J.B. Yoon, R.G. Roeder, P.R. Cook, and S. Murphy. 1998. Regional and temporal specialization in the nucleus: a transcriptionally-active nuclear domain rich in PTF, Oct1 and PIKA antigens associates with specific chromosomes early in the cell cycle. EMBO J. 17:1768-1778. doi:10.1093/emboj/17.6.1768
32. Qin, Z.S., J. Yu, J. Shen, C.A. Maher, M. Hu, S. Kalyana-Sundaram, J. Yu, and A.M. Chinnaiyan. 2010. HPeak: an HMM-based algorithm for defining read-enriched regions in ChIP-Seq data. BMC Bioinformatics. 11:369. doi:10.1186/1471-2105-11-369
33. Rai, R., H. Zheng, H. He, Y. Luo, A. Multani, P.B. Carpenter, and S. Chang. 2010. The function of classical and alternative non-homologous endjoining pathways in the fusion of dysfunctional telomeres. EMBO J. 29:2598-2610. doi:10.1038/emboj.2010.142
34. Reina-San-Martin, B., J. Chen, A. Nussenzweig, and M.C. Nussenzweig. 2007. Enhanced intra-switch region recombination during immunoglobulin class switch recombination in 53BP1-/- B cells. Eur. J. Immunol. 37:235-239. doi:10.1002/eji.200636789
35. Robertson, G., M. Hirst, M. Bainbridge, M. Bilenky, Y. Zhao, T. Zeng, G. Euskirchen, B. Bernier, R. Varhol, A. Delaney, et al. 2007. Genomewide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods. 4:651-657. doi:10.1038/nmeth1068
36. Salic, A., and T.J. Mitchison. 2008. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA. 105:2415-2420. doi:10.1073/pnas.0712168105
37. 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. doi:10.1038/nature06337
38. 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. doi:10.1083/jcb.151.7.1381
39. Schwartz, M., E. Zlotorynski, and B. Kerem. 2006. The molecular basis of common and rare fragile sites. Cancer Lett. 232:13-26. doi:10.1016/j.canlet.2005.07.039
40. Shanbhag, N.M., I.U. Rafalska-Metcalf, C. Balane-Bolivar, S.M. Janicki, and R.A. Greenberg. 2010. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell. 141:970-981. doi:10.1016/j.cell.2010.04.038
41. Spector, D.L. 2006. SnapShot: Cellular bodies. Cell. 127:1071. doi:10.1016/j.cell.2006.11.026
42. Stucki, M., and S.P. Jackson. 2006. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst.). 5:534-543. doi:10.1016/j.dnarep.2006.01.012
43. Ward, I.M., K. Minn, J. van Deursen, and J. Chen. 2003. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23:2556-2563. doi:10.1128/MCB.23.7.2556-2563.2003
44. Ward, I.M., B. Reina-San-Martin, A. Olaru, K. Minn, K. Tamada, J.S. Lau, M. Cascalho, L. Chen, A. Nussenzweig, F. Livak, et al. 2004. 53BP1 is required for class switch recombination. J. Cell Biol. 165:459-464. doi:10.1083/jcb.200403021
45. Zhang, Y., T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137. doi:10.1186/gb-2008-9-9-r137
46. Zwilling, S., A. Annweiler, and T. Wirth. 1994. The POU domains of the Oct1 and Oct2 transcription factors mediate specific interaction with TBP. Nucleic Acids Res. 22:1655-1662. doi:10.1093/nar/22.9.1655