Repair of radiation induced DNA double strand breaks by backup NHEJ is enhanced in G2

DNA Repair

Volumn 7, Issue 2, 2008, Pages 329-338

  Wu, Wenqi ^a   Wang, Minli ^a   Wu, Weizhong ^a   Singh, Satyendra K ^a   Mussfeldt, Tamara ^a   Iliakis, George ^a  

^a UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

Author keywords

Backup pathways; Cell cycle; DNA double strand breaks (DSBs); DNA Ligase IV; Homologous recombination repair (HRR); Ionizing radiation (IR); Non homologous end joining (NHEJ); Rad54

Indexed keywords

KU ANTIGEN; LIGASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RAD54 PROTEIN;

ANIMAL CELL; ARTICLE; ASSAY; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; FIBROBLAST; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; MOUSE; MUTANT; NONHOMOLOGOUS END JOINING; NONHUMAN; PLASMID; PRIORITY JOURNAL; RADIATION INJURY;

ANIMALS; ANTIGENS, NUCLEAR; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; DNA BREAKS, DOUBLE-STRANDED; DNA LIGASES; DNA REPAIR; DNA-BINDING PROTEINS; EMBRYO RESEARCH; FLOW CYTOMETRY; G2 PHASE; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS;

EUKARYOTA;

EID: 37549006429     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.11.008     Document Type: Article

References (56)

1. Symington L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66 (2002) 630-670
2. Jackson S.P. Sensing and repairing DNA double-strand breaks. Carcinogenesis 23 (2002) 687-696
3. Valerie K., and Povirk L.F. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22 (2003) 5792-5812
4. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4 (2003) 1-11
5. Wyman C., Ristic D., and Kanaar R. Homologous recombination-mediated double-strand break repair. DNA Repair (Amst.) 3 (2004) 827-833
6. Paques F., and Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63 (1999) 349-404
7. Johnson R.D., and Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19 (2000) 3398-3407
8. Jasin M. Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene 21 (2002) 8981-8993
9. Tamulevicius P., Wang M., and Iliakis G. Homology-directed repair is required for the development of radioresistance during S phase: interplay between double-strand break repair and checkpoint response. Radiat. Res. 167 (2007) 1-11
10. Thompson L.H., and Schild D. Recombinational DNA repair and human disease. Mutat. Res. 509 (2002) 49-78
11. Lieber M.R., Ma Y., Pannicke U., and Schwarz K. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4 (2003) 712-720
12. Mills K.D., Ferguson D.O., and Alt F.W. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 194 (2003) 77-95
13. Rothkamm K., Krüger I., Thompson L.H., and Löbrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23 (2003) 5706-5715
14. Metzger L., and Iliakis G. Kinetics of DNA double strand breaks throughout the cell cycle as assayed by pulsed field gel electrophoresis in CHO cells. Int. J. Radiat. Biol. 59 (1991) 1325-1339
15. Iliakis G., Wang H., Perrault A.R., Boecker W., Rosidi B., Windhofer F., Wu W., Guan J., Terzoudi G., and Pantelias G. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome Res. 104 (2004) 14-20
16. Wang H., Zeng Z.-C., Bui T.-A., Sonoda E., Takata M., Takeda S., and Iliakis G. Efficient rejoining of radiation-induced DNA double-strand breaks in vertebrate cells deficient in genes of the RAD52 epistasis group. Oncogene 20 (2001) 2212-2224
17. DiBiase S.J., Zeng Z.-C., Chen R., Hyslop T., Curran Jr. W.J., and Iliakis G. DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res. 60 (2000) 1245-1253
18. Perrault R., Wang H., Wang M., Rosidi B., and Iliakis G. Backup pathways of NHEJ are suppressed by DNA-PK. J. Cell. Biochem. 92 (2004) 781-794
19. Wang H., Rosidi B., Perrault R., Wang M., Zhang L., Windhofer F., and Iliakis G. DNA Ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 65 (2005) 4020-4030
20. Audebert M., Salles B., and Calsou P. 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 (2004) 55117-55126
21. Wang M., Wu W., Wu W., Rosidi B., Zhang L., Wang H., and Iliakis G. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 34 (2006) 6170-6182
22. Caldecott K.W. Mammalian DNA single-strand break repair: an X-ra(y)ted affair. Bioessays 23 (2001) 447-455
23. Kabotyanski E.B., Gomelsky L., Han J.-O., Stamato T.D., and Roth D.B. Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res. 26 (1998) 5333-5342
24. Verkaik N.S., Esveldt-van Lange R.E.E., van Heemst D., Brüggenwirth H.T., Hoeijmakers J.H.J., Zdzienicka M.Z., and van Gent D.C. Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells. Eur. J. Immunol. 32 (2002) 701-709
25. Soulas-Sprauel P., Le Guyader G., Rivera-Munoz P., Abramowski V., Olivier-Martin C., Goujet-Zalc C., Charneau P., and de Villartay J.-P. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 204 (2007) 1717-1727
26. Corneo B., Wendland R.L., Deriano L., Cui X., Klein I.A., Wong S.-Y., Arnal S., Holub A.J., Weller G.R., et al. Rag mutations reveal robust alternative end joining. Nature 449 (2007) 483-486
27. Nussenzweig A., and Nussenzweig M.C. A backup DNA repair pathway moves to the forefront. Cell 131 (2007) 223-225
28. Yan C.T., Boboila C., Souza E.K., Franco S., Hickernell T.R., Murphy M., Gumaste S., Geyer M., Zarrin A.A., et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449 (2007) 478-482
29. Essers J., Hendriks R.W., Swagemakers S.M.A., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H.J., and Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89 (1997) 195-204
30. Dronkert M.L., Beverloo H.B., Johnson R.D., Hoeijmakers J.H., Jasin M., and Kanaar R. Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol. Cell. Biol. 20 (2000) 3147-3156
31. Mills K.D., Ferguson D.O., Essers J., Eckersdorff M., Kanaar R., and Alt F.W. Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev. 18 (2004) 1283-1292
32. Frank K.M., Sharpless N.E., Gao Y., Sekiguchi J.M., Fergson D.O., Zhu C., Manis J.P., Horner J., DePinho R.A., and Alt F.W. DNA Ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5 (2000) 993-1002
33. Gao Y., Chaudhuri Y., Zhu C., Davidson L., Weaver D.T., and Alt F.W. A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity 9 (1998) 367-376
34. Taccioli G.E., Amatucci A.G., Beamish H.J., Gell D., Xiang X.H., Arzayus M.I.T., Priestley A., Jackson S.P., Rothstein A.M., et al. Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity. Immunity 9 (1998) 355-366
35. Ouyang B.H., Nussenzweig A., Kurimasa A., da Costa Soares V., Li X., Cordon-Cardo C., Li W.-h., Cheong N., Nussenzweig M., et al. Ku70 is required for DNA repair but not for T cell antigen receptor gene recombination in vivo. J. Exp. Med. 186 (1997) 921-929
36. Windhofer F., Wu W., and Iliakis G. Low levels of DNA ligases III and IV sufficient for effective NHEJ (p n/a). J. Cell. Physiol. 213 (2007) 475-483
37. Seluanov A., Mittelman D., Pereira-Smith O.M., Wilson J.H., and Gorbunova V. DNA end joining becomes less efficient and more error-prone during cellular senescence. Proc. Natl. Acad. Sci. USA 101 (2004) 7624-7629
38. Borrelli M.J., Mackey M.A., and Dewey W.C. A method for freezing synchronous mitotic and G1 cells. Exp. Cell Res. 170 (1987) 363-368
39. Iliakis G., Metzger L., Denko N., and Stamato T.D. Detection of DNA double strand breaks in synchronous cultures of CHO cells by means of asymmetric field inversion gel electrophoresis. Int. J. Radiat. Biol. 59 (1991) 321-341
40. Wang H., Perrault A.R., Takeda Y., Qin W., Wang H., and Iliakis G. Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res. 31 (2003) 5377-5388
41. Mateos S., Slijepcevic P., MacLeod R.A.F., and Bryant P.E. DNA double-strand break rejoining in xrs5 cells is more rapid in the G2 than in the G1 phase of the cell cycle. Mutat. Res. 315 (1994) 181-187
42. Lee S.E., Mitchell R.A., Cheng A., and Hendrickson E.A. Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell. Biol. 17 (1997) 1425-1433
43. Windhofer F., Wu W., Wang M., Singh S.K., Saha J., Rosidi B., and Iliakis G. Marked dependence on growth state of backup pathways of NHEJ. Int. J. Radiat. Oncol. Biol. Phys. 68 (2007) 1462-1470
44. 2 Phase DNA Double-strand Break Repair. J. Biol. Chem. 276 (2001) 44413-44418
45. Pierce A.J., Hu P., Han M., Ellis N., and Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15 (2001) 3237-3242
46. Delacote F., Han M., Stamato T.D., Jasin M., and Lopez B.S. An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res. 30 (2002) 3454-3463
47. Allen C., Halbrook J., and Nickoloff J.A. Interactive competition between homologous recombination and non-homologous end joining. Mol Cancer Res 10 (2003) 913-920
48. Tan T.L.R., Kanaar R., and Wyman C. Rad54, a Jack of all trades in homologous recombination. DNA Repair (Amst.) 2 (2003) 787-794
49. Heyer W.-D., Li X., Rolfsmeier M., and Zhang X.-P. Rad54: the Swiss Army knife of homologous recombination?. Nucleic Acids Res. 34 (2006) 4115-4125
50. Jaco I., Munoz P., Goytisolo F., Wesoly J., Bailey S., Taccioli G., and Blasco M.A. Role of mammalian Rad54 in telomere length maintenance. Mol. Cell. Biol. 23 (2003) 5572-5580
51. Couedel C., Mills K.D., Barchi M., Shen L., Olshen A., Johnson R.D., Nussenzweig A., Essers J., Kanaar R., et al. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev. 18 (2004) 1293-1304
52. Essers J., van Steeg H., de Wit J., Swagemakers S.M., Vermeij M., Hoeijmakers J.H., and Kanaar R. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J. 19 (2000) 1703-1710
53. -/- mutant of the chicken DT40 cell line. Cell 89 (1997) 185-193
54. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., and Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break. EMBO J. 17 (1998) 5497-5508
55. Ward J.F. DNA damage produced by ionizing radiation in mammalian cells: Identities, mechanisms of formation, and reparability. Prog. Nucl. Acid Res. 35 (1988) 95-125
56. Asaad N.A., Zeng Z.-C., Guan J., Thacker J., and Iliakis G. Homologous recombination as a potential target for caffeine radiosensitization in mammalian cells: Reduced caffeine radiosensitization in XRCC2 and XRCC3 mutants. Oncogene 19 (2000) 5788-5800