53BP1 deficiency combined with telomere dysfunction activates ATR-dependent DNA damage response

Journal of Cell Biology

Volumn 197, Issue 2, 2012, Pages 283-300

  Martínez, Paula ^a   Flores, Juana M ^b   Blasco, Maria A ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; PROTEIN 53BP1; TELOMERIC REPEAT BINDING FACTOR 1; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; NONHISTONE PROTEIN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; TELOMERIC REPEAT BINDING FACTOR 2; TRF2 PROTEIN, MOUSE; TRP53BP1 PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MUTANT; CHROMOSOME ABERRATION; CONTROLLED STUDY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO CELL; EMBRYO DEVELOPMENT; ENZYME PHOSPHORYLATION; FIBROBLAST; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RECOMBINATION REPAIR; SEQUENCE HOMOLOGY; TELOMERE; ANIMAL; C57BL MOUSE; DNA DAMAGE; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA END-JOINING REPAIR; DNA-BINDING PROTEINS; HOMOLOGOUS RECOMBINATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 1; TELOMERIC REPEAT BINDING PROTEIN 2; TUMOR SUPPRESSOR PROTEINS;

EID: 84861934553     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201110124     Document Type: Article

References (71)

1. Audebert, M., B. Salles, and P. Calsou. 2004. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 279:55117-55126. http://dx.doi.org/10.1074/jbc.M404524200
2. Bailey, S.M., M.A. Brenneman, and E.H. Goodwin. 2004. Frequent recombination in telomeric DNA may extend the proliferative life of telomerasenegative cells. Nucleic Acids Res. 32:3743-3751. http://dx.doi.org/10.1093/nar/gkh691
3. 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. http://dx.doi.org/10.1083/jcb.200503043
4. Blasco, M.A. 2007. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 8:299-309. http://dx.doi.org/10.1038/nrg2047
5. 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. http://dx.doi.org/10.1016/j.cell.2006.10.043
6. 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 triplenegative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17:688-695. http://dx.doi.org/10.1038/nsmb.1831
7. 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. http://dx.doi.org/10.1016/j.cell.2010.03.012
8. Cao, L., X. Xu, S.F. Bunting, J. Liu, R.H. Wang, L.L. Cao, J.J. Wu, T.N. Peng, J. Chen, A. Nussenzweig, et al. 2009. A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol. Cell. 35:534-541. http://dx.doi.org/10.1016/j.molcel.2009.06.037
9. Celli, G.B., and T. de Lange. 2005. DNA processing is not required for ATMmediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7:712-718. http://dx.doi.org/10.1038/ncb1275
10. Celli, G.B., E.L. Denchi, and T. de Lange. 2006. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 8:885-890. http://dx.doi.org/10.1038/ncb1444
11. Chiang, Y.J., S.H. Kim, L. Tessarollo, J. Campisi, and R.J. Hodes. 2004. Telomere-associated protein TIN2 is essential for early embryonic development through a telomerase-independent pathway. Mol. Cell. Biol. 24:6631-6634. http://dx.doi.org/10.1128/MCB.24.15.6631-6634.2004
12. Chin, L., S.E. Artandi, Q. Shen, A. Tam, S.L. Lee, G.J. Gottlieb, C.W. Greider, and R.A. DePinho. 1999. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell. 97:527-538. http://dx.doi.org/10.1016/S0092-8674(00)80762-X
13. Corneo, B., R.L. Wendland, L. Deriano, X. Cui, I.A. Klein, S.Y. Wong, S. Arnal, A.J. Holub, G.R. Weller, B.A. Pancake, et al. 2007. Rag mutations reveal robust alternative end joining. Nature. 449:483-486. http://dx.doi.org/10.1038/nature06168
14. d'Adda di Fagagna, F., P.M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N.P. Carter, and S.P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature. 426:194-198. http://dx.doi.org/10.1038/nature02118
15. de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A.M. Carr, A.R. Lehmann, and J.H. Hoeijmakers. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479-482. http://dx.doi.org/10.1016/S0960-9822(00)00447-4
16. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110. http://dx.doi.org/10.1101/gad.1346005
17. de Lange, T. 2009. How telomeres solve the end-protection problem. Science. 326:948-952. http://dx.doi.org/10.1126/science.1170633
18. Denchi, E.L. 2009. Give me a break: how telomeres suppress the DNA damage response. DNA Repair (Amst.). 8:1118-1126. http://dx.doi.org/10.1016/j.dnarep.2009.04.013
19. 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. http://dx.doi.org/10.1038/nature07433
20. Dunham, M.A., A.A. Neumann, C.L. Fasching, and R.R. Reddel. 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26:447-450. http://dx.doi.org/10.1038/82586
21. Elson, A., Y. Wang, C.J. Daugherty, C.C. Morton, F. Zhou, J. Campos-Torres, and P. Leder. 1996. Pleiotropic defects in ataxia-telangiectasia proteindeficient mice. Proc. Natl. Acad. Sci. USA. 93:13084-13089. http://dx.doi.org/10.1073/pnas.93.23.13084
22. Espejel, S., P. Klatt, J. Ménissier-de Murcia, J. Martín-Caballero, J.M. Flores, G. Taccioli, G. de Murcia, and M.A. Blasco. 2004. Impact of telomerase ablation on organismal viability, aging, and tumorigenesis in mice lacking the DNA repair proteins PARP-1, Ku86, or DNA-PKcs. J. Cell Biol. 167:627-638. http://dx.doi.org/10.1083/jcb.200407178
23. 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, et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993-997. http://dx.doi.org/10.1038/ncb884
24. Haber, J.E. 2008. Alternative endings. Proc. Natl. Acad. Sci. USA. 105:405-406. http://dx.doi.org/10.1073/pnas.0711334105
25. Hendzel, M.J., Y. Wei, M.A. Mancini, A. Van Hooser, T. Ranalli, B.R. Brinkley, D.P. Bazett-Jones, and C.D. Allis. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma. 106:348-360. http://dx.doi.org/10.1007/s004120050256
26. Hockemeyer, D., J.P. Daniels, H. Takai, and T. de Lange. 2006. Recent expansion of the telomeric complex in rodents: Two distinct POT1 proteins protect mouse telomeres. Cell. 126:63-77. http://dx.doi.org/10.1016/j.cell.2006.04.044
27. Jazayeri, A., J. Falck, C. Lukas, J. Bartek, G.C. Smith, J. Lukas, and S.P. Jackson. 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8:37-45. http://dx.doi.org/10.1038/ncb1337
28. Karlseder, J., D. Broccoli, Y. Dai, S. Hardy, and T. de Lange. 1999. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science. 283:1321-1325. http://dx.doi.org/10.1126/science.283.5406.1321
29. Karlseder, J., L. Kachatrian, H. Takai, K. Mercer, S. Hingorani, T. Jacks, and T. de Lange. 2003. Targeted deletion reveals an essential function for the telomere length regulator Trf1. Mol. Cell. Biol. 23:6533-6541. http://dx.doi.org/10.1128/MCB.23.18.6533-6541.2003
30. Kibe, T., G.A. Osawa, C.E. Keegan, and T. de Lange. 2010. Telomere protection by TPP1 is mediated by POT1a and POT1b. Mol. Cell. Biol. 30:1059-1066. http://dx.doi.org/10.1128/MCB.01498-09
31. Lazzerini Denchi, E., G. Celli, and T. de Lange. 2006. Hepatocytes with extensive telomere deprotection and fusion remain viable and regenerate liver mass through endoreduplication. Genes Dev. 20:2648-2653. http://dx.doi.org/10.1101/gad.1453606
32. Lieber, M.R. 2008. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 283:1-5. http://dx.doi.org/10.1074/jbc.R700039200
33. Mahaney, B.L., K. Meek, and S.P. Lees-Miller. 2009. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous endjoining. Biochem. J. 417:639-650. http://dx.doi.org/10.1042/BJ20080413
34. 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. http://dx.doi.org/10.1038/ni1067
35. Martínez, P., and M.A. Blasco. 2010. Role of shelterin in cancer and aging. Aging Cell. 9:653-666. http://dx.doi.org/10.1111/j.1474-9726.2010.00596.x
36. Martínez, P., and M.A. Blasco. 2011. Telomeric and extra-telomeric roles for telomerase and the telomere-binding proteins. Nat. Rev. Cancer. 11:161-176. http://dx.doi.org/10.1038/nrc3025
37. Martínez, P., M. Thanasoula, P. Muñoz, C. Liao, A. Tejera, C. McNees, J.M. Flores, O. Fernández-Capetillo, M. Tarsounas, and M.A. Blasco. 2009. Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev. 23:2060-2075. http://dx.doi.org/10.1101/gad.543509
38. Maser, R.S., K.K. Wong, E. Sahin, H. Xia, M. Naylor, H.M. Hedberg, S.E. Artandi, and R.A. DePinho. 2007. DNA-dependent protein kinase catalytic subunit is not required for dysfunctional telomere fusion and checkpoint response in the telomerase-deficient mouse. Mol. Cell. Biol. 27:2253-2265. http://dx.doi.org/10.1128/MCB.01354-06
39. Mimitou, E.P., and L.S. Symington. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature. 455:770-774. http://dx.doi.org/10.1038/nature07312
40. Mimitou, E.P., and L.S. Symington. 2009. DNA end resection: many nucleases make light work. DNA Repair (Amst.). 8:983-995. http://dx.doi.org/10.1016/j.dnarep.2009.04.017
41. Modesti, M., and R. Kanaar. 2001. DNA repair: spot(light)s on chromatin. Curr. Biol. 11:R229-R232. http://dx.doi.org/10.1016/S0960-9822(01)00112-9
42. Muñoz, P., R. Blanco, J.M. Flores, and M.A. Blasco. 2005. XPF nucleasedependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat. Genet. 37:1063-1071. http://dx.doi.org/10.1038/ng1633
43. Muñoz, P., R. Blanco, G. de Carcer, S. Schoeftner, R. Benetti, J.M. Flores, M. Malumbres, and M.A. Blasco. 2009. TRF1 controls telomere length and mitotic fidelity in epithelial homeostasis. Mol. Cell. Biol. 29:1608-1625. http://dx.doi.org/10.1128/MCB.01339-08
44. Murga, M., S. Bunting, M.F. Montaña, R. Soria, F. Mulero, M. Cañamero, Y. Lee, P.J. McKinnon, A. Nussenzweig, and O. Fernandez-Capetillo. 2009. A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging. Nat. Genet. 41:891-898. http://dx.doi.org/10.1038/ng.420
45. 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
46. Palm, W., and T. de Lange. 2008. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42:301-334. http://dx.doi.org/10.1146/annurev.genet.41.110306.130350
47. Pierce, A.J., P. Hu, M. Han, N. Ellis, and M. Jasin. 2001. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15:3237-3242. http://dx.doi.org/10.1101/gad.946401
48. 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. http://dx.doi.org/10.1038/emboj.2010.142
49. 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. http://dx.doi.org/10.1083/jcb.153.3.613
50. Samper, E., F.A. Goytisolo, P. Slijepcevic, P.P. van Buul, and M.A. Blasco. 2000. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 1:244-252. http://dx.doi.org/10.1093/embo-reports/kvd051
51. 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
52. Sfeir, A., S.T. Kosiyatrakul, D. Hockemeyer, S.L. MacRae, J. Karlseder, C.L. Schildkraut, and T. de Lange. 2009. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell. 138:90-103. http://dx.doi.org/10.1016/j.cell.2009.06.021
53. Sfeir, A., S. Kabir, M. van Overbeek, G.B. Celli, and T. de Lange. 2010. Loss of Rap1 induces telomere recombination in the absence of NHEJ or a DNA damage signal. Science. 327:1657-1661. http://dx.doi.org/10.1126/science.1185100
54. Smogorzewska, A., and T. de Lange. 2004. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73:177-208. http://dx.doi.org/10.1146/annurev.biochem.73.071403.160049
55. Soulas-Sprauel, P., G. Le Guyader, P. Rivera-Munoz, V. Abramowski, C. Olivier-Martin, C. Goujet-Zalc, P. Charneau, and J.P. de Villartay. 2007. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 204:1717-1727. http://dx.doi.org/10.1084/jem.20070255
56. Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-1556. http://dx.doi.org/10.1016/S0960-9822(03)00542-6
57. Tejera, A.M., M. Stagno d'Alcontres, M. Thanasoula, R.M. Marion, P. Martinez, C. Liao, J.M. Flores, M. Tarsounas, and M.A. Blasco. 2010. TPP1 is required for TERT recruitment, telomere elongation during nuclear reprogramming, and normal skin development in mice. Dev. Cell. 18:775-789. http://dx.doi.org/10.1016/j.devcel.2010.03.011
58. Thanasoula, M., J.M. Escandell, P. Martinez, S. Badie, P. Muñoz, M.A. Blasco, and M. Tarsounas. 2010. p53 prevents entry into mitosis with uncapped telomeres. Curr. Biol. 20:521-526. http://dx.doi.org/10.1016/j.cub.2010.01.046
59. van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell. 92:401-413. http://dx.doi.org/10.1016/S0092-8674(00)80932-0
60. Varley, H., H.A. Pickett, J.L. Foxon, R.R. Reddel, and N.J. Royle. 2002. Molecular characterization of inter-telomere and intra-telomere mutations in human ALT cells. Nat. Genet. 30:301-305. http://dx.doi.org/10.1038/ng834
61. Wang, B., S. Matsuoka, P.B. Carpenter, and S.J. Elledge. 2002. 53BP1, a mediator of the DNA damage checkpoint. Science. 298:1435-1438. http://dx.doi.org/10.1126/science.1076182
62. 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
63. Ward, I.M., K. Minn, K.G. Jorda, and J. Chen. 2003a. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278:19579-19582. http://dx.doi.org/10.1074/jbc.C300117200
64. Ward, I.M., K. Minn, J. van Deursen, and J. Chen. 2003b. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23:2556-2563. http://dx.doi.org/10.1128/MCB.23.7.2556-2563.2003
65. 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. http://dx.doi.org/10.1083/jcb.200403021
66. Williams, R.S., G. Moncalian, J.S. Williams, Y. Yamada, O. Limbo, D.S. Shin, L.M. Groocock, D. Cahill, C. Hitomi, G. Guenther, et al. 2008. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell. 135:97-109. http://dx.doi.org/10.1016/j.cell.2008.08.017
67. Wong, K.K., R.S. Maser, E. Sahin, S.T. Bailey, H. Xia, H. Ji, K. McNamara, M. Naylor, R.T. Bronson, S. Ghosh, et al. 2007. Diminished lifespan and acute stress-induced death in DNA-PKcs-deficient mice with limiting telomeres. Oncogene. 26:2815-2821. http://dx.doi.org/10.1038/sj.onc.1210099
68. Wu, L., A.S. Multani, H. He, W. Cosme-Blanco, Y. Deng, J.M. Deng, O. Bachilo, S. Pathak, H. Tahara, S.M. Bailey, et al. 2006. Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell. 126:49-62. http://dx.doi.org/10.1016/j.cell.2006.05.037
69. Xie, A., A. Hartlerode, M. Stucki, S. Odate, N. Puget, A. Kwok, G. Nagaraju, C. Yan, F.W. Alt, J. Chen, et al. 2007. Distinct roles of chromatinassociated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell. 28:1045-1057. http://dx.doi.org/10.1016/j.molcel.2007.12.005
70. Yan, C.T., C. Boboila, E.K. Souza, S. Franco, T.R. Hickernell, M. Murphy, S. Gumaste, M. Geyer, A.A. Zarrin, J.P. Manis, et al. 2007. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature. 449:478-482. http://dx.doi.org/10.1038/nature06020
71. Zou, L., and S.J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 300:1542-1548. http://dx.doi.org/10.1126/science.1083430