Impairment of homologous recombination control in a Fanconi anemia-like Chinese hamster cell mutant

Biology of the Cell

Volumn 96, Issue 7, 2004, Pages 545-552

  Larminat, Florence ^a,b   Germanier, Maryse ^a   Papouli, Efterpi ^a   Defais, Martine ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b Université de Toulouse Paul Sabatier   (France)

Author keywords

DNA interstrand cross link; Fanconi anemia; Gene conversion; Homologous recombination; Rad51

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; DNA BINDING PROTEIN; RAD51 PROTEIN;

ANIMAL; ARTICLE; CELL LINE; DNA REPAIR; FANCONI ANEMIA; GENETIC RECOMBINATION; GENETICS; HAMSTER; METABOLISM; MUTATION; PATHOLOGY;

ANIMALS; BRCA1 PROTEIN; BRCA2 PROTEIN; CELL LINE; CRICETINAE; DNA REPAIR; DNA-BINDING PROTEINS; FANCONI ANEMIA; MUTATION; RAD51 RECOMBINASE; RECOMBINATION, GENETIC;

EID: 16244413138     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1016/j.biolcel.2004.06.001     Document Type: Short Survey

References (53)

1. Akkari, Y.M., Bateman, R.L., Reifsteck, C.A., Olson, S.B., Grompe, M., 2000. DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol. Cell. Biol 20, 8283-8289.
2. Allen, C., Kurimasa, A., Brenneman, M.A., Chen, D.J., Nickoloff, J.A., 2002. DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. USA 99, 3758-3763.
3. Arwert, F., Rooimans, M.A., Westerveld, A., Simons, J.W., Zdzienicka, M.Z., 1991. The Chinese hamster cell mutant V-H4 is homologous to Fanconi anemia (complementation group A). Cytogenet. Cell Genet. 56, 23-26.
4. Baumann, P., West, S.C., 1998. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci 23, 247-251.
5. Bhattacharyya, A., Ear, U.S., Koller, B.H., Weichselbaum, R.R., Bishop, D.K., 2000. The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J Biol Chem 275, 23899-23903.
6. Bishop, D.K., Ear, U., Bhattacharyya, A., Calderone, C., Beckett, M., Weichselbaum, R.R., Shinohara, A., 1998. Xrcc3 is required for assembly of Rad51 complexes in vivo. J Biol Chem 273, 21482-21488.
7. Capizzi, R.L., Jameson, J.W., 1973. A table for the estimation of the spontaneous mutation rate of cells in culture. Mutat Res 17, 147-148.
8. Collins, A.R., 1993. Mutant rodent cell lines sensitive to ultraviolet light, ionizing radiation and cross-linking agents: a comprehensive survey of genetic and biochemical characteristics. Mutat. Res 293, 99-118.
9. D'Andrea, A.D., Grompe, M., 2003. The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 3, 23-34.
10. De Silva, I.U., McHugh, P.J., Clingen, P.H., Hartley, J.A., 2000. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 20, 7980-7990.
11. Digweed, M., Rothe, S., Demuth, I., Scholz, R., Schindler, D., Stumm, M., Grompe, M., Jordan, A., Sperling, K., 2002. Attenuation of the formation of DNA-repair foci containing RAD51 in Fanconi anaemia. Carcinogenesis 23, 1121-1126.
12. Donahue, S.L., Campbell, C., 2002. A DNA double strand break repair defect in Fanconi anemia fibroblasts. J Biol Chem 277, 46243-46247.
13. Dronkert, M.L., Kanaar, R., 2001. Repair of DNA interstrand cross-links. Mutat Res 486, 217-247.
14. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M., D'Andrea, A.D., 2001. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7, 249-262.
15. Godthelp, B.C., Artwert, F., Joenje, H., Zdzienicka, M.Z., 2002. Impaired DNA damage-induced nuclear Rad51 foci formation uniquely characterizes Fanconi anemia group D1. Oncogene 21, 5002-5005.
16. Haaf, T., Golub, E.I., Reddy, G., Radding, C.M.,Ward, D.C., 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.
17. Howlett, N.G., Taniguchi, T., Olson, S., Cox, B., Waisfisz, Q., De Die-Smulders, C., Persky, N., Grompe, M., Joenje, H., Pals, G., Ikeda, H., Fox, E.A., D'Andrea, A.D., 2002. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297, 606-609.
18. Ishida, R., Buchwald, M., 1982. Susceptibility of Fanconi's anemia lymphoblasts to DNA-cross-linking and alkylating agents. Cancer Res 42, 4000-4006.
19. Joenje, H., Patel, K.J., 2001. The emerging genetic and molecular basis of Fanconi anaemia. Nat. Rev. Genet 2, 446-457.
20. Joenje, H., Oostra, A.B., Wijker, M., di Summa, F.M., van Berkel, C.G., Rooimans, M.A., Ebell, W., van Weel, M., Pronk, J.C., Buchwald, M., Arwert, F., 1997. Evidence for at least eight Fanconi anemia genes. Am. J. Hum. Genet 61, 940-944.
21. Jones, N.J., 1994. Genetic analysis of mitomycin C-hypersensitive Chinese hamster cell mutants. Mutagenesis 9, 477-482.
22. Karanjawala, Z.E., Grawunder, U., Hsieh, C.L., Lieber, M.R., 1999. The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts. Curr. Biol 9, 1501-1504.
23. Kraakman-van der Zwet, M., Overkamp, W.J., van Lange, R.E., Essers, J., van Duijn-Goedhart, A., Wiggers, I., Swaminathan, S., van Buul, P.P., Errami, A., Tan, R.T., Jaspers, N.G., Sharan, S.K., Kanaar, R., Zdzienicka, M.Z., 2002. Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol Cell Biol 22, 669-679.
24. Lambert, S., Lopez, B.S., 2000. Characterization of mammalian RAD51 double strand break repair using non-lethal dominant-negative forms. EMBO J 19, 3090-3099.
25. Larminat, F., Cambois, G., Zdzienicka, M.Z., Defais, M., 1998. Lack of correlation between repair of DNA interstrand cross-links and hypersensitivity of hamster cells towards mitomycin C and cisplatin. FEBS Lett 437, 97-100.
26. Larminat, F., Germanier, M., Papouli, E., Defais, M., 2002. Deficiency in BRCA2 leads to increase in non-conservative homologous recombination. Oncogene 21, 5188-5192.
27. 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.
28. Liu, N., Lamerdin, J.E., Tebbs, R.S., Schild, D., Tucker, J.D., Shen, M.R., Brookman, K.W., Siciliano, M.J.,Walter, C.A., Fan,W., Narayana, L.S., Zhou, Z.Q., Adamson, A.W., Sorensen, K.J., Chen, D.J., Jones, N.J., Thompson, L.H., 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.
29. Lundberg, R., Mavinakere, M., Campbell, C., 2001. Deficient DNA end joining activity in extracts from Fanconi anemia fibroblasts. J Biol Chem 276, 9543-9549.
30. Masson, J.Y., Tarsounas, M.C., Stasiak, A.Z., Stasiak, A., Shah, R., McIlwraith, M.J., Benson, F.E.,West, S.C., 2001. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev 15, 3296-3307.
31. Medhurst, A.L., Huber, P.A., Waisfisz, Q., de Winter, J.P., Mathew, C.G., 2001. Direct interactions of the five known Fanconi anaemia proteins suggest a common functional pathway. Hum. Mol. Genet 10, 423-429.
32. Meyn, M.S., 1993. High spontaneous intrachromosomal recombination rates in ataxia-telangiectasia. Science 260, 1327-1330.
33. Moynahan, M.E., Chiu, J.W., Koller, B.H., Jasin, M., 1999. Brca1 controls homology-directed DNA repair. Mol. Cell 4, 511-518.
34. Moynahan, M.E., Pierce, A.J., Jasin, M., 2001. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 7, 263-272.
35. Moynahan, M.E., Cui, T.Y., Jasin, M., 2001. Homology-directed DNA repair, mitomycin-c resistance, and chromosome stability is restored with correction of a BRCA1 mutation. Cancer Res 61, 4842-4850.
36. Papouli, E., Defais, M., Larminat, F., 2002. Overexpression of metallothionein-II sensitizes rodent cells to apoptosis induced by DNA cross-linking agent through inhibition of NF-kappa B activation. J. Biol. Chem 277, 4764-4769.
37. Papouli, E., Lafon, C., Valette, A., Zdzienicka, M.Z., Defais, M., Larminat, F., 2000. Involvement of apoptosis in mitomycin C hypersensitivity of Chinese hamster cell mutants. Biochem. Pharmacol 59, 1101-1107.
38. Pichierri, P., Averbeck, D., Rosselli, F., 2002. DNA cross-link-dependent RAD50/MRE11/NBS1 subnuclear assembly requires the Fanconi anemia C protein. Hum. Mol. Genet 11, 2531-2546.
39. Qiao, F., Moss, A., Kupfer, G.M., 2001. Fanconi anemia proteins localize to chromatin and the nuclear matrix in a DNA damage- and cell cycle-regulated manner. J. Biol. Chem 276, 23391-23396.
40. Richardson, C., Jasin, M., 2000. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol 20, 9068-9075.
41. Rothkamm, K., Kruger, I., Thompson, L.H., Lobrich, M., 2003. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol 23, 5706-5715.
42. Smith, J., Andrau, J.C., Kallenbach, S., Laquerbe, A., Doyen, N., Papadopoulo, D., 1998. Abnormal rearrangements associated with V(D)J recombination in Fanconi anemia. J. Mol. Biol 281, 815-825.
43. Sonoda, E., Sasaki, M.S., Buerstedde, J.M., Bezzubova, O., Shinohara, A., Ogawa, H., Takata, M., Yamaguchi-Iwai, Y., Takeda, S., 1998. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17, 598-608.
44. Takata, M., Sasaki, M.S., Tachiiri, S., Fukushima, T., Sonoda, E., Schild, D., Thompson, L.H., Takeda, S., 2001. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol 21, 2858-2866.
45. Taniguchi, T., Garcia-Higuera, I., Andreassen, P.R., Gregory, R.C., Grompe, M., D'Andrea, A.D., 2002. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 & RAD51. Blood 100, 2414-2420.
46. Thyagarajan, B., Campbell, C., 1997. Elevated homologous recombination activity in fanconi anemia fibroblasts. J Biol Chem 272, 23328-23333.
47. Van Den Bosch, M., Bree, R.T., Lowndes, N.F., 2003. The MRN complex: coordinating and mediating the response to broken chromosomes. EMBO Rep 4, 844-849.
48. Verkaik, N.S., Esveldt-van Lange, R.E., van Heemst, D., Bruggenwirth, H.T., Hoeijmakers, J.H., Zdzienicka, M.Z., van Gent, D.C., 2002. Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells. Eur. J. Immunol 32, 701-709.
49. Yamamoto, K., Ishiai, M., Matsushita, N., Arakawa, H., Lamerdin, J.E., Buerstedde, J.M., Tanimoto, M., Harada, M., Thompson, L.H., Takata, M., 2003. Fanconi anemia FANCG protein in mitigating radiation- and enzyme-induced DNA double-strand breaks by homologous recombination in vertebrate cells. Mol. Cell. Biol 23, 5421-5430.
50. Yu, V.P., Koehler, M., Steinlein, C., Schmid, M., Hanakahi, L.A., van Gool, A.J., West, S.C., Venkitaraman, A.R., 2000. Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev 14, 1400-1406.
51. Zdzienicka, M.Z., Simons, J.W., 1987. Mutagen-sensitive cell lines are obtained with a high frequency in V79 Chinese hamster cells. Mutat Res 178, 235-244.
52. Zdzienicka, M.Z., 1995. Mammalian mutants defective in the response to ionizing radiation-induced DNA damage. Mutat. Res 336, 203-213.
53. Zdzienicka, M.Z., Arwert, F., Neuteboom, I., Rooimans, M., Simons, J.W., 1990. The Chinese hamster V79 cell mutant V-H4 is phenotypically like Fanconi anemia cells. Somat. Cell. Mol. Genet 16, 575-581.