Uncoupling of RAD51 focus formation and cell survival after replication fork stalling in RAD51D null CHO cells

Environmental and Molecular Mutagenesis

Volumn 53, Issue 2, 2012, Pages 114-124

  Urbin, Salustra S ^a   Elvers, Ingegerd ^b   Hinz, John M ^c   Helleday, Thomas ^b   Thompson, Larry H ^a  

^a LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

DNA replication; Homologous recombination; Hydroxyurea; RAD51 foci; RAD51 paralogs

Indexed keywords

APHIDICOLIN; CAMPTOTHECIN; HYDROXYUREA; KU 58684; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE S PHASE; CELL DEATH; CELL GROWTH; CELL SURVIVAL; CHO CELL; CYTOTOXICITY; DNA REPAIR; DNA REPLICATION; FEMALE; IN VITRO STUDY; NONHUMAN; PULSED FIELD GEL ELECTROPHORESIS; RECOMBINATION REPAIR;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CHO CELLS; CRICETINAE; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA-BINDING PROTEINS; ENZYME INHIBITORS; GENE KNOCKOUT TECHNIQUES; HYDROXYUREA; KINETICS; MUTANT PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; RAD51 RECOMBINASE;

EUKARYOTA; VERTEBRATA;

EID: 84856563780     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.21672     Document Type: Article

References (66)

1. Adachi N, So S, Koyama H. 2004. Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of topoisomerase I-mediated DNA damage. J Biol Chem 279: 37343-37348.
2. Arnaudeau C, Lundin C, Helleday T. 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.
3. Audebert M, Salles B, 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.
4. Bertrand P, Rouillard D, Boulet A, Levalois C, Soussi T, Lopez BS. 1997. Increase of spontaneous intrachromosomal homologous recombination in mammalian cells expressing a mutant p53 protein. Oncogene 14: 1117-1122.
5. Braybrooke JP, Li JL, Wu L, Caple F, Benson FE, Hickson ID. 2003. Functional interaction between the Bloom's syndrome helicase and the RAD51 paralog, RAD51L3 (RAD51D). J Biol Chem 278: 48357-48366.
6. Braybrooke JP, Spink KG, Thacker J, Hickson ID. 2000. The RAD51 family member, RAD51L3, Is a DNA-stimulated ATPase that forms a complex with XRCC2. J Biol Chem 275: 29100-29106.
7. Bryant HE, Helleday T. 2006. Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res 34: 1685-1691.
8. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. 2005. Specific killing of BRCA2-deficient tumors with inhibitors of poly(ADP-ribose) polymerase. Nature 434: 913-917.
9. Chaung W, Mi LJ, Boorstein RJ. 1997. The p53 status of Chinese hamster V79 cells frequently used for studies on DNA damage and DNA repair. Nucleic Acids Res 25: 992-994.
10. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, et al. 2005. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434: 917-921.
11. Franchitto A, Pirzio LM, Prosperi E, Sapora O, Bignami M, Pichierri P. 2008. Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81-dependent pathway. J Cell Biol 183: 241-252.
12. Godthelp BC, Wiegant WW, Van Duijn-Goedhart A, Scharer OD, Van Buul PP, Kanaar R, Zdzienicka MZ. 2002. Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability. Nucleic Acids Res 30: 2172-2182.
13. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC. 1995. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92: 2298-2302.
14. Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, Maas A, Essers J, Hickson ID, Kanaar R. 2007. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 14: 1096-1104.
15. Henry-Mowatt J, Masson JY, Johnson PA, Clements PM, Benson FE, Thompson LH, Takeda S, West SC, Caldecott KW. 2003. XRCC3 and Rad51 modulate replication fork progression on damaged vertebrate chromosomes. Mol Cell 11: 1109-1117.
16. Hinz JM, Helleday T, Meuth M. 2003. Reduced apoptotic response to camptothecin in CHO cells deficient in XRCC3. Carcinogenesis 24: 249-253.
17. Hinz JM, Tebbs RS, Wilson PF, Nham PB, Salazar EP, Nagasawa H, Urbin SS, Bedford JS, Thompson LH. 2006. Repression of mutagenesis by Rad51D-mediated homologous recombination. Nucleic Acids Res 34: 1358-1368.
18. Hiyama T, Katsura M, Yoshihara T, Ishida M, Kinomura A, Tonda T, Asahara T, Miyagawa K. 2006. Haploinsufficiency of the Mus81-Eme1 endonuclease activates the intra-S-phase and G2/M checkpoints and promotes rereplication in human cells. Nucleic Acids Res 34: 880-892.
19. Hoy CA, Salazar EP, Thompson LH. 1984. Rapid detection of DNA-damaging agents using repair-deficient CHO cells. Mutat Res 130: 321-332.
20. Hsiang YH, Liu LF. 1988. Identification of mammalian DNA topoisomerase I as an intracellular target of the anticancer drug camptothecin. Cancer Res 48: 1722-1726.
21. Hu T, Miller CM, Ridder GM, Aardema MJ. 1999. Characterization of p53 in Chinese hamster cell lines CHO-K1, CHO-WBL, and CHL: Implications for genotoxicity testing. Mutat Res 426: 51-62.
22. Janz C, Wiesmuller L. 2002. Wild-type p53 inhibits replication-associated homologous recombination. Oncogene 21: 5929-5933.
23. Jones NJ, Ellard S, Waters R, Parry EM. 1993. Cellular and chromosomal hypersensitivity to DNA crosslinking agents and topoisomerase inhibitors in the radiosensitive Chinese hamster irs mutants: Phenotypic similarities to ataxia telangiectasia and Fanconi's anaemia cells. Carcinogenesis 14: 2487-2494.
24. Koc A, Wheeler LJ, Mathews CK, Merrill GF. 2004. Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J Biol Chem 279: 223-230.
25. Kraakman-van der Zwet M, Overkamp WJ, van Lange RE, Essers J, van Duijn-Goedhart A, Wiggers I, Swaminathan S, van Buul PP, Errami A, Tan RT, et al. 2002. Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol Cell Biol 22: 669-679.
26. Krokan H, Wist E, Krokan RH. 1981. Aphidicolin inhibits DNA synthesis by DNA polymerase alpha and isolated nuclei by a similar mechanism. Nucleic Acids Res 9: 4709-4719.
27. Kumari A, Schultz N, Helleday T. 2004. p53 protects from replication-associated DNA double-strand breaks in mammalian cells. Oncogene 23: 2324-2329.
28. Kurumizaka H, Ikawa S, Nakada M, Eda K, Kagawa W, Takata M, Takeda S, Yokoyama S, Shibata T. 2001. Homologous-pairing activity of the human DNA-repair proteins Xrcc3.Rad51C. Proc Natl Acad Sci USA 98: 5538-5543.
29. Kurumizaka H, Ikawa S, Nakada M, Enomoto R, Kagawa W, Kinebuchi T, Yamazoe M, Yokoyama S, Shibata T. 2002. Homologous-pairing, and ring- and filament-structure formation activities of the human Xrcc2-Rad51D complex. J Biol Chem 277: 14315-14320.
30. Lee H, Larner JM, Hamlin JL. 1997. Cloning and characterization of Chinese hamster p53 cDNA. Gene 184: 177-183.
31. Lio YC, Mazin AV, Kowalczykowski SC, Chen DJ. 2003. Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro. J Biol Chem 278: 2469-2478.
32. Liu N. 2002. XRCC2 is required for the formation of Rad51 foci induced by ionizing radiation and DNA cross-linking agent mitomycin C. J Biomed Biotechnol 2: 106-113.
33. Liu N, Lamerdin JE, Tebbs RS, Schild D, Tucker JD, Shen MR, Brookman KW, Siciliano MJ, Walter CA, Fan W and others. 1998. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA crosslinks and other damages. Mol Cell 1: 783-793.
34. Liu N, Lim CS. 2005. Differential roles of XRCC2 in homologous recombinational repair of stalled replication forks. J Cell Biochem 95: 942-954.
35. Liu N, Schild D, Thelen MP, Thompson LH. 2002. Involvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells. Nucleic Acids Res 30: 1009-1015.
36. Lundin C, Erixon K, Arnaudeau C, Schultz N, Jenssen D, Meuth M, Helleday T. 2002. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol Cell Biol 22: 5869-5878.
37. Masson JY, Tarsounas MC, Stasiak AZ, Stasiak A, Shah R, McIlwraith MJ, Benson FE, West SC. 2001. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev 15: 3296-3307.
38. McCabe N, Turner NC, Lord CJ, Kluzek K, Bialkowska A, Swift S, Giavara S, O'Connor M J, Tutt AN, Zdzienicka MZ, et al. 2006. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res 66: 8109-8115.
39. Mekeel KL, Tang W, Kachnic LA, Luo CM, De Frank JS, Powell SN. 1997. Inactivation of p53 results in high rates of homologous recombination. Oncogene 14: 1847-1857.
40. Miller KA, Yoshikawa DM, McConnell IR, Clark R, Schild D, Albala JS. 2002. RAD51C interacts with RAD51B and is central to a larger protein complex in vivo exclusive of RAD51. J Biol Chem 277: 8406-8411.
41. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. 2010. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 37: 492-502.
42. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. 2010. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 10: 293-301.
43. Saintigny Y, Lopez BS. 2002. Homologous recombination induced by replication inhibition, is stimulated by expression of mutant p53. Oncogene 21: 488-492.
44. Saintigny Y, Rouillard D, Chaput B, Soussi T, Lopez BS. 1999. Mutant p53 proteins stimulate spontaneous and radiation-induced intrachromosomal homologous recombination independently of the alteration of the transactivation activity and of the G1 checkpoint. Oncogene 18: 3553-3563.
45. Saleh-Gohari N, Bryant HE, Schultz N, Parker KM, Cassel TN, Helleday T. 2005. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol Cell Biol 25: 7158-7169.
46. Schultz N, Lopez E, Saleh-Gohari N, Helleday T. 2003. Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res 31: 4959-4964.
47. Sigurdsson S, Van Komen S, Bussen W, Schild D, Albala JS, Sung P. 2001. Mediator function of the human Rad51B-Rad51C complex in Rad51/RPA-catalyzed DNA strand exchange. Genes Dev 15: 3308-3318.
48. Takao N, Kato H, Mori R, Morrison C, Sonada E, Sun X, Shimizu H, Yoshioka K, Takeda S, Yamamoto K. 1999. Disruption of ATM in p53-null cells causes multiple functional abnormalities in cellular response to ionizing radiation. Oncogene 18: 7002-7009.
49. Takata M, Sasaki MS, Sonoda E, Fukushima T, Morrison C, Albala JS, Swagemakers SM, Kanaar R, Thompson LH, Takeda S. 2000. The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol Cell Biol 20: 6476-6482.
50. Takata M, Sasaki MS, Tachiiri S, Fukushima T, Sonoda E, Schild D, Thompson LH, Takeda S. 2001. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol Cell Biol 21: 2858-2866.
51. Thacker J. 2005. The RAD51 gene family, genetic instability and cancer. Cancer Lett 219: 125-135.
52. Thacker J, Ganesh AN. 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.
53. Thompson LH, Hinz JM. 2009. Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: Mechanistic insights. Mutat Res 668: 54-72.
54. Thompson LH, Jones NJ. 2010. Stabilizing and remodeling the blocked DNA replication fork: Anchoring FANCM and the Fanconi anemia damage response. Mol Cell 37: 749-751.
55. Thompson LH, Schild D. 2002. Recombinational DNA repair and human disease. Mutat Res 509: 49-78.
56. Thorslund T, West SC. 2007. BRCA2: A universal recombinase regulator. Oncogene 26: 7720-7730.
57. Tzang BS, Lai YC, Hsu M, Chang HW, Chang CC, Huang PC, Liu YC. 1999. Function and sequence analyses of tumor suppressor gene p53 of CHO.K1 cells. DNA Cell Biol 18: 315-321.
58. Wang M, Wu W, Wu W, Rosidi B, Zhang L, Wang H, 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.
59. Wang X, Takenaka K, Takeda S. 2010. PTIP promotes DNA double-strand break repair through homologous recombination. Genes Cells 15: 243-254.
60. Warren M, Lord CJ, Masabanda J, Griffin D, Ashworth A. 2003. Phenotypic effects of heterozygosity for a BRCA2 mutation. Hum Mol Genet 12: 2645-2656.
61. Wiese C, Collins DW, Albala JS, Thompson LH, Kronenberg A, Schild D. 2002. Interactions involving the Rad51 paralogs Rad51C and XRCC3 in human cells. Nucleic Acids Res 30: 1001-1008.
62. Wiese C, Hinz JM, Tebbs RS, Nham PB, Urbin SS, Collins DW, Thompson LH, Schild D. 2006. Disparate requirements for the Walker A and B ATPase motifs of human RAD51D in homologous recombination. Nucleic Acids Res 34: 2833-2843.
63. Willers H, McCarthy EE, Alberti W, Dahm-Daphi J, Powell SN. 2000. Loss of wild-type p53 function is responsible for upregulated homologous recombination in immortal rodent fibroblasts. Int J Radiat Biol 76: 1055-1062.
64. Xia SJ, Shammas MA, Shmookler Reis RJ. 1997. Elevated recombination in immortal human cells is mediated by HsRAD51 Recombinase. Mol Cell Biol 17: 7171-7158.
65. Yonetani Y, Hochegger H, Sonoda E, Shinya S, Yoshikawa H, Takeda S, Yamazoe M. 2005. Differential and collaborative actions of Rad51 paralog proteins in cellular response to DNA damage. Nucleic Acids Res 33: 4544-4552.
66. Yuan SS, Chang HL, Lee EY. 2003. Ionizing radiation-induced Rad51 nuclear focus formation is cell cycle-regulated and defective in both ATM(-/-) and c-Abl(-/-) cells. Mutat Res 525: 85-92.