Cancer genomics guide clinical practice in personalized medicine

Therapie

Volumn 72, Issue 4, 2017, Pages 439-451

  Lehmann Che, Jacqueline ^a,b   Poirot, Brigitte ^a,b   Boyer, Jean Christophe ^c,d   Evrard, Alexandre ^c,e  

^a SAINT LOUIS HOSPITAL   (France)

^b CNRS   (France)

^c DEPARTMENT OF NEUROLOGY   (France)

^d UNIV MONTPELLIER   (France)

^e INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

Author keywords

Personalized medicine; Targeted therapy; Theranostic biomarkers

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; B RAF KINASE; BRACA1 PROTEIN; BRACA2 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; K RAS PROTEIN; KIT PROTENIN; N RAS PROTEIN; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN; RAS PROTEIN; REACTIVE OXYGEN METABOLITE; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ALK GENE; ARTICLE; BRAF GENE; CANCER GENETICS; CLINICAL PRACTICE; EGFR GENE; ERBB2 GENE; GENE FUNCTION; GENE LOSS; GENE MUTATION; GENETIC SCREENING; HUMAN; KIT GENE; MET GENE; NEXT GENERATION SEQUENCING; NONHUMAN; ONCOGENE; ONCOGENE K RAS; ONCOGENE N RAS; PDGFR GENE; PERSONALIZED MEDICINE; PRIORITY JOURNAL; ROS GENE; GENETICS; HIGH THROUGHPUT SEQUENCING; MOLECULARLY TARGETED THERAPY; NEOPLASM; PHARMACOGENETICS;

HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; PHARMACOGENETICS; PRECISION MEDICINE;

EID: 85014085041     PISSN: 00405957     EISSN: 19585578     Source Type: Journal    
DOI: 10.1016/j.therap.2016.09.015     Document Type: Article

References (91)

1. Hanahan, D., Weinberg, R.A., The hallmarks of cancer. Cell 100:1 (2000), 57–70.
2. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144:5 (2011), 646–674.
3. Weinstein, I.B., Cancer. Addiction to oncogenes – the Achilles heal of cancer. Science 297:5578 (2002), 63–64.
4. Pagliarini, R., Shao, W., Sellers, W.R., Oncogene addiction: pathways of therapeutic response, resistance, and road maps toward a cure. EMBO Rep 16:3 (2015), 280–296.
5. Barlesi, F., Mazieres, J., Merlio, J.P., Debieuvre, D., Mosser, J., Lena, H., et al. Routine molecular profiling of patients with advanced non-small-cell lung cancer: results of a 1-year nationwide programme of the French Cooperative Thoracic Intergroup (IFCT). Lancet 387:10026 (2016), 1415–1426.
6. Cheng, F., Su, L., Qian, C., Circulating tumor DNA: a promising biomarker in the liquid biopsy of cancer. Oncotarget 7:30 (2016), 48832–48841, 10.18632/oncotarget.9453.
7. Pietrasz, D., Pécuchet, N., Fabre, E., Blons, H., Chevalier, L., Taly, V., et al. What future for circulating tumor DNA? Current data and prospects in colorectal, non-small cell lung and pancreatic cancers. Bull Cancer 103:1 (2016), 55–65.
8. Sherwood, J.L., Corcoran, C., Brown, H., Sharpe, A.D., Musilova, M., Kohlmann, A., Optimised pre-analytical methods improve KRAS mutation detection in circulating tumour DNA (ctDNA) from patients with non-small cell lung cancer (NSCLC). PLoS One, 11(2), 2016, e0150197.
9. Pohl, G., Shih, IeM., Principle and applications of digital PCR. Expert Rev Mol Diagn 4:1 (2004), 41–47.
10. Basnet, S., Zhang, Z.Y., Liao, W.Q., Li, S.H., Li, P.S., Ge, H.Y., The prognostic value of circulating cell-free DNA in colorectal cancer: a meta-analysis. J Cancer 7:9 (2016), 1105–1113.
11. Ai, B., Liu, H., Huang, Y., Peng, P., Circulating cell-free DNA as a prognostic and predictive biomarker in non-small cell lung cancer. Oncotarget 7:28 (2016), 44583–44595.
12. Ali, M.A., Chronic myeloid leukemia in the era of tyrosine kinase inhibitors: an evolving paradigm of molecularly targeted therapy. Mol Diagn Ther 20:4 (2016), 315–333.
13. O'Brien, S.G., Guilhot, F., Larson, R.A., Gathmann, I., Baccarani, M., Cervantes, F., et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med 348:11 (2003), 994–1004.
14. Akiyama, T., Sudo, C., Ogawara, H., Toyoshima, K., Yamamoto, T., The product of the human c-erbB-2 gene: a 185-kilodalton glycoprotein with tyrosine kinase activity. Science 232:4758 (1986), 1644–1646.
15. Slamon, D.J., Clark, G.M., Wong, S.G., Levin, W.J., Ullrich, A., McGuire, W.L., Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235:4785 (1987), 177–182.
16. Drebin, J.A., Link, V.C., Weinberg, R.A., Greene, M.I., Inhibition of tumor growth by a monoclonal antibody reactive with an oncogene-encoded tumor antigen. Proc Natl Acad Sci U S A 83:23 (1986), 9129–9133.
17. Goldenberg, M.M., Trastuzumab, a recombinant DNA-derived humanized monoclonal antibody, a novel agent for the treatment of metastatic breast cancer. Clin Ther 21:2 (1999), 309–318.
18. Slamon, D.J., Leyland-Jones, B., Shak, S., Fuchs, H., Paton, V., Bajamonde, A., et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344:11 (2001), 783–792.
19. Wolff, A.C., Hammond, M.E., Hicks, D.G., Dowsett, M., McShane, L.M., Allison, K.H., et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol 31:31 (2013), 3997–4013.
20. Jacquemier, J., Spyratos, F., Esterni, B., Mozziconacci, M.J., Antoine, M., Arnould, L., et al. SISH/CISH or qPCR as alternative techniques to FISH for determination of HER2 amplification status on breast tumors core needle biopsies: a multicenter experience based on 840 cases. BMC Cancer, 13, 2013, 351.
21. Bang, Y.J., Van Cutsem, E., Feyereislova, A., Chung, H.C., Shen, L., Sawaki, A., et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 376:9742 (2010), 687–697.
22. Wainberg, Z.A., Anghel, A., Desai, A.J., Ayala, R., Luo, T., Safran, B., et al. Lapatinib, a dual EGFR and HER2 kinase inhibitor, selectively inhibits HER2-amplified human gastric cancer cells and is synergistic with trastuzumab in vitro and in vivo. Clin Cancer Res 16:5 (2010), 1509–1519.
23. Stephens, P., Hunter, C., Bignell, G., Edkins, S., Davies, H., Teague, J., et al. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature 431:7008 (2004), 525–526.
24. Garrido-Castro, A.C., Felip, E., HER2 driven non-small cell lung cancer (NSCLC): potential therapeutic approaches. Transl Lung Cancer Res 2:2 (2013), 122–127.
25. Li, C., Sun, Y., Fang, R., Han, X., Luo, X., Wang, R., et al. Lung adenocarcinomas with HER2-activating mutations are associated with distinct clinical features and HER2/EGFR copy number gains. J Thorac Oncol 7:1 (2012), 85–89.
26. Wang, S.E., Narasanna, A., Perez-Torres, M., Xiang, B., Wu, F.Y., et al. HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 10:1 (2006), 25–38.
27. Han, S.W., Kim, T.Y., Jeon, Y.K., Hwang, P.G., Im, S.A., Lee, K.H., et al. Optimization of patient selection for gefitinib in non-small cell lung cancer by combined analysis of epidermal growth factor receptor mutation, K-ras mutation, and Akt phosphorylation. Clin Cancer Res 12:8 (2006), 2538–2544.
28. Tomizawa, K., Suda, K., Onozato, R., Kosaka, T., Endoh, H., Sekido, Y., et al. Prognostic and predictive implications of HER2/ERBB2/neu gene mutations in lung cancers. Lung Cancer 74:1 (2011), 139–144.
29. Paez, J.G., Jänne, P.A., Lee, J.C., Tracy, S., Greulich, H., Gabriel, S., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304:5676 (2004), 1497–1500.
30. Sharma, S.V., Bell, D.W., Settleman, J., Haber, D.A., Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 7:3 (2007), 169–181.
31. Mok, T.S., Wu, Y.L., Thongprasert, S., Yang, C.H., Chu, D.T., Saijo, N., et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 361:10 (2009), 947–957.
32. Rosell, R., Carcereny, E., Gervais, R., Vergnenegre, A., Massuti, B., Felip, E., et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol 13:3 (2012), 239–246.
33. Yu, H.A., Arcila, M.E., Rekhtman, N., Sima, C.S., Zakowski, M.F., Pao, W., et al. Analysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-mutant lung cancers. Clin Cancer Res 19:8 (2013), 2240–2247.
34. Yun, C.H., Mengwasser, K.E., Toms, A.V., Woo, M.S., Greulich, H., Wong, K.K., et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci U S A 105:6 (2008), 2070–2075.
35. Chong, C.R., Janne, P.A., The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med 19:11 (2013), 1389–1400.
36. Soda, M., Choi, Y.L., Enomoto, M., Takada, S., Yamashita, Y., Ishikawa, S., et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 448:7153 (2007), 561–566.
37. Soda, M., Takada, S., Takeuchi, K., Choi, Y.L., Enomoto, M., Ueno, T., et al. A mouse model for EML4-ALK-positive lung cancer. Proc Natl Acad Sci U S A 105:50 (2008), 19893–19897.
38. Soda, M., Isobe, K., Inoue, A., Maemondo, M., Oizumi, S., Fujita, Y., et al. A prospective PCR-based screening for the EML4-ALK oncogene in non-small cell lung cancer. Clin Cancer Res 18:20 (2012), 5682–5689.
39. Kwak, E.L., Bang, Y.J., Camidge, D.R., Shaw, A.T., Solomon, B., Maki, R.G., et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 363:18 (2010), 1693–1703.
40. Camidge, D.R., Bang, Y.J., Kwak, E.L., Iafrate, A.J., Varella-Garcia, M., Fox, S.B., et al. Activity and safety of crizotinib in patients with ALK-positive non-small-cell lung cancer: updated results from a phase 1 study. Lancet Oncol 13:10 (2012), 1011–1019.
41. Choi, Y.L., Soda, M., Yamashita, Y., Ueno, T., Takashima, J., Nakajima, T., et al. EML4-ALK mutations in lung cancer that confer resistance to ALK inhibitors. N Engl J Med 363:18 (2010), 1734–1739.
42. Friboulet, L., Li, N., Katayama, R., Lee, C.C., Gainor, J.F., Crystal, A.S., et al. The ALK inhibitor ceritinib overcomes crizotinib resistance in non-small cell lung cancer. Cancer Discov 4:6 (2014), 662–673.
43. Paik, P.K., Drilon, A., Fan, P.D., Yu, H., Rekhtman, N., Ginsberg, M.S., et al. Response to MET inhibitors in patients with stage IV lung adenocarcinomas harboring MET mutations causing exon 14 skipping. Cancer Discov 5:8 (2015), 842–849.
44. Frampton, G.M., Ali, S.M., Rosenzweig, M., Chmielecki, J., Lu, X., Bauer, T.M., et al. Activation of MET via diverse exon 14 splicing alterations occurs in multiple tumor types and confers clinical sensitivity to MET inhibitors. Cancer Discov 5:8 (2015), 850–859.
45. Liu, X., Jia, Y., Stoopler, M.B., Shen, Y., Cheng, H., Chen, J., et al. Next-generation sequencing of pulmonary sarcomatoid carcinoma reveals high frequency of actionable MET gene mutations. J Clin Oncol 34:8 (2016), 794–802.
46. Jenkins, R.W., Oxnard, G.R., Elkin, S., Sullivan, E.K., Carter, J.L., Barbie, D.A., Response to crizotinib in a patient with lung adenocarcinoma harboring a MET splice site mutation. Clin Lung Cancer 16:5 (2015), e101–e104.
47. Acquaviva, J., Wong, R., Charest, A., The multifaceted roles of the receptor tyrosine kinase ROS in development and cancer. Biochim Biophys Acta 1795:1 (2009), 37–52.
48. Shaw, A.T., Ou, S.H., Bang, Y.J., Camidge, D.R., Solomon, B.J., Salgia, R., et al. Crizotinib in ROS1-rearranged non-small-cell lung cancer. N Engl J Med 371:21 (2014), 1963–1971.
49. Mazières, J., Zalcman, G., Crinò, L., Biondani, P., Barlesi, F., Filleron, T., et al. Crizotinib therapy for advanced lung adenocarcinoma and a ROS1 rearrangement: results from the EUROS1 cohort. J Clin Oncol 33:9 (2015), 992–999.
50. McCubrey, J.A., Steelman, L.S., Chappell, W.H., Abrams, S.L., Wong, E.W., Chang, F., et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 1773:8 (2007), 1263–1284.
51. Fearon, E.R., Molecular genetics of colorectal cancer. Annu Rev Pathol 6 (2011), 479–507.
52. Lièvre, A., Bachet, J.B., Le Corre, D., Boige, V., Landi, B., Emile, J.F., et al. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res 66:8 (2006), 3992–3995.
53. Peeters, M., Douillard, J.Y., Van Cutsem, E., Siena, S., Zhang, K., Williams, R., et al. Mutant KRAS codon 12 and 13 alleles in patients with metastatic colorectal cancer: assessment as prognostic and predictive biomarkers of response to panitumumab. J Clin Oncol 31:6 (2013), 759–765.
54. Peeters, M., Karthaus, M., Rivera, F., Terwey, J.H., Douillard, J.Y., Panitumumab in metastatic colorectal cancer: the importance of tumour RAS status. Drugs 75:7 (2015), 731–748.
55. Misale, S., Yaeger, R., Hobor, S., Scala, E., Janakiraman, M., Liska, D., et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 486:7404 (2012), 532–536.
56. Rapp, U.R., Goldsborough, M.D., Mark, G.E., Bonner, T.I., Groffen, J., Reynolds, F.H. Jr., et al. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. Proc Natl Acad Sci U S A 80:14 (1983), 4218–4222.
57. Davies, H., Bignell, G.R., Cox, C., Stephens, P., Edkins, S., Clegg, S., et al. Mutations of the BRAF gene in human cancer. Nature 417:6892 (2002), 949–954.
58. Bollag, G., Tsai, J., Zhang, J., Zhang, C., Ibrahim, P., Nolop, K., et al. Vemurafenib: the first drug approved for BRAF-mutant cancer. Nat Rev Drug Discov 11:11 (2012), 873–886.
59. Tsai, J., Lee, J.T., Wang, W., Zhang, J., Cho, H., Mamo, S., et al. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci U S A 105:8 (2008), 3041–3046.
60. Solit, D.B., Garraway, L.A., Pratilas, C.A., Sawai, A., Getz, G., Basso, A., et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 439:7074 (2006), 358–362.
61. Cox, A.D., Der, C.J., The raf inhibitor paradox: unexpected consequences of targeted drugs. Cancer Cell 17:3 (2010), 221–223.
62. Prahallad, A., Sun, C., Huang, S., Di Nicolantonio, F., Salazar, R., Zecchin, D., et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 483:7387 (2012), 100–103.
63. Galván-Banqueri, M., Ubago-Pérez, R., Molina-López, T., The relative clinical efficacy of trametinib–dabrafenib and cobimetinib–vemurafenib in advanced melanoma: an indirect comparison. J Clin Pharm Ther 41:3 (2016), 285–289.
64. Harlé, A., Salleron, J., Franczak, C., Dubois, C., Filhine-Tressarieu, P., Leroux, A., et al. Detection of BRAF mutations using a fully automated platform and comparison with high resolution melting, real-time allele specific amplification, immunohistochemistry and next generation sequencing assays, for patients with metastatic melanoma. PLoS One, 11(4), 2016, e0153576.
65. Carter, J., Tseng, L.H., Zheng, G., Dudley, J., Illei, P., Gocke, C.D., et al. Non-p.V600E BRAF mutations are common using a more sensitive and broad detection tool. Am J Clin Pathol 144:4 (2015), 620–628.
66. Hanks, S.K., Quinn, A.M., Hunter, T., The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:4861 (1988), 42–52.
67. Rubin, B.P., Singer, S., Tsao, C., Duensing, A., Lux, M.L., Ruiz, R., et al. KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res 61:22 (2001), 8118–8121.
68. Hirota, S., Isozaki, K., Moriyama, Y., Hashimoto, K., Nishida, T., Ishiguro, S., et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279:5350 (1998), 577–580.
69. Miettinen, M., Lasota, J., Gastrointestinal stromal tumors: review on morphology, molecular pathology, prognosis, and differential diagnosis. Arch Pathol Lab Med 130:10 (2006), 1466–1478.
70. Heinrich, M.C., Corless, C.L., Duensing, A., McGreevey, L., Chen, C.J., Joseph, N., et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299:5607 (2003), 708–710.
71. Duensing, A., Medeiros, F., McConarty, B., Joseph, N.E., Panigrahy, D., Singer, S., et al. Mechanisms of oncogenic KIT signal transduction in primary gastrointestinal stromal tumors (GISTs). Oncogene 23:22 (2004), 3999–4006.
72. Corless, C.L., Gastrointestinal stromal tumors: what do we know now?. Mod Pathol 27:Suppl. 1 (2014), S1–S16.
73. Lasota, J., Miettinen, M., Clinical significance of oncogenic KIT and PDGFRA mutations in gastrointestinal stromal tumours. Histopathology 53:3 (2008), 245–266.
74. Verweij, J., van Oosterom, A., Blay, J.Y., Judson, I., Rodenhuis, S., van der Graaf, W., et al. Imatinib mesylate (STI-571 Glivec Gleevec) is an active agent for gastrointestinal stromal tumours, but does not yield responses in other soft-tissue sarcomas that are unselected for a molecular target. Results from an EORTC Soft Tissue and Bone Sarcoma Group phase II study. Eur J Cancer 39:14 (2003), 2006–2011.
75. Demetri, G.D., von Mehren, M., Blanke, C.D., Van den Abbeele, A.D., Eisenberg, B., Roberts, P.J., et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 347:7 (2002), 472–480.
76. van Oosterom, A.T., Judson, I., Verweij, J., Stroobants, S., Donato di Paola, E., Dimitrijevic, S., et al. Safety and efficacy of imatinib (STI571) in metastatic gastrointestinal stromal tumours: a phase I study. Lancet 358:9291 (2001), 1421–1423.
77. Debiec-Rychter, M., Dumez, H., Judson, I., Wasag, B., Verweij, J., Brown, M., et al. Use of c-KIT/PDGFRA mutational analysis to predict the clinical response to imatinib in patients with advanced gastrointestinal stromal tumours entered on phase I and II studies of the EORTC Soft Tissue and Bone Sarcoma Group. Eur J Cancer 40:5 (2004), 689–695.
78. Debiec-Rychter, M., Sciot, R., Le Cesne, A., Schlemmer, M., Hohenberger, P., van Oosterom, A.T., et al. KIT mutations and dose selection for imatinib in patients with advanced gastrointestinal stromal tumours. Eur J Cancer 42:8 (2006), 1093–1103.
79. Demetri, G.D., van Oosterom, A.T., Garrett, C.R., Blackstein, M.E., Shah, M.H., Verweij, J., et al. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 368:9544 (2006), 1329–1338.
80. Wu, L., Zhang, Z., Yao, H., Liu, K., Wen, Y., Xiong, L., Clinical efficacy of second-generation tyrosine kinase inhibitors in imatinib-resistant gastrointestinal stromal tumors: a meta-analysis of recent clinical trials. Drug Des Devel Ther 8 (2014), 2061–2067.
81. Caestecker, K.W., Van de Walle, G.R., The role of BRCA1 in DNA double-strand repair: past and present. Exp Cell Res 319:5 (2013), 575–587.
82. Hartwell, L.H., Szankasi, P., Roberts, C.J., Murray, A.W., Friend, S.H., Integrating genetic approaches into the discovery of anticancer drugs. Science 278:5340 (1997), 1064–1068.
83. Kaelin, W.G. Jr., The concept of synthetic lethality in the context of anticancer therapy. Nat Rev Cancer 5:9 (2005), 689–698.
84. Bryant, H.E., Schultz, N., Thomas, H.D., Parker, K.M., Flower, D., Lopez, E., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434:7035 (2005), 913–917.
85. Farmer, H., McCabe, N., Lord, C.J., Tutt, A.N., Johnson, D.A., Richardson, T.B., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434:7035 (2005), 917–921.
86. Fong, P.C., Boss, D.S., Yap, T.A., Tutt, A., Wu, P., Mergui-Roelvink, M., et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361:2 (2009), 123–134.
87. Fong, P.C., Yap, T.A., Boss, D.S., Carden, C.P., Mergui-Roelvink, M., Gourley, C., et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol 28:15 (2010), 2512–2519.
88. Ledermann, J., Harter, P., Gourley, C., Friedlander, M., Vergote, I., Rustin, G., et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med 366:15 (2012), 1382–1392.
89. Dizdar, O., Arslan, C., Altundag, K., Altundag, advances in PARP inhibitors for the treatment of breast cancer. Expert Opin Pharmacother 16:18 (2015), 2751–2758.
90. Konstantinopoulos, P.A., Ceccaldi, R., Shapiro, G.I., D'Andrea, A.D., Homologous recombination deficiency: exploiting the fundamental vulnerability of ovarian cancer. Cancer Discov 5:11 (2015), 1137–1154.
91. INCa 2016. http://www.e-cancer.fr/Professionnels-de-la-recherche/Recherche-clinique/Le-programme-AcSe/L-essentiel [accessed 20 January 2017].