Secondary mutations of BRCA1/2 and drug resistance

Cancer Science

Volumn 102, Issue 4, 2011, Pages 663-669

  Dhillon, Kiranjit K ^a   Swisher, Elizabeth M ^b   Taniguchi, Toshiyasu ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; CARBOPLATIN; CISPLATIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR;

BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER RECURRENCE; CANCER RESISTANCE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; DNA CROSS LINKING; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FANCONI ANEMIA; GENE DELETION; GENE MUTATION; HUMAN; NONHUMAN; OVARY CANCER; OVARY CARCINOMA; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, BRCA1; GENES, BRCA2; HUMANS; MUTATION;

EID: 79952746216     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2010.01840.x     Document Type: Review

References (76)

1. Agarwal R, Kaye SB. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 2003; 3: 502-16.
2. Rabik CA, Dolan ME. Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev 2007; 33: 9-23.
3. Sakai W, Swisher EM, Karlan BY et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 2008; 451: 1116-20.
4. Swisher EM, Sakai W, Karlan BY, Wurz K, Urban N, Taniguchi T. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res 2008; 68: 2581-6.
5. Sakai W, Swisher EM, Jacquemont C et al. Functional restoration of BRCA2 protein by secondary BRCA2 mutations in BRCA2-mutated ovarian carcinoma. Cancer Res 2009; 69: 6381-6.
6. Edwards SL, Brough R, Lord CJ et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature 2008; 451: 1111-5.
7. Evers B, Helleday T, Jonkers J. Targeting homologous recombination repair defects in cancer. Trends Pharmacol Sci 2010; 31: 372-80.
8. Kadouri L, Hubert A, Rotenberg Y et al. Cancer risks in carriers of the BRCA1/2 Ashkenazi founder mutations. J Med Genet 2007; 44: 467-71.
9. Thompson D, Easton DF. Cancer Incidence in BRCA1 Mutation Carriers. J Natl Cancer Inst 2002; 94: 1358-65.
10. King MC, Marks JH, Mandell JB. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 2003; 302: 643-6.
11. Chen S, Parmigiani G. Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol 2007; 25: 1329-33.
12. Neuhausen SL, Marshall CJ. Loss of heterozygosity in familial tumors from three BRCA1-linked kindreds. Cancer Res 1994; 54: 6069-72.
13. Collins N, McManus R, Wooster R et al. Consistent loss of the wild type allele in breast cancers from a family linked to the BRCA2 gene on chromosome 13q12-13. Oncogene 1995; 10: 1673-5.
14. Gudmundsson J, Johannesdottir G, Bergthorsson JT et al. Different tumor types from BRCA2 carriers show wild-type chromosome deletions on 13q12-q13. Cancer Res 1995; 55: 4830-2.
15. Skoulidis F, Cassidy LD, Pisupati V et al. Germline Brca2 heterozygosity promotes Kras(G12D)-driven carcinogenesis in a murine model of familial pancreatic cancer. Cancer Cell 2010; 18: 499-509.
16. Howlett NG, Taniguchi T, Olson S et al. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 2002; 297: 606-9.
17. D'Andrea AD. Susceptibility pathways in Fanconi's anemia and breast cancer. N Engl J Med 2010; 362: 1909-19.
18. Alter BP, Rosenberg PS, Brody LC. Clinical and molecular features associated with biallelic mutations in FANCD1/BRCA2. J Med Genet 2007; 44: 1-9.
19. Moynahan ME, Chiu JW, Koller BH, Jasin M. Brca1 controls homology-directed DNA repair. Mol Cell 1999; 4: 511-8.
20. Moynahan ME, Pierce AJ, Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 2001; 7: 263-72.
21. Yu X, Wu LC, Bowcock AM, Aronheim A, Baer R. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J Biol Chem 1998; 273: 25388-92.
22. Chen L, Nievera CJ, Lee AY, Wu X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 2008; 283: 7713-20.
23. Jensen RB, Carreira A, Kowalczykowski SC. Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 2010; 467: 678-83.
24. Tischkowitz M, Xia B. PALB2/FANCN: recombining cancer and Fanconi anemia. Cancer Res 2010; 70: 7353-9.
25. Murphy CG, Moynahan ME. BRCA gene structure and function in tumor suppression: a repair-centric perspective. Cancer J 2010; 16: 39-47.
26. Yuan SS, Lee SY, Chen G, Song M, Tomlinson GE, Lee EY. BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res 1999; 59: 3547-51.
27. Bhattacharyya A, Ear US, Koller BH, Weichselbaum RR, Bishop DK. 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 2000; 275: 23899-903.
28. Bryant HE, Schultz N, Thomas HD et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005; 434: 913-7.
29. 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.
30. McCabe KM, Olson SB, Moses RE. DNA interstrand crosslink repair in mammalian cells. J Cell Physiol 2009; 220: 569-73.
31. Akkari YM, Bateman RL, Reifsteck CA, Olson SB, Grompe M. DNA replication is required To elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 2000; 20: 8283-9.
32. Sarkar S, Davies AA, Ulrich HD, McHugh PJ. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J 2006; 25: 1285-94.
33. Knipscheer P, Raschle M, Smogorzewska A et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009; 326: 1698-701.
34. Boyd J, Sonoda Y, Federici MG et al. Clinicopathologic features of BRCA-linked and sporadic ovarian cancer. JAMA 2000; 283: 2260-5.
35. Cass I, Baldwin RL, Varkey T, Moslehi R, Narod SA, Karlan BY. Improved survival in women with BRCA-associated ovarian carcinoma. Cancer 2003; 97: 2187-95.
36. Chetrit A, Hirsh-Yechezkel G, Ben-David Y, Lubin F, Friedman E, Sadetzki S. Effect of BRCA1/2 mutations on long-term survival of patients with invasive ovarian cancer: the national Israeli study of ovarian cancer. J Clin Oncol 2008; 26: 20-5.
37. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 2010; 10: 293-301.
38. Fong PC, Boss DS, Yap TA et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009; 361: 123-34.
39. Audeh MW, Carmichael J, Penson RT et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 2010; 376: 245-51.
40. Fong PC, Yap TA, Boss DS et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol 2010; 28: 2512-9.
41. Tutt A, Robson M, Garber JE et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet 2010; 376: 235-44.
42. Rottenberg S, Jaspers JE, Kersbergen A et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci USA 2008; 105: 17079-84.
43. Hirschhorn R. In vivo reversion to normal of inherited mutations in humans. J Med Genet 2003; 40: 721-8.
44. Hamanoue S, Yagasaki H, Tsuruta T et al. Myeloid lineage-selective growth of revertant cells in Fanconi anaemia. Br J Haematol 2006; 132: 630-5.
45. Mankad A, Taniguchi T, Cox B et al. Natural gene therapy in monozygotic twins with Fanconi anemia. Blood 2006; 107: 3084-90.
46. Ikeda H, Matsushita M, Waisfisz Q et al. Genetic reversion in an acute myelogenous leukemia cell line from a Fanconi anemia patient with biallelic mutations in BRCA2. Cancer Res 2003; 63: 2688-94.
47. Wiegant WW, Overmeer RM, Godthelp BC, van Buul PP, Zdzienicka MZ. Chinese hamster cell mutant, V-C8, a model for analysis of Brca2 function. Mutat Res 2006; 600: 79-88.
48. Abbott DW, Freeman ML, Holt JT. Double-strand break repair deficiency and radiation sensitivity in BRCA2 mutant cancer cells. J Natl Cancer Inst 1998; 90: 978-85.
49. Esashi F, Galkin VE, Yu X, Egelman EH, West SC. Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2. Nat Struct Mol Biol 2007; 14: 468-74.
50. Issaeva N, Thomas HD, Djureinovic T et al. 6-thioguanine selectively kills BRCA2-defective tumors and overcomes PARP inhibitor resistance. Cancer Res 2010; 70: 6268-76.
51. Gazdar AF, Kurvari V, Virmani A et al. Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer. Int J Cancer 1998; 78: 766-74.
52. Langdon SP, Lawrie SS, Hay FG et al. Characterization and properties of nine human ovarian adenocarcinoma cell lines. Cancer Res 1988; 48: 6166-72.
53. Evers B, Jonkers J. Mouse models of BRCA1 and BRCA2 deficiency: past lessons, current understanding and future prospects. Oncogene 2006; 25: 5885-97.
54. Mak TW, Hakem A, McPherson JP et al. Brca1 required for T cell lineage development but not TCR loci rearrangement. Nat Immunol 2000; 1: 77-82.
55. Liu X, Holstege H, van der Gulden H et al. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer. Proc Natl Acad Sci USA 2007; 104: 12111-6.
56. Xu X, Wagner KU, Larson D et al. Conditional mutation of Brca1 in mammary epithelial cells results in blunted ductal morphogenesis and tumour formation. Nat Genet 1999; 22: 37-43.
57. Xu X, Qiao W, Linke SP et al. Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Nat Genet 2001; 28: 266-71.
58. Ludwig T, Fisher P, Murty V, Efstratiadis A. Development of mammary adenocarcinomas by tissue-specific knockout of Brca2 in mice. Oncogene 2001; 20: 3937-48.
59. Cheung AM, Hande MP, Jalali F et al. Loss of Brca2 and p53 synergistically promotes genomic instability and deregulation of T-cell apoptosis. Cancer Res 2002; 62: 6194-204.
60. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 2001; 29: 418-25.
61. McAllister KA, Bennett LM, Houle CD et al. Cancer susceptibility of mice with a homozygous deletion in the COOH-terminal domain of the Brca2 gene. Cancer Res 2002; 62: 990-4.
62. Rottenberg S, Nygren AO, Pajic M et al. Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer. Proc Natl Acad Sci USA 2007; 104: 12117-22.
63. Hay T, Matthews JR, Pietzka L et al. Poly(ADP-ribose) polymerase-1 inhibitor treatment regresses autochthonous Brca2/p53-mutant mammary tumors in vivo and delays tumor relapse in combination with carboplatin. Cancer Res 2009; 69: 3850-5.
64. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006; 5: 219-34.
65. Shafee N, Smith CR, Wei S et al. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Cancer Res 2008; 68: 3243-50.
66. 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.
67. Maheswaran S, Sequist LV, Nagrath S et al. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 2008; 359: 366-77.
68. Roche-Lestienne C, Soenen-Cornu V, Grardel-Duflos N et al. Several types of mutations of the Abl gene can be found in chronic myeloid leukemia patients resistant to STI571, and they can pre-exist to the onset of treatment. Blood 2002; 100: 1014-8.
69. McVey M, Lee SE. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet 2008; 24: 529-38.
70. Xie K, Doles J, Hemann MT, Walker GC. Error-prone translesion synthesis mediates acquired chemoresistance. Proc Natl Acad Sci USA 2010; 107: 20792-7.
71. Zhong Q, Chen CF, Chen PL, Lee WH. BRCA1 facilitates microhomology-mediated end joining of DNA double strand breaks. J Biol Chem 2002; 277: 28641-7.
72. Bouwman P, Aly A, Escandell JM et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 2010; 17: 688-95.
73. Bunting SF, Callen E, Wong N et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010; 141: 243-54.
74. Jacquemont C, Taniguchi T. Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res 2007; 67: 7395-405.
75. Deans AJ, Khanna KK, McNees CJ, Mercurio C, Heierhorst J, McArthur GA. Cyclin-dependent kinase 2 functions in normal DNA repair and is a therapeutic target in BRCA1-deficient cancers. Cancer Res 2006; 66: 8219-26.
76. Dungey FA, Caldecott KW, Chalmers AJ. Enhanced radiosensitization of human glioma cells by combining inhibition of poly(ADP-ribose) polymerase with inhibition of heat shock protein 90. Mol Cancer Ther 2009; 8: 2243-54.