Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition

Cancer Research

Volumn 66, Issue 16, 2006, Pages 8109-8115

  McCabe, Nuala ^a   Turner, Nicholas C ^a   Lord, Christopher J ^a   Kluzek, Katarzyna ^b   Białkowska, Aneta ^b   Swift, Sally ^a   Giavara, Sabrina ^c   O'Connor, Mark J ^c   Tutt, Andrew N ^a   Zdzienicka, Małgorzata Z ^b,d   Smith, Graeme C M ^c   Ashworth, Alan ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b NICOLAUS COPERNICUS UNIVERSITY   (Poland)

^c KuDOS Pharmaceuticals Ltd   (United Kingdom)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PROTEIN; ATM PROTEIN; ATR PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; EXORIBONUCLEASE; FANCONI ANEMIA PROTEIN A; FANCONI ANEMIA PROTEIN C; FANCONI ANEMIA PROTEIN D2; NIBRIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN DELETED IN SPLIT HAND SPLIT FOOT SYNDROME 1; RAD51 PROTEIN; RAD54 PROTEIN; REPLICATION PROTEIN A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME INHIBITION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SENSITIVITY ANALYSIS;

ANIMALS; BRCA1 PROTEIN; BRCA2 PROTEIN; DNA DAMAGE; DNA REPAIR; EMBRYO; ENZYME INHIBITORS; FLUOROBENZENES; MICE; MICE, KNOCKOUT; PHTHALAZINES; POLY(ADP-RIBOSE) POLYMERASES; RECOMBINATION, GENETIC; STEM CELLS;

EID: 33748065304     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-0140     Document Type: Article

References (48)

1. Turner N, Tutt A, Ashworth A. Targeting the DNA repair defect of BRCA tumours. Curr Opin Pharmacol 2005;5:388-93.
2. Venkitaraman AR. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 2002;108:171-82.
3. Moynahan ME, Pierce AJ, Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 2001;7:263-72.
4. Moynahan ME, Chiu JW, Koller BH, Jasin M. Brca1 controls homology-directed DNA repair. Mol Cell 1999;4: 511-8.
5. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol 2004; 24:9305-16.
6. Tutt A, Bertwistle D, Valentine J, et al. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J 2001;20:4704-16.
7. Brody LC. Treating cancer by targeting a weakness. N Engl J Med 2005;353:949-50.
8. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917-21.
9. Gallmeier E, Kern SE. Absence of specific cell killing of the BRCA2-deficient human cancer cell line CAPAN1 by poly(ADP-ribose) polymerase inhibition. Cancer Biol Ther 2005;4:703-6.
10. McCabe N, Lord CJ, Tutt AN, Martin NM, Smith GC, Ashworth A. BRCA2-deficient CAPAN-1 cells are extremely sensitive to the inhibition of poly (ADP-ribose) polymerase: an issue of potency. Cancer Biol Ther 2005; 4:934-6.
11. Schultz N, Lopez E, Saleh-Gohari N, Helleday T. Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res 2003;31:4959-64.
12. Hickson I, Zhao Y, Richardson CJ, et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004;64:9152-9.
13. Cerosaletti KM, Desai-Mehta A, Yeo TC, Kraakman-van Der Zwet M, Zdzienicka MZ, Concannon P. Retroviral expression of the NBS1 gene in cultured Nijmegen breakage syndrome cells restores normal radiation sensitivity and nuclear focus formation. Mutagenesis 2000;15:281-6.
14. Kraakman-van der Zwet M, Overkamp WJ, Friedl AA, et al. Immortalization and characterization of Nijmegen Breakage syndrome fibroblasts. Mutat Res 1999; 434:17-27.
15. Kraakman-van der Zwet M, Overkamp WJ, Jaspers NG, Natarajan AT, Lohman PH, Zdzienicka MZ. Complementation of chromosomal aberrations in AT/NBS hybrids: inadequacy of RDS as an endpoint in complementation studies with immortal NBS cells. Mutat Res 2001;485:177-85.
16. Gudmundsdottir K, Lord CJ, Witt E, Tutt AN, Ashworth A. DSS1 is required for RAD51 focus formation and genomic stability in mammalian cells. EMBO Rep 2004;5:989-93.
17. Sorensen CS, Hansen LT, Dziegielewski J, et al. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 2005;7:195-201.
18. Li J, Zou C, Bai Y, Wazer DE, Band V, Gao Q. DSS1 is required for the stability of BRCA2. Oncogene 2006;25: 1186-94.
19. Wang Y, Putnam CD, Kane MF, et al. Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability, and cancer in mice. Nat Genet 2005;37:750-5.
20. Mazin AV, Alexeev AA, Kowalczykowski SC. A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J Biol Chem 2003;278: 14029-36.
21. Essers J, Hendriks RW, Swagemakers SM, et al. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 1997;89: 195-204.
22. Morrison C, Sonoda E, Takao N, Shinohara A, Yamamoto K, Takeda S. The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J 2000;19:463-71.
23. Wang H, Wang H, Powell SN, Iliakis G, Wang Y. ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonhomologous end joining. Cancer Res 2004;64: 7139-43.
24. Sarkaria JN, Busby EC, Tibbetts RS, et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 1999;59: 4375-82.
25. Zhang J, Willers H, Feng Z, et al. Chk2 phosphorylation of BRCA1 regulates DNA double-strand break repair. Mol Cell Biol 2004;24:708-18.
26. Stiff T, Reis C, Alderton GK, Woodbine L, O'Driscoll M, Jeggo PA. Nbs1 is required for ATR-dependent phosphorylation events. EMBO J 2005;24:199-208.
27. Tauchi H, Kobayashi J, Morishima K, et al. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 2002;420:93-8.
28. Wang X, D'Andrea AD. The interplay of Fanconi anemia proteins in the DNA damage response. DNA Repair (Amst) 2004;3:1063-9.
29. Venkitaraman AR. Tracing the network connecting BRCA and Fanconi anaemia proteins. Nat Rev Cancer 2004;4:266-76.
30. Garcia-Higuera I, Taniguchi T, Ganesan S, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 2001;7:249-62.
31. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, D'Andrea AD. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 2002;100:2414-20.
32. Hussain S, Wilson JB, Medhurst AL, et al. Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum Mol Genet 2004;13:1241-8.
33. Wang H, Powell SN, Iliakis G, Wang Y. ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonhomologous end joining. Cancer Res 2004;64:7139-43.
34. Nakanishi K, Yang YG, Pierce AJ, et al. Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc Natl Acad Sci U S A 2005; 102:1110-5.
35. Yamamoto K, Ishiai M, Matsushita N, et al. Fanconi anemia FANCG protein in mitigating radiation- and enzyme-induced DNA double-strand breaks by homologous recombination in vertebrate cells. Mol Cell Biol 2003;23:5421-30.
36. Yamamoto K, Hirano S, Ishiai M, et al. Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination. Mol Cell Biol 2005;25:34-43.
37. Niedzwiedz W, Mosedale G, Johnson M, Ong CY, Pace P, Patel KJ. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 2004;15:607-20.
38. Kraakman-van der Zwet M, Overkamp WJ, van Lange RE, et al. Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol Cell Biol 2002; 22:669-79.
39. Tan TL, Essers J, Citterio E, et al. Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Curr Biol 1999;9:325-8.
40. Godthelp BC, Wiegant WW, Waisfisz Q, et al. Inducibility of nuclear Rad51 foci after DNA damage distinguishes all Fanconi anemia complementation groups from D1/BRCA2. Mutat Res 2006;594:39-48.
41. Turner N, Tutt A, Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer 2004;4:814-9.
42. Bullrich F, Rasio D, Kitada S, et al. ATM mutations in B-cell chronic lymphocytic leukemia. Cancer Res 1999; 59:24-7.
43. Vorechovsky I, Luo L, Ortmann E, Steinmann D, Dork T. Missense mutations at ATM gene and cancer risk. Lancet 1999;353:1276.
44. Swift M, Morrell D, Massey RB, Chase CL. Incidence of cancer in 161 families affected by ataxia-telangiectasia. N Engl J Med 1991;325:1831-6.
45. Bell DW, Varley JM, Szydlo TE, et al. Heterozygous germ line HCHK2 mutations in Li-Fraumeni syndrome. Science 1999;286:2528-31.
46. Miller CW, Ikezoe T, Krug U, et al. Mutations of the CHK2 gene are found in some osteosarcomas, but are rare in breast, lung, and ovarian tumors. Genes Chromosomes Cancer 2002;33:17-21.
47. Marsit CJ, Liu M, Nelson HH, Posner M, Suzuki M, Kelsey KT. Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene 2004;23:1000-4.
48. Narayan G, Arias-Pulido H, Nandula SV, et al. Promoter hypermethylation of FANCF: disruption of Fanconi anemia-BRCA pathway in cervical cancer. Cancer Res 2004;64:2994-7.