Importance of the cell cycle phase for the choice of the appropriate DSB repair pathway, for genome stability maintenance: The trans-S double-strand break repair model

Cell Cycle

Volumn 7, Issue 1, 2008, Pages 33-38

  Delacôte, Fabien ^a   Lopez, Bernard S ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

Cell cycle; Double strand break; Genome rearrangements; Homologous recombination; Mammalian cells; Nonhomologous end joining

Indexed keywords

DOUBLE STRANDED DNA;

CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENE REARRANGEMENT; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; REVIEW; SISTER CHROMATID;

MAMMALIA;

EID: 38349145553     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.1.5149     Document Type: Review

References (52)

1. Jung D, Alt FW. Unraveling V(D)J recombination; insights into gene regulation. Cell 2004;116:299-311.
2. Cohen PE, Pollard JW. Regulation of meiotic recombination and prophase I progression in mammals. Bioessays 2001; 23:996-1009.
3. Kleckner N. Meiosis: how could it work? Proc Natl Acad Sci USA 1996; 93:8167-74.
4. Jackson SP, Jeggo PA. DNA double-strand break repair and V(D)J recombination: involvement of DNA-PK. Trends Biochem Sci 1995; 20:412-5.
5. Guirouilh-Barbat J et al. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol Cell 2004; 14:611-23.
6. Revy P, Malivert L, de Villartay JP. Cernunnos-XLF, a recently identified non-homologous end-joining factor required for the development of the immune system. Curr Opin Allergy Clin Immunol 2006; 6:416-20.
7. Feldmann E, Schmiemann V, Goedecke W, Reichenberger S, Pfeiffer P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res 2000; 28:2585-96.
8. Paques F, Haber JE. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 1999; 63:349-404.
9. Liu N et al. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol Cell 1998; 1:783-93.
10. Sonoda E et al. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 1998; 17:598-608.
11. Difilippantonio MJ et al. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 2000; 404:510-4.
12. Ferguson DO et al. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc Natl Acad Sci USA 2000;97:6630-3.
13. Bertrand P, Lambert S, Joubert C, Lopez BS. Overexpression of mammalian Rad51 does not stimulate tumorigenesis while a dominant-negative Rad51 affects centrosome fragmentation, ploidy and stimulates tumorigenesis, in p53-defective CHO cells. Oncogene 2003;22:7587-92.
14. Amor M, Parker KL, Globerman H, New MI, White PC. Mutation in the CYP21B gene (Ile-172-Asn) causes steroid 21-hydroxylase deficiency. Proc Natl Acad Sci USA 1988;85:1600-4.
15. Purandare SM, Patel PI. Recombination hot spots and human disease. Genome Res 1997;7:773-86.
16. Greaves MF, Wiemels J. Origins of chromosome translocations in childhood leukaemia. Nat Rev Cancer 2003; 3:639-49.
17. Zucman-Rossi J, Legoix P, Victor JM, Lopez B, Thomas G. Chromosome translocation based on illegitimate recombination in human tumors. Proc Natl Acad Sci USA 1998;95:11786-91.
18. Weinstock DM, Elliott B, Jasin M. A model of oncogenic rearrangements: differences between chromosomal translocation mechanisms and simple double-strand break repair. Blood 2006; 107:777-80.
19. Saintigny Y et al. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J 2001; 20:3861-70.
20. Couedel C et al. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev 2004; 18:1293-304.
21. Mills KD et al. Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev 2004; 18:1283-92.
22. Fabre F, Boulet A, Roman H. Gene conversion at different points in the mitotic cycle of Saccharomyces cerevisiae. Mol Gen Genet 1984; 195:139-43.
23. Kadyk LC, Hartwell LH. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 1992; 132:387-402.
24. Johnson RD, Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J 2000; 19:3398-407.
25. Guirouilh-Barbat J, Huck S, Lopez BS. S phase progression stimulates both the mutagenic KU-independent pathway and mutagenic processing of KU-dependant intermediates, for non homologous end joining. Oncogene In press.
26. Zhu C et al. Unrepaired DNA Breaks in p53-Deficient Cells Lead to Oncogenic Gene Amplification Subsequent to Translocations. Cell 2002; 109:811-21.
27. Difilippantonio MJ et al. Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification. J Exp Med 2002; 196:469-80.
28. Brouillette S, Chartrand P. Intermolecular recombination assay for mammalian cells that produces recombinants carrying both homologous and nonhomologous junctions. Mol Cell Biol 1987; 7:2248-55.
29. Belmaaza A, Wallenburg JC, Brouillette S, Gusew N, Chartrand P. Genetic exchange between endogenous and exogenous LINE-1 repetitive elements in mouse cells. Nucleic Acids Res 1990; 18:6385-91.
30. Belmaaza A, Chartrand P. One-sided invasion events in homologous recombination at double-strand breaks. Mutat Res 1994; 314:199-208.
31. Richardson C, Jasin M. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol Cell Biol 2000; 20:9068-75.
32. Pierce AJ, Hu P, Han M, Ellis N, Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 2001; 15:3237-42.
33. Delacote F, Han M, Stamato TD, Jasin M, Lopez BS. An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res 2002; 30:3454-63.
34. Allen C, Kurimasa A, Brenneman MA, Chen DJ, Nickoloff JA. DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc Natl Acad Sci USA 2002; 99:3758-63.
35. Cheong N, Wang X, Wang Y, Iliakis G. Loss of S-phase-dependent radioresistance in irs-1 cells exposed to X-rays. Mutat Res 1994; 314:77-85.
36. Takata M et al. 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 1998; 17:5497-508.
37. Rothkamm K, Kruger I, Thompson LH, Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003; 23:5706-15.
38. Hinz JM, Yamada NA, Salazar EP, Tebbs RS, Thompson LH. Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Repair (Amst) 2005; 4:782-92.
39. 1 checkpoint-defective cells. Oncogene 2007;26:2769-80.
40. Yuan ZM et al. Regulation of Rad51 function by c-Abl in response to DNA damage. J Biol Chem 1998; 273:3799-802.
41. Aten JA et al. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 2004; 303:92-5.
42. Kim JS et al. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J Cell Biol 2005; 170:341-7.
43. Esashi F et al. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 2005; 434:598-604.
44. Saleh-Gohari N, Helleday T. Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucleic Acids Res 2004; 32:3683-8.
45. Rodrigue A et al. Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J 2006; 25:222-31.
46. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 1995; 92:2298-302.
47. Ira G et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 2004; 431:1011-7.
48. Jazayeri A et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006; 8:37-45.
49. Gangloff S, Soustelle C, Fabre F. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat Genet 2000; 25:192-4.
50. Saintigny Y, Makienko K, Swanson C, Emond MJ, Monnat RJ, Jr. Homologous recombination resolution defect in werner syndrome. Mol Cell Biol 2002; 22:6971-8.
51. Lambert S, Lopez BS. Characterization of mammalian RAD51 double strand break repair using non lethal dominant negative forms. EMBO J. 2000; 19:3090-9.
52. Michel B et al. Rescue of arrested replication forks by homologous recombination. Proc Natl Acad Sci USA 2001; 98:8181-8.