Pathways of DNA double-strand break repair during the mammalian cell cycle

Molecular and Cellular Biology

Volumn 23, Issue 16, 2003, Pages 5706-5715

  Rothkamm, Kai ^a   Krüger, Ines ^a   Thompson, Larry H ^b   Löbrich, Markus ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL DEATH; CELL SURVIVAL; CHINESE HAMSTER; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; EPISTASIS; GENETIC RECOMBINATION; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RADIOSENSITIVITY;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BROMODEOXYURIDINE; CELL CYCLE; CELL LINE; CELL NUCLEUS; CHO CELLS; CRICETINAE; DNA DAMAGE; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, RADIATION; FLOW CYTOMETRY; G1 PHASE; G2 PHASE; MICROSCOPY, FLUORESCENCE; PHENOTYPE; RECOMBINATION, GENETIC; S PHASE; TIME FACTORS;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS; MAMMALIA;

EID: 0042632901     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.16.5706-5715.2003     Document Type: Article

References (73)

1. Arnaudeau, C., C. Lundin, and T. Helleday. 2001. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 307:1235-1245.
2. Asaad, N. A., Z. C. Zeng, J. Guan, J. Thacker, and G. Iliakis. 2000. Homologous recombination as a potential target for caffeine radiosensitization in mammalian cells: reduced caffeine radiosensitization in XRCC2 and XRCC3 mutants. Oncogene 19:5788-5800.
3. Baumann, P., and S. C. West. 1997. The human Rad51 protein: polarity of strand transfer and stimulation by hRP-A. EMBO J. 16:5198-5206.
4. Baumann, P., and S. C. West. 1998. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci. 23:247-251.
5. Bezzubova, O., A. Silbergleit, Y. Yamaguchi-Iwai, S. Takeda, and J. M. Buerstedde. 1997. Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line. Cell 89:185-193.
6. Blunt, T., N. J. Finnie, G. E. Taccioli, G. C. Smith, J. Demengeot, T. M. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo, and S. P. Jackson. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80:813-823.
7. Brenneman, M. A., A. E. Weiss, J. A. Nickoloff, and D. J. Chen. 2000. XRCC3 is required for efficient repair of chromosome breaks by homologous recombination. Mutat. Res. 459:89-97.
8. Cartwright, R., C. E. Tambini, P. J. Simpson, and J. Thacker. 1998. The XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family. Nucleic Acids Res. 26:3084-3089.
9. Chang, C., K. A. Biedermann, M. Mezzina, and J. M. Brown, 1993. Characterization of the DNA double strand break repair defect in scid mice. Cancer Res. 53:1244-1248.
10. Cheong, N., Y. Wang, M. Jackson, and G. Iliakis. 1992. Radiation-sensitive irs mutants rejoin DNA double-strand breaks with efficiency similar to that of parental V79 cells but show altered response to radiation-induced G2 delay. Mutat. Res. 274:111-122.
11. Cheong, N., X. Wang, Y. Wang, and G. Iliakis. 1994. Loss of S-phase-dependent radioresistance in irs-1 cells exposed to X-rays. Mutat. Res. 314:77-85.
12. Croimie, G. A., J. C. Connelly, and D. R. F. Leach. 2001. Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. Mol. Cell 8:1163-1174.
13. Cui, X., M. Brenneman, J. Meyne, M. Oshimura, E. H. Goodwin, and D. J. Chen. 1999. The XRCC2 and XRCC3 repair genes are required for chromosome stability in mammalian cells. Mutat. Res. 434:75-88.
14. Dronkert, M. L., H. B. Beverloo, R. D. Johnson, J. H. Hoeijmakers, M. Jasin, and R. Kanaar. 2000. Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol. Cell. Biol. 20:3147-3156.
15. Essers, J., R. W. Hendriks, S. M. Swagemakers, C. Troelstra, J. de Wit, D. Bootsma, J. H. Hoeijmakers, and R. Kanaar. 1997. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89:195-204.
16. Essers, J., H. van Steeg, J. de Wit, S. M. Swagemakers, M. Vermeij, J. H. Hoeijmakers, and R. Kanaar. 2000. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J. 19:1703-1710.
17. Fuller, L. F., and R. B. Painter. 1988. A Chinese hamster ovary line hypersensitive to ionizing radiation and deficient in repair replication. Mutat. Res. 193:109-121.
18. Golub, E. I., R. C. Gupta, T. Haaf, M. S. Wold, and C. M. Radding. 1998. Interaction of human rad51 recombination protein with single-stranded DNA binding protein, RPA. Nucleic Acids Res. 26:5388-5393.
19. Haber, J. E. 1999. DNA recombination: the replication connection. Trends Biochem. Sci. 24:271-275.
20. Haber, J. E. 2000. Partners and pathways repairing a double-strand break. Trends Genet. 16:259-264.
21. Hoeijmakers, J. H. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411:366-374.
22. Jackson, S. P. 2002. Sensing and repairing DNA double-strand breaks. Carcinogenesis 23:687-696.
23. Jeggo, P. A. 1998. DNA breakage and repair. Adv. Genet. 38:185-218.
24. Johnson, R. D., N. Liu, and M. Jasin. 1999. Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination. Nature 401:397-399.
25. Johnson, R. D., and M. Jasin. 2000. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19:3398-3407.
26. Jones, N. J., S. A. Stewart, and L. H. Thompson. 1990. Biochemical and genetic analysis of the Chinese hamster mutants irs1 and irs2 and their comparison to cultured ataxia telangiectasia cells. Mutagenesis 5:15-23.
27. Kühne, M., K. Rothkamm, and M. Löbrich. 2000. No dose-dependence of DNA double-strand break misrejoining following alpha-particle irradiation. Int. J. Radiat. Biol. 76:891-900.
28. Kurimasa, A., S. Kumano, N. V. Boubnov, M. D. Story, C. S. Tung, S. R. Peterson, and D. J. Chen. 1999. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol. Cell, Biol. 19:3877-3884.
29. Lee, S. E., R. A. Mitchell, A. Cheng, and E. A. Hendrickson. 1997. 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. 17:1425-1433.
30. Lim, D. S., and P. Hasty. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:7133-7143.
31. Limoli, C. L., E. Giedzinski, W. M. Bonner, and J. E. Cleaver. 2002. UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, gamma-H2AX formation, and Mre11 relocalization. Proc. Natl. Acad. Sci. USA 99:233-238.
32. Liu, N., J. E. Lamerdin, R. S. Tebbs, D. Schild, J. D. Tucker, M. R. Shen, K. W. Brookman, M. J. Siciliano, C. A. Walter, W. Fan, L. S. Narayana, Z. Q. Zhou, A. W. Adamson, K. J. Sorensen, D. J. Chen, N. J. Jones, and L. R. Thompson. 1998. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol. Cell 1:783-793.
33. Löbrich, M., B. Rydberg, and P. K. Cooper. 1995. Repair of x-ray-induced DNA double-strand breaks in specific NotI restriction fragments in human fibroblasts: joining of correct and incorrect ends. Proc. Natl. Acad. Sci. USA 92:12050-12054.
34. Löbrich, M., M. Kühne, J. Wetzel, and K. Rothkamm. 2000. Joining of correct and incorrect DNA double-strand break ends in normal human and ataxia telangiectasia fibroblasts. Genes Chromosomes Cancer 27:59-68.
35. Lundin, C., K. Erixon, C. Arnaudeau, N. Schultz, D. Jenssen, M. Meuth, and T. Helleday. 2002. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22:5869-5878.
36. Mateos, S., P. Slijepcevic, R. A. MacLeod, and P. E. Bryant. 1994. 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. 315:181-187.
37. Olive, P. L. 1998. The role of DNA single- and double-strand breaks in cell killing by ionizing radiation. Radiat. Res. 150:842-851.
38. Pierce, A. J., R. D. Johnson, L. H. Thompson, and M. Jasin. 1999. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13:2633-2638.
39. Priestley, A., H. J. Beamish, D. Gell, A. G. Amatucci, M. C. Muhlmann-Diaz, B. K. Singleton, G. C. Smith, T. Blunt, L. C. Schalkwyk, J. S. Bedford, S. P. Jackson, P. A. Jeggo, and G. E. Taccioli. 1998. Molecular and biochemical characterisation of DNA-dependent protein kinase-defective rodent mutant irs-20. Nucleic Acids Res. 26:1965-1973.
40. Riballo, E., S. E. Critchlow, S. H. Teo, A. J. Doherty, A. Priestley, B. Broughton, B. Kysela, H. Beamish, N. Plowman, C. F. Arlett, A. R. Lehmann, S. P. Jackson, and P. A. Jeggo. 1999. Identification of a defect in DNA ligase IV in a radiosensitive leukaemia patient. Curr. Biol. 9:699-702.
41. Richardson, C., M. E. Moynahan, and M. Jasin. 1998. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:3831-3842.
42. Richardson, C., and M. Jasin. 2000. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405:697-700.
43. 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.
44. Rijkers, T., J. Van Den Ouweland, B. Morolli, A. G. Rolink, W. M. Baarends, P. P. Van Sloun, P. H. Lohman, and A. Pastink. 1998. Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18:6423-6429.
45. Rogakou, E. P., D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858-5868.
46. Rogakou, E. P., C. Boon, C. Redon, and W. M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905-916.
47. Rothkamm, K., and M. Löbrich. 1999. Misrejoining of DNA double-strand breaks in primary and transformed human and rodent cells: a comparison between the HPRT region and other genomic locations. Mutat. Res. 433:193-205.
48. Rothkamm, K., M. Kühne, P. A. Jeggo, and M. Löbrich. 2001. Radiation-induced genomic rearrangements formed by nonhomologous end-joining of DNA double-strand breaks. Cancer Res. 61:3886-3893.
49. Rothkamm, K., and M. Löbrich. 2003. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc. Natl. Acad. Sci. USA 100:5057-5062.
50. Saintigny, Y., F. Delacote, G. Vares, F. Petitot, S. Lambert, D. Averbeck, and B. S. Lopez. 2001. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20:3861-3870.
51. Sedelnikova, O. A., E. P. Rogakou, I. G. Panyutin, and W. M. Bonner. 2002. Quantitative detection of (125)1dU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat. Res. 158:486-492.
52. Sigurdsson, S., K. Trujillo, B. Song, S. Stratton, and P. Sung. 2001. Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J. Biol. Chem. 276:8798-8806.
53. Smith, G. C., and S. P. Jackson. 1999. The DNA-dependent protein kinase. Genes Dev. 13:916-934.
54. Sonoda, E., M. S. Sasaki, J. M. Buerstedde, O. Bezzubova, A. Shinohara, H, Ogawa, M. Takata, Y. Yamaguchi-Iwai, and S. Takeda. 1998. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:598-608.
55. Stamato, T. D., R. Weinstein, A. Giaccia, and L. Mackenzie. 1983. Isolation of cell cycle-dependent gamma ray-sensitive Chinese hamster ovary cell. Somatic Cell Genet. 9:165-173.
56. Sung, P., K. M. Trujillo, and S. Van Komen. 2000. Recombination factors of Saccharomyces cerevisiae. Mutat. Res. 451:257-275.
57. Takata, M., M. S. Sasaki, E. Sonoda, C. Morrison, M. Hashimoto, H. Utsumi, Y. Yamaguchi-Iwai, A. Shinohara, and S. Takeda. 1998. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17:5497-5508.
58. Takata, M., M. S. Sasaki, S. Tachiiri, T. Fukushima, E. Sonoda, D. Schild, L. H. Thompson, and S. Takeda. 2001. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 21:2858-2866.
59. Tebbs, R. S., Y. Zhao, J. D. Tucker, J. B. Scheerer, M. J. Siciliano, M. Hwang, N. Liu, R. J. Legerski, and L. H. Thompson. 1995. Correction of chromosomal instability and sensitivity to diverse mutagens by a cloned cDNA of the XRCC3 DNA repair gene. Proc. Natl. Acad. Sci. USA 92:6354-6358.
60. Thacker, J., and A. N. Ganesh. 1990. DNA-break repair, radioresistance of DNA synthesis, and camptothecin sensitivity in the radiation-sensitive irs mutants: comparisons to ataxia-telangiectasia cells. Mutat. Res. 235:49-58.
61. Thacker, J. 1999. A surfeit of RAD51-like genes? Trends Genet. 15:166-168.
62. Thompson, L. H., and D. Schild. 1999. The contribution of homologous recombination in preserving genome integrity in mammalian cells. Biochimie 81:87-105.
63. Thompson, L. H., and D. Scbild. 2001. Homologous recombinational repair of DNA ensures mammalian chromosome stability, Mutat. Res. 477:131-153.
64. Thompson, L. H., and D. Schild. 2002. Recombinational DNA repair and human disease. Mutat. Res. 509:49-78.
65. Tucker, J. D., N. J. Jones, N. A. Allen, J. L. Minkler, L. H. Thompson, and A. V. Carrano. 1991. Cytogenetic characterization of the ionizing radiation-sensitive Chinese hamster mutant irs1. Mutat. Res. 254:143-152.
66. Van Dyck, E., A. Z. Stasiak, A. Stasiak, and S. C. West. 1999. Binding of double-strand breaks in DNA by human Rad52 protein. Nature 398:728-731.
67. 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.
68. Vlahos, C. J., W. F. Matter, K. Y. Hui, and R. F. Brown. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241-5248.
69. Wachsberger, P. R., W. H. Li, M. Guo, D. Chen, N. Cheong, C. C. Ling, G. Li, and G. Iliakis. 1999. Rejoining of DNA double-strand breaks in Ku80-deficient mouse fibroblasts. Radiat. Res. 151:398-407.
70. Wang, H., Z. C. Zeng, T. A. Bui, E. Sonoda, M. Takata, S. Takeda, and G. Iliakis. 2001. Efficient rejoining of radiation-induced DNA double-strand breaks in vertebrate cells deficient in genes of the RAD52 epistasis group. Oncogene 20:2212-2224.
71. Ward, I. M., and J. Chen. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276:47759-47762.
72. Whitmore, G. F., A. J. Varghese, and S. Gulyas. 1989. Cell cycle responses of two X-ray sensitive mutants defective in DNA repair. Int. J. Radiat. Biol. 56:657-665.
73. Yamaguchi-Iwai, Y., E. Sonoda, J. M. Buerstedde, O. Bezzubova, C. Morrison, M. Takata, A. Shinohara, and S. Takeda. 1998. Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell. Biol. 18:6430-6435.