Poly (ADP-ribose) polymerase inhibitors: On the horizon of tailored and personalized therapies for epithelial ovarian cancer

Current Opinion in Oncology

Volumn 24, Issue 5, 2012, Pages 564-571

  Ratner, Elena S ^a   Sartorelli, Alan C ^a   Lin, Z Ping ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BRCA; ovarian cancer; overall survival; poly (ADP ribose) polymerase inhibitors; synthetic lethality

Indexed keywords

BEVACIZUMAB; BRCA1 PROTEIN; BRCA2 PROTEIN; CARBOPLATIN; CEDIRANIB; CISPLATIN; CYCLOPHOSPHAMIDE; DOXORUBICIN; GEMCITABINE; INIPARIB; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OLAPARIB; PACLITAXEL; PLACEBO; RUCAPARIB; TEMOZOLOMIDE; TOPOTECAN; TUMOR MARKER; VELIPARIB;

ADVANCED CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RELAPSE; CANCER RESISTANCE; CANCER SURVIVAL; CELL DEATH; DNA CROSS LINKING; DNA REPAIR; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SCREENING; DRUG TARGETING; DRUG TOLERABILITY; EXCISION REPAIR; GENE EXPRESSION PROFILING; GENE MUTATION; HEREDITARY BREAST AND OVARIAN CANCER SYNDROME; MOLECULAR GENETICS; NONHUMAN; OVARY CARCINOMA; OVERALL SURVIVAL; PERSONALIZED MEDICINE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RECOMBINATION REPAIR; RECURRENCE FREE SURVIVAL; RECURRENT CANCER; REVIEW; SINGLE STRANDED DNA BREAK; TREATMENT RESPONSE; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT;

ANIMALS; ENZYME INHIBITORS; FEMALE; HUMANS; INDIVIDUALIZED MEDICINE; MICE; OVARIAN NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84865519032     PISSN: 10408746     EISSN: 1531703X     Source Type: Journal    
DOI: 10.1097/CCO.0b013e3283564230     Document Type: Review

References (61)

1. Jemal A, Siegel R, Xu J, et al. Cancer statistics, 2010. CA Cancer J Clin 2010; 60:277-300.
2. Parmar MK, Ledermann JA, Colombo N, et al. Paclitaxel plus platinum-based chemotherapy versus conventional platinum-based chemotherapy in women with relapsed ovarian cancer: the ICON4/AGO-OVAR-2.2 trial. Lancet 2003; 361:2099-2106.
3. du Bois A, Luck HJ, Meier W, et al. A randomized clinical trial of cisplatin/paclitaxel versus carboplatin/paclitaxel as first-line treatment of ovarian cancer. J Natl Cancer Inst 2003; 95:1320-1329.
4. McGuire WP, Hoskins WJ, Brady MF, et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N Engl J Med 1996; 334:1-6. (Pubitemid 26012496)
5. Piccart MJ, Bertelsen K, James K, et al. Randomized intergroup trial of cisplatin-paclitaxel versus cisplatin-cyclophosphamide in women with advanced epithelial ovarian cancer: three-year results. J Natl Cancer Inst 2000; 92:699-708. (Pubitemid 30365530)
6. Lister-Sharp D, McDonagh MS, Khan KS, et al. A rapid and systematic review of the effectiveness and cost-effectiveness of the taxanes used in the treatment of advanced breast and ovarian cancer. Health Technol Assess 2000; 4:1-113.
7. Cannistra SA. Is there a 'best' choice of second-line agent in the treatment of recurrent, potentially platinum-sensitive ovarian cancer? J Clin Oncol 2002; 20:1158-1160. (Pubitemid 34177418)
8. Gordon AN, Fleagle JT, Guthrie D, et al. Recurrent epithelial ovarian carcinoma: a randomized phase III study of pegylated liposomal doxorubicin versus topotecan. J Clin Oncol 2001; 19:3312-3322. (Pubitemid 32642183)
9. Kaelin WG Jr. The concept of synthetic lethality in the context of anticancer therapy. Nat Rev Cancer 2005; 5:689-698. (Pubitemid 41486362)
10. Arnaudeau C, Lundin C, Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J Mol Biol 2001; 307:1235-1245. (Pubitemid 33027636)
11. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005; 434:917-921. (Pubitemid 40559006)
12. Tutt AN, Lord CJ, McCabe N, et al. Exploiting the DNA repair defect in BRCA mutant cells in the design of new therapeutic strategies for cancer. Cold Spring Harb Symp Quant Biol 2005; 70:139-148. (Pubitemid 44124865)
13. Starita LM, Parvin JD. The multiple nuclear functions of BRCA1: transcription, ubiquitination and DNA repair. Curr Opin Cell Biol 2003; 15:345-350. (Pubitemid 36638654)
14. Chen L, Nievera CJ, Lee AY, et al. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 2008; 283:7713-7720.
15. Yun MH, Hiom K. CtIP-BRCA1 modulates the choice of DNA double-strandbreak repair pathway throughout the cell cycle. Nature 2009; 459:460-463.
16. Sy SM, Huen MS, Chen J. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci USA 2009; 106:7155-7160.
17. Zhang F, Ma J, Wu J, et al. PALB2 links BRCA1 and BRCA2 in the DNAdamage response. Curr Biol 2009; 19:524-529.
18. Holloman WK. Unraveling the mechanism of BRCA2 in homologous recombination. Nat Struct Mol Biol 2011; 18:748-754.
19. Shrivastav M, De Haro LP, Nickoloff JA. Regulation of DNA double-strand break repair pathway choice. Cell Res 2008; 18:134-147.
20. Pennington KP, Swisher EM. Hereditary ovarian cancer: beyond the usual suspects. Gynecol Oncol 2012; 124:347-353.
21. Walsh T, Casadei S, Lee MK, et al. Mutations in 12 genes for inherited ovarian, fallopian tube, and peritoneal carcinoma identified by massively parallel sequencing. Proc Natl Acad Sci USA 2011; 108:18032-18037.
22. Ratner ES, Keane FK, Lindner R, et al. A KRAS variant is a biomarker of poor outcome, platinum chemotherapy resistance and a potential target for therapy in ovarian cancer. Oncogene 2011. [Epub ahead of print] New finding on a Kras variant that serves as a biomarker of poor clinical outcome and a therapeutic target in ovarian cancer.
23. Turner N, Tutt A, Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer 2004; 4:814-819. (Pubitemid 39331153)
24. Baldwin RL, Nemeth E, Tran H, et al. BRCA1 promoter region hypermethylation in ovarian carcinoma: a population-based study. Cancer Res 2000; 60:5329-5333.
25. Catteau A, Harris WH, Xu CF, et al. Methylation of the BRCA1 promoter region in sporadic breast and ovarian cancer: correlation with disease characteristics. Oncogene 1999; 18:1957-1965. (Pubitemid 29150082)
26. Esteller M, Silva JM, Dominguez G, et al. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J Natl Cancer Inst 2000; 92:564-569. (Pubitemid 30212318)
27. Hennessy BT, Timms KM, Carey MS, et al. Somatic mutations in BRCA1 and BRCA2 could expand the number of patients that benefit from poly (ADP ribose) polymerase inhibitors in ovarian cancer. J Clin Oncol 2010; 28:3570-3576.
28. Foster KA, Harrington P, Kerr J, et al. Somatic and germline mutations of the BRCA2 gene in sporadic ovarian cancer. Cancer Res 1996; 56:3622-3625. (Pubitemid 26271999)
29. Hilton JL, Geisler JP, Rathe JA, et al. Inactivation of BRCA1 and BRCA2 in ovarian cancer. J Natl Cancer Inst 2002; 94:1396-1406. (Pubitemid 35154144)
30. Taniguchi T, Tischkowitz M, Ameziane N, et al. Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nat Med 2003; 9:568-574. (Pubitemid 36597103)
31. Olopade OI, Wei M. FANCF methylation contributes to chemoselectivity in ovarian cancer. Cancer Cell 2003; 3:417-420. (Pubitemid 38340287)
32. Hughes-Davies L, Huntsman D, Ruas M, et al. EMSY links the BRCA2 pathway to sporadic breast and ovarian cancer. Cell 2003; 115:523-535. (Pubitemid 37506042)
33. Banerjee S, Kaye S. PARP inhibitors in BRCA gene-mutated ovarian cancer and beyond. Curr Oncol Rep 2011; 13:442-449.
34. Sibghatullah, Husain I, Carlton W, Sancar A. Human nucleotide excision repair in vitro: repair of pyrimidine dimers, psoralen and cisplatin adducts by HeLa cell-free extract. Nucleic Acids Res 1989; 17:4471-4484. (Pubitemid 19165022)
35. Zdraveski ZZ, Mello JA, Marinus MG, et al. Multiple pathways of recombination define cellular responses to cisplatin. Chem Biol 2000; 7:39-50. (Pubitemid 30141924)
36. Lin ZP, Lee Y, Lin F, et al. Reduced level of ribonucleotide reductase R2 subunits increases dependence on homologous recombination repair of cisplatin-induced DNA damage. Mol Pharmacol 2011; 80:1000-1012.
37. Bhattacharyya A, Ear US, Koller BH, et al. 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; 275:23899-23903. (Pubitemid 30624678)
38. Sgagias MK, Wagner KU, Hamik B, et al. Brca1-deficient murine mammary epithelial cells have increased sensitivity to CDDP and MMS. Cell Cycle 2004; 3:1451-1456. (Pubitemid 40310683)
39. Chetrit A, Hirsh-Yechezkel G, Ben-David Y, et al. 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; 26:20-25.
40. Bolton KL, Chenevix-Trench G, Goh C, et al. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA 2012; 307:382-390.
41. Tan DS, Rothermundt C, Thomas K, et al. BRCAness' syndrome in ovarian cancer: a case-control study describing the clinical features and outcome of patients with epithelial ovarian cancer associated with BRCA1 and BRCA2 mutations. J Clin Oncol 2008; 26:5530-5536.
42. McCabe N, Turner NC, Lord CJ, et al. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res 2006; 66:8109-8115. (Pubitemid 44299177)
43. 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; 28:2512-2519.
44. 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; 376:245-251.
45. 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; 361:123-134.
46. Gelmon KA, Tischkowitz M, Mackay H, et al. Olaparib in patients with recurrent high-grade serous or poorly differentiated ovarian carcinoma or triple-negative breast cancer: a phase 2, multicentre, open-label, nonrandomised study. Lancet Oncol 2011; 12:852-861.
47. Ledermann J, Harter P, Gourley C, et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med 2012; 366:1382-1392.
48. Kaye SB, Lubinski J, Matulonis U, et al. Phase II, open-label, randomized, multicenter study comparing the efficacy and safety of olaparib, a poly (ADPribose) polymerase inhibitor, and pegylated liposomal doxorubicin in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer. J Clin Oncol 2012; 30:372-379.
49. 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; 105:17079-17084.
50. 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; 69:3850-3855.
51. Evers B, Drost R, Schut E, et al. Selective inhibition of BRCA2-deficient mammary tumor cell growth by AZD2281 and cisplatin. Clin Cancer Res 2008; 14:3916-3925.
52. Palma JP, Rodriguez LE, Bontcheva-Diaz VD, et al. The PARP inhibitor, ABT-888 potentiates temozolomide: correlation with drug levels and reduction in PARP activity in vivo. Anticancer Res 2008; 28:2625-2635.
53. Donawho CK, Luo Y, Penning TD, et al. ABT-888, an orally active poly(ADP-ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin Cancer Res 2007; 13:2728-2737. (Pubitemid 46795129)
54. Norquist B, Wurz KA, Pennil CC, et al. Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol 2011; 29:3008-3015.
55. 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; 69:6381-6386.
56. Swisher EM, Sakai W, Karlan BY, et al. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res 2008; 68:2581-2586. (Pubitemid 351556255)
57. Sakai W, Swisher EM, Karlan BY, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 2008; 451:1116-1120. (Pubitemid 351317449)
58. Konstantinopoulos PA, Spentzos D, Karlan BY, et al. Gene expression profile of BRCAness that correlates with responsiveness to chemotherapy and with outcome in patients with epithelial ovarian cancer. J Clin Oncol 2010; 28:3555-3561.
59. Kang J, D'Andrea AD, Kozono D. A DNA repair pathway-focused score for prediction of outcomes in ovarian cancer treated with platinum-based chemotherapy. J Natl Cancer Inst 2012; 104:670-681.
60. Mukhopadhyay A, Elattar A, Cerbinskaite A, et al. Development of a functional assay for homologous recombination status in primary cultures of epithelial ovarian tumor and correlation with sensitivity to poly(ADP-ribose) polymerase inhibitors. Clin Cancer Res 2010; 16:2344-2351.
61. Willers H, Taghian AG, Luo CM, et al. Utility of DNA repair protein foci for the detection of putative BRCA1 pathway defects in breast cancer biopsies. Mol Cancer Res 2009; 7:1304-1309.