Requirement for Parp-1 and DNA ligases 1 or 3 but not of Xrcc1 in chromosomal translocation formation by backup end joining

Nucleic Acids Research

Volumn 42, Issue 10, 2014, Pages 6380-6392

  Soni, Aashish ^a   Siemann, Maria ^a   Grabos, Martha ^a   Murmann, Tamara ^a   Pantelias, Gabriel E ^b   Iliakis, George ^a  

^a UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

^b INSTITUTE OF NUCLEAR TECHNOLOGY AND RADIATION PROTECTION   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE 1; POLYDEOXYRIBONUCLEOTIDE SYNTHASE 3; POLYDEOXYRIBONUCLEOTIDE SYNTHASE 4; RAD54 PROTEIN; UNCLASSIFIED DRUG; XRCC1 PROTEIN;

ARTICLE; BACKUP NONHOMOLOGOUS END JOINING; CARCINOGENESIS; CELL CYCLE G2 PHASE; CELL DEATH; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA END JOINING REPAIR; DNA END RESECTION; DNA MISREPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; G2 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; HUMAN; HUMAN CELL; METAPHASE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; PRIORITY JOURNAL; PROTEIN FUNCTION; RAD54 GENE; RADIATION DOSE; RADIATION EXPOSURE; RECOMBINATION REPAIR;

ANIMALS; CELLS, CULTURED; CRICETINAE; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA LIGASES; DNA-BINDING PROTEINS; G2 PHASE; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MICE; POLY(ADP-RIBOSE) POLYMERASES; RADIATION, IONIZING; RECOMBINATIONAL DNA REPAIR; TRANSLOCATION, GENETIC;

EID: 84903167737     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku298     Document Type: Article

References (63)

1. Roukos, V., Voss, T.C., Schmidt, C.K., Lee, S., Wangsa, D. and Misteli, T. (2013) Spatial dynamics of chromosome translocations in living cells. Science, 341, 660-664.
2. Bunting, S.F. and Nussenzweig, A. (2013) End-joining, translocations and cancer. Nat. Rev. Cancer, 13, 443-454.
3. Loucas, B.D. and Cornforth, M.N. (2013) The LET dependence of unrepaired chromosome damage in human cells: a break too far? Radiat. Res., 179, 393-405.
4. Lieber, M.R. (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem., 79, 1.1-1.31.
5. Mladenov, E. and Iliakis, G. (2011) Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mut. Res./Fundamental Mol. Mech. Mutagen., 711, 61-72.
6. Kinner, A., Wu, W., Staudt, C. and Iliakis, G. (2008) γ-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res., 36, 5678-5694.
7. San Filippo, J., Sung, P. and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem., 77, 229-257.
8. Iliakis, G. (2009) Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother. Oncol., 92, 310-315.
9. Schipler, A. and Iliakis, G. (2013) DNA double-strand-break complexity levels and their possible contributions to the probability for error-prone processing and repair pathway choice. Nucleic Acids Res., 41, 7589-7605.
10. Audebert, M., Salles, B. and Calsou, P. (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.
11. Wang, H., Rosidi, B., Perrault, R., Wang, M., Zhang, L., Windhofer, F. and Iliakis, G. (2005) DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res., 65, 4020-4030.
12. Mansour, W.Y., Rhein, T. and Dahm-Daphi, J. (2010) The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies. Nucleic Acids Res., 38, 6065-6077.
13. Liang, L., Deng, L., Nguyen, S.C., Zhao, X., Maulion, C.D., Shao, C. and Tischfield, J.A. (2008) Human DNA ligases I and III, but not ligase IV, are required for microhomology-mediated end joining of DNA double-strand breaks. Nucleic Acids Res., 36, 3297-3310.
14. Arakawa, H., Bednar, T., Wang, M., Paul, K., Mladenov, E., Bencsik-Theilen, A.A. and Iliakis, G. (2012) Functional redundancy between DNA ligases I and III in DNA replication in vertebrate cells. Nucleic Acids Res., 40, 2599-2610.
15. Paul, K., Wang, M., Mladenov, E., Bencsik-Theilen, A.A., Bednar, T., Wu, W., Arakawa, H. and Iliakis, G. (2013) DNA ligases I and III cooperate in alternative non-homologous end-joining in vertebrates. PLoS One, 8, e59505.
16. Rass, E., Grabarz, A., Plo, I., Gautier, J., Bertrand, P. and Lopez, B.S. (2009) Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol., 16, 819-825.
17. Dinkelmann, M., Spehalski, E., Stoneham, T., Buis, J., Wu, Y., Sekiguchi, J.M. and Ferguson, D.O. (2009) Multiple functions of MRN in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol., 16, 808-813.
18. Xie, A., Kwok, A. and Scully, R. (2009) Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol., 16, 814-818.
19. Zhang, Y. and Jasin, M. (2011) An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat. Struct. Mol. Biol., 18, 80-84.
20. Zhang, Y. and Rowley, J.D. (2006) Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair, 5, 1282-1297.
21. Kelly, L.M. and Gilliland, D.G. (2002) Genetics of myeloid leukemias. Annu. Rev. Genom. Hum. Genet., 3, 179-198.
22. Nickoloff, J.A., De Haro, L.P., Wray, J. and Hromas, R. (2008) Mechanisms of leukemia translocations. Curr. Opin. Hematol., 15, 338-345.
23. Ferguson, D.O., Sekiguchi, J.M., Chang, S., Frank, K.M., Gao, Y., DePinho, R.A. and Alt, F.W. (2000) The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc. Natl. Acad. Sci. U.S.A., 97, 6630-6633.
24. Weinstock, D.M., Brunet, E. and Jasin, M. (2007) Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol., 9, 978-981.
25. Simsek, D. and Jasin, M. (2010) Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat. Struct. Mol. Biol., 17, 410-416.
26. Simsek, D., Brunet, E., Wong, S.Y.-W., Katyal, S., Gao, Y., McKinnon, P.J., Lou, J., Zhang, L., Li, J., Rebar, E.J. et al. (2011) DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet., 7, e1002080.
27. Combs, S.E. and Debus, J. (2013) Treatment with heavy charged particles: systematic review of clinical data and current clinical (comparative) trials. Acta Oncol., 52, 1272-1286.
28. Boboila, C., Oksenych, V., Gostissa, M., Wang, J.H., Zha, S., Zhang, Y., Chai, H., Lee, C.-S., Jankovic, M., Saez, L.-M.A. et al. (2012) Robust chromosomal DNA repair via alternative end-joining in the absence of X-ray repair cross-complementing protein 1 (XRCC1). Proc. Natl. Acad. Sci. U.S.A., 109, 2473-2478.
29. Wang, M., Wu, W., Wu, W., Rosidi, B., Zhang, L., Wang, H. and Iliakis, G. (2006) PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res., 34, 6170-6182.
30. Bryant, H.E., Schultz, N., Thomas, H.D., Parker, K.M., Flower, D., Lopez, E., Kyle, S., Meuth, M., Curtin, N.J. and Helleday, T. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913-917.
31. Farmer, H., McCabe, N., Lord, C.J., Tutt, A.N.J., Johnson, D.A., Richardson, T.B., Santarosa, M., Dillon, K.J., Hickson, I., Knights, C. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
32. Wray, J., Williamson, E.A., Singh, S.B., Wu, Y., Cogle, C.R., Weinstock, D.M., Zhang, Y., Lee, S.-H., Zhou, D., Shao, L. et al. (2013) PARP1 is required for chromosomal translocations. Blood, 121, 4359-4365.
33. Wu, W., Wang, M., Wu, W., Singh, S.K., Mussfeldt, T. and Iliakis, G. (2008) Repair of radiation induced DNA double strand breaks by backup NHEJ is enhanced in G2. DNA Repair, 7, 329-338.
34. 2 in Chinese hamster mutant cells with defects in the classical pathway of NHEJ. Radiat. Res., 170, 512-520.
35. Yang, Y.-G., Cortes, U., Patnaik, S., Jasin, M. and Wang, Z.-Q. (2004) Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene, 23, 3872-3882.
36. Chen, X., Zhong, S., Zhu, X., Dziegielewska, B., Ellenberger, T., Wilson, G.M., MacKerell, A.D. Jr and Tomkinson, A.E. (2008) Rational design of human DNA ligase inhibitors that target cellular DNA replication and repair. Cancer Res., 68, 3169-3177.
37. Bryant, P.E., Mozdarani, H. and Marr, C. (2008) G2-phase chromatid break kinetics in irradiated DNA repair mutant hamster cell lines using calyculin-induced PCC and colcemid-block. Mutat. Res., 657, 8-12.
38. V Forment, Josep, V Walker, Rachael and P Jackson, Stephen (2012) A high-throughput, flow cytometry-based method to quantify DNA-end resection in mammalian cells. Cytometry. Part A : the journal of the International Society for Analytical Cytology, 81, 922-928. [PubMed]
39. Bryant, P.E. and Mozdarani, H. (2007) A comparison of G2 phase radiation-induced chromatid break kinetics using calyculin-PCC with those obtained using colcemid block. Mutagenesis, 22, 359-362.
40. Shovman, O., Riches, A.C., Adamson, D. and Bryant, P.E. (2008) An improved assay for radiation-induced chromatid breaks using a colcemid block and calyculin-induced PCC combination. Mutagenesis, 23, 267-270.
41. Terry, S.Y.A., Riches, A.C. and Bryant, P.E. (2009) Suppression of topoisomerase IIα expression and function in human cells decreases chromosomal radiosensitivity. Mut. Res./Fundamental Mol. Mech. Mutagen., 663, 40-45.
42. Bryant, P.E., Riches, A.C. and Terry, S.Y.A. (2010) Mechanisms of the formation of radiation-induced chromosomal aberrations. Mut. Res./Genet. Toxicol. Environment. Mutagen., 701, 23-26.
43. Bryant, P.E., Riches, A.C., Shovman, O., Dewar, J.A. and Adamson, D.J.A. (2012) Topoisomerase IIα levels and G2 radiosensitivity in T-lymphocytes of women presenting with breast cancer. Mutagenesis, 27, 737-741.
44. DiBiase, S.J., Zeng, Z.-C., Chen, R., Hyslop, T., Curran, W.J. Jr and Iliakis, G. (2000) DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res., 60, 1245-1253.
45. Singh, S.K., Wu, W., Wu, W., Wang, M. and Iliakis, G. (2009) Extensive repair of DNA double-strand breaks in cells deficient in the DNA-PK dependent pathway of NHEJ after exclusion of heat-labile sites. Radiat. Res., 172, 152-164.
46. Iliakis, G., Wang, H., Perrault, A.R., Boecker, W., Rosidi, B., Windhofer, F., Wu, W., Guan, J., Terzoudi, G. and Pantelias, G. (2004) Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome. Res., 104, 14-20.
47. Robert, I., Dantzer, F. and Reina-San-Martin, B. (2009) Parp1 facilitates alternative NHEJ, whereas Parp2 suppresses IgH/c-myc translocations during immunoglobulin class switch recombination. J. Exp. Med., 206, 1047-1056.
48. Abdelkarim, G.E., Gertz, K., Harms, C., Katchanov, J., Dirnagl, U., Szabo, C. and Endres, M. (2001) Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke. Int. J. Mol. Med., 7, 255-260.
49. Garcia Soriano, F., Virag, L., Jagtap, P., Szabo, E., Mabley, J.G., Liaudet, L., Marton, A., Hoyt, D.G., Murthy, K.G.K., Salzman, A.L. et al. (2001) Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nat. Med., 7, 108-113.
50. Fattah, F., Lee, E.H., Weisensel, N., Wang, Y., Lichter, N. and Hendrickson, E.A. (2010) Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet., 6, e1000855.
51. Shibata, A., Moiani, D., Arvai, A.S., Perry, J., Harding, S.M., Genois, M.-M., Maity, R., van Rossum-Fikkert, S., Kertokalio, A., Romoli, F. et al. (2014) DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol. Cell, 53, 7-18.
52. Iliakis, G., Wu, W., Wang, M., Terzoudi, G.I. and Pantelias, G.E. (2007) Backup Pathways of Nonhomologous End joining May Have a Dominant Role in the Formation of Chromosome Aberrations. In: Obe, G. and Vijayalaxmi, (eds). Chromosomal Alterations. Springer Verlag, Berlin, Heidelberg, New York, pp. 67-85.
53. Boboila, C., Alt, F.W. and Schwer, B. (2012) In Frederick, W.A. (ed.), Advances in Immunology, Vol. 116. Academic Press, pp. 1-49.
54. Alt, Frederick W., Zhang, Y., Meng, F.-L., Guo, C. and Schwer, B. (2013) Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell, 152, 417-429.
55. McVey, M. and Lee, S.E. (2008) MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet., 24, 529-538.
56. Deriano, L., Stracker, T.H., Baker, A., Petrini, J.H.J. and Roth, D.B. (2009) Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Mol. Cell, 34, 13-25.
57. Truong, L.N., Li, Y., Shi, L.Z., Hwang, P.Y.-H., He, J., Wang, H., Razavian, N., Berns, M.W. and Wu, X. (2013) Microhomology-mediated end joining and homologus recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc. Natl. Acad. Sci. U.S.A., 110, 7720-7725.
58. Zhu, C., Mills, K.D., Ferguson, D.O., Lee, C., Manis, J., Fleming, J., Gao, Y., Morton, C.C. and Alt, F.W. (2002) Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell, 109, 811-821.
59. Weinstock, D.M., Elliott, B. and Jasin, M. (2006) A model of oncogenic rearrangements: differences between chromosomal translocation mechanisms and simple double-strand break repair. Blood, 107, 777-780.
60. Lord, C.J. and Ashworth, A. (2013) Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat. Med., 19, 1381-1388.
61. Lord, C.J. and Ashworth, A. (2012) The DNA damage response and cancer therapy. Nature, 481, 287-294.
62. Saribasak, H., Maul, R.W., Cao, Z., McClure, R.L., Yang, W., McNeill, D.R., Wilson, D.M. and Gearhart, P.J. (2011) XRCC1 suppresses somatic hypermutation and promotes alternative nonhomologous end joining in Igh genes. J. Exp. Med., 208, 2209-2216.
63. Han, L., Mao, W. and Yu, K. (2012) X-ray repair cross-complementing protein 1 (XRCC1) deficiency enhances class switch recombination and is permissive for alternative end joining. Proc. Natl. Acad. Sci. U.S.A., 109, 4604-4608.