Ovarian cancer molecular stratification and tumor heterogeneity: A necessity and a challenge

Frontiers in Oncology

Volumn 5, Issue OCT, 2015, Pages

  Symeonides, Stefan ^a   Gourley, Charlie ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Bevacizumab; Heterogeneity; Olaparib; Ovarian cancer; Stratification

Indexed keywords

AFLIBERCEPT; ANGIOPOIETIN RECEPTOR; BEVACIZUMAB; BRCA1 PROTEIN; BRCA2 PROTEIN; CA 125 ANTIGEN; CEDIRANIB; IMATINIB; MESOTHELIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NINTEDANIB; NIRAPARIB; OLAPARIB; PAZOPANIB; RUCAPARIB; SORAFENIB; SUNITINIB; TALAZOPARIB; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 3; VELIPARIB;

ANTIANGIOGENIC THERAPY; CANCER CHEMOTHERAPY; CELL HETEROGENEITY; GENE MUTATION; GENETIC HETEROGENEITY; GERMLINE MUTATION; HOMOLOGOUS RECOMBINATION; HUMAN; MOLECULARLY TARGETED THERAPY; MONOTHERAPY; NOTE; OUTCOME ASSESSMENT; OVARY CANCER; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROGRESSION FREE SURVIVAL; SOMATIC MUTATION; STRATIFICATION;

EID: 84947075829     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2015.00229     Document Type: Note

References (47)

1. Burger RA, Brady MF, Bookman MA, Fleming GF, Monk BJ, Huang H, et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med (2011) 365(26):2473-83. doi: 10.1056/NEJMoa1104390
2. Perren TJ, Swart AM, Pfisterer J, Ledermann JA, Pujade-Lauraine E, Kristensen G, et al. A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med (2011) 365(26):2484-96. doi:10.1056/NEJMoa1103799
3. Aghajanian C, Blank SV, Goff BA, Judson PL, Teneriello MG, Husain A, et al. OCEANS: a randomized, double-blind, placebo-controlled phase III trial of chemotherapy with or without bevacizumab in patients with platinum-sensitive recurrent epithelial ovarian, primary peritoneal, or fallopian tube cancer. J Clin Oncol (2012) 30(17):2039-45. doi:10.1200/JCO.2012.42.0505
4. Pujade-Lauraine E, Hilpert F, Weber B, Reuss A, Poveda A, Kristensen G, et al. Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: the AURELIA open-label randomized phase III trial. J Clin Oncol (2014) 32(13):1302-8. doi:10.1200/JCO.2013.51.4489
5. Monk BJ, Pujade-Lauraine E, Burger RA. Integrating bevacizumab into the management of epithelial ovarian cancer: the controversy of front-line versus recurrent disease. Ann Oncol (2013) 24(Suppl 10):x53-8. doi:10.1093/annonc/mdt472
6. du Bois A, Floquet A, Kim JW, Rau J, del Campo JM, Friedlander M, et al. Incorporation of pazopanib in maintenance therapy of ovarian cancer. J Clin Oncol (2014) 32(30):3374-82. doi:10.1200/JCO.2014.55.7348
7. Matulonis UA, Berlin S, Ivy P, Tyburski K, Krasner C, Zarwan C, et al. Cediranib, an oral inhibitor of vascular endothelial growth factor receptor kinases, is an active drug in recurrent epithelial ovarian, fallopian tube, and peritoneal cancer. J Clin Oncol (2009) 27(33):5601-6. doi:10.1200/JCO.2009.23.2777
8. Ledermann JA, Hackshaw A, Kaye S, Jayson G, Gabra H, McNeish I, et al. Randomized phase II placebo-controlled trial of maintenance therapy using the oral triple angiokinase inhibitor BIBF 1120 after chemotherapy for relapsed ovarian cancer. J Clin Oncol (2011) 29(28):3798-804. doi:10.1200/JCO.2010.33.5208
9. Coleman RL, Duska LR, Ramirez PT, Heymach JV, Kamat AA, Modesitt SC, et al. Phase 1-2 study of docetaxel plus aflibercept in patients with recurrent ovarian, primary peritoneal, or fallopian tube cancer. Lancet Oncol (2011) 12(12):1109-17. doi:10.1016/S1470-2045(11)70244-3
10. Karlan BY, Oza AM, Richardson GE, Provencher DM, Hansen VL, Buck M, et al. Randomized, double-blind, placebo-controlled phase II study of AMG 386 combined with weekly paclitaxel in patients with recurrent ovarian cancer. J Clin Oncol (2012) 30(4):362-71. doi:10.1200/JCO.2010.34.3178
11. Baumann KH, du Bois A, Meier W, Rau J, Wimberger P, Sehouli J, et al. A phase II trial (AGO 2.11) in platinum-resistant ovarian cancer: a randomized multicenter trial with sunitinib (SU11248) to evaluate dosage, schedule, tolerability, toxicity and effectiveness of a multitargeted receptor tyrosine kinase inhibitor monotherapy. Ann Oncol (2012) 23(9):2265-71. doi:10.1093/annonc/mds003
12. Hainsworth JD, Thompson DS, Bismayer JA, Gian VG, Merritt WM, Whorf RC, et al. Paclitaxel/carboplatin with or without sorafenib in the first-line treatment of patients with stage III/IV epithelial ovarian cancer: a randomized phase II study of the Sarah Cannon Research Institute. Cancer Med (2015) 4(5):673-81. doi:10.1002/cam4.376
13. Safra T, Andreopoulou E, Levinson B, Borgato L, Pothuri B, Blank S, et al. Weekly paclitaxel with intermittent imatinib mesylate (Gleevec): tolerance and activity in recurrent epithelial ovarian cancer. Anticancer Res (2010) 30(9):3243-7.
14. Lambrechts D, Lenz HJ, de Haas S, Carmeliet P, Scherer SJ. Markers of response for the antiangiogenic agent bevacizumab. J Clin Oncol (2013) 31(9):1219-30. doi:10.1200/JCO.2012.46.2762
15. Backen A, Renehan AG, Clamp AR, Berzuini C, Zhou C, Oza A, et al. The combination of circulating Ang1 and Tie2 levels predicts progression-free survival advantage in bevacizumab-treated patients with ovarian cancer. Clin Cancer Res (2014) 20(17):4549-58. doi:10.1158/1078-0432.CCR-13-3248
16. Jayson GC, de Haas S, Delmar P, Miles DW, Shah MA, Van Cutsem E, et al. Evaluation of plasma VEGFA as a potential predictive pan-tumour biomarker for bevacizumab. Eur J Cancer (2011) 47(Suppl 1):S96. doi:10.1016/S0959-8049(11)70641-4
17. Collinson F, Hutchinson M, Craven RA, Cairns DA, Zougman A, Wind TC, et al. Predicting response to bevacizumab in ovarian cancer: a panel of potential biomarkers informing treatment selection. Clin Cancer Res (2013) 19(18):5227-39. doi:10.1158/1078-0432.CCR-13-0489
18. Gourley C, McCavigan A, Perren T, Paul J, Michie CO, Churchman M, et al. Molecular subgroup of high-grade serous ovarian cancer (HGSOC) as a predictor of outcome following bevacizumab. J Clin Oncol (2014) 32(5s):abstr 5502.
19. Burger RA, Sill MW, Monk BJ, Greer BE, Sorosky JI. Phase II trial of bevacizumab in persistent or recurrent epithelial ovarian cancer or primary peritoneal cancer: a Gynecologic Oncology Group Study. J Clin Oncol (2007) 25(33):5165-71. doi:10.1200/JCO.2007.11.5345
20. Cannistra SA, Matulonis UA, Penson RT, Hambleton J, Dupont J, Mackey H, et al. Phase II study of bevacizumab in patients with platinum-resistant ovarian cancer or peritoneal serous cancer. J Clin Oncol (2007) 25(33):5180-6. doi:10.1200/JCO.2007.12.0782
21. Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol (2014) 15(8):852-61. doi:10.1016/S1470-2045(14)70228-1
22. 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 (2012) 366(15):1382-92. doi:10.1056/NEJMoa1105535
23. Ihnen M, zu Eulenburg C, Kolarova T, Qi JW, Manivong K, Chalukya M, et al. Therapeutic potential of the poly(ADP-ribose) polymerase inhibitor rucaparib for the treatment of sporadic human ovarian cancer. Mol Cancer Ther (2013) 12(6):1002-15. doi:10.1158/1535-7163.MCT-12-0813
24. Jones P, Wilcoxen K, Rowley M, Toniatti C. Niraparib: a Poly(ADP-ribose) polymerase (PARP) inhibitor for the treatment of tumors with defective homologous recombination. J Med Chem (2015) 58(8):3302-14. doi:10.1021/jm5018237
25. Coleman RL, Sill M, Aghajanian C, Gray HJ, Tewari KS, Rubin SC, et al. A phase II evaluation of the potent, highly selective PARP inhibitor veliparib in the treatment of persistent or recurrent epithelial ovarian, fallopian tube, or primary peritoneal cancer in patients who carry a germline BRCA1 or BRCA2 mutation-a Gynecologic Oncology Group study. Gynecol Oncol (2014) 133(s1):56. doi:10.1016/j.ygyno.2015.03.042
26. Roche H, Blum J, Eiermann W, Im YH, Martin M, Mina L, et al. P1.01A phase 3 study of the oral PARP inhibitor talazoparib (BMN 673) in BRCA mutation subjects with advanced breast cancer (EMBRACA). Ann Oncol (2015) 26(Suppl 2):ii16. doi:10.1093/annonc/mdv090.1
27. Fong PC, Boss DS, Yap TA, 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 (2009) 361(2):123-34. doi:10.1056/NEJMoa0900212
28. Fong PC, Yap TA, Boss DS, Carden CP, 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 (2010) 28(15):2512-9. doi:10.1200/JCO.2009.26.9589
29. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, 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(9737):245-51. doi:10.1016/S0140-6736(10)60893-8
30. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature (2011) 474(7353):609-15. doi:10.1038/nature10166
31. Tan DS, Rothermundt C, Thomas K, Bancroft E, Eeles R, Shanley S, 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(34):5530-6. doi:10.1200/JCO.2008.16.1703
32. Yang D, Khan S, Sun Y, Hess K, Shmulevich I, Sood AK, et al. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. JAMA (2011) 306(14):1557-65. doi:10.1001/jama.2011.1456
33. Carser JE, Quinn JE, Michie CO, O'Brien EJ, McCluggage WG, Maxwell P, et al. BRCA1 is both a prognostic and predictive biomarker of response to chemotherapy in sporadic epithelial ovarian cancer. Gynecol Oncol (2011) 123(3):492-8. doi:10.1016/j.ygyno.2011.08.017
34. Hennessy BT, Timms KM, Carey MS, Gutin A, Meyer LA, Flake DD II, 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(22):3570-6. doi:10.1200/JCO.2009.27.2997
35. Press JZ, De Luca A, Boyd N, Young S, Troussard A, Ridge Y, et al. Ovarian carcinomas with genetic and epigenetic BRCA1 loss have distinct molecular abnormalities. BMC Cancer (2008) 8:17. doi:10.1186/1471-2407-8-17
36. Bowtell DD. The genesis and evolution of high-grade serous ovarian cancer. Nat Rev Cancer (2010) 10(11):803-8. doi:10.1038/nrc2946
37. Gourley C, Michie CO, Roxburgh P, Yap TA, Harden S, Paul J, et al. Increased incidence of visceral metastases in Scottish patients with BRCA1/2-defective ovarian cancer: an extension of the ovarian BRCAness phenotype. J Clin Oncol (2010) 28(15):2505-11. doi:10.1200/JCO.2009.25.1082
38. Bolton KL, Chenevix-Trench G, Goh C, Sadetzki S, Ramus SJ, Karlan BY, et al. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA (2012) 307(4):382-90. doi:10.1001/jama.2012.20
39. Candido-dos-Reis FJ, Song H, Goode EL, Cunningham JM, Fridley BL, Larson MC, et al. Germline mutation in BRCA1 or BRCA2 and ten-year survival for women diagnosed with epithelial ovarian cancer. Clin Cancer Res (2015) 21(3):652-7. doi:10.1158/1078-0432.CCR-14-2497
40. Zeller C, Dai W, Steele NL, Siddiq A, Walley AJ, Wilhelm-Benartzi CS, et al. Candidate DNA methylation drivers of acquired cisplatin resistance in ovarian cancer identified by methylome and expression profiling. Oncogene (2012) 31(42):4567-76. doi:10.1038/onc.2011.611
41. Sakai W, Swisher EM, Jacquemont C, Chandramohan KV, Couch FJ, Langdon SP, et al. Functional restoration of BRCA2 protein by secondary BRCA2 mutations in BRCA2-mutated ovarian carcinoma. Cancer Res (2009) 69(16):6381-6. doi:10.1158/0008-5472.CAN-09-1178
42. Edwards SL, Brough R, Lord CJ, Natrajan R, Vatcheva R, Levine DA, et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature (2008) 451(7182):1111-5. doi:10.1038/nature06548
43. 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(8):2581-6. doi:10.1158/0008-5472.CAN-08-0088
44. Norquist B, Wurz KA, Pennil CC, Garcia R, Gross J, Sakai W, et al. Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol (2011) 29(22):3008-15. doi:10.1200/JCO.2010.34.2980
45. Sakai W, Swisher EM, Karlan BY, Agarwal MK, Higgins J, Friedman C, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature (2008) 451(7182):1116-20. doi:10.1038/nature06633
46. Lheureux S, Ledermann JA, Kaye SB, Gourley C, Friedlander M, Bowtell D, et al. Characterization of ovarian cancer long-term responders on olaparib. J Clin Oncol (2014) 32(5s):abstr 5534.
47. Liu JF, Barry WT, Birrer M, Lee JM, Buckanovich RJ, Fleming GF, et al. Combination cediranib and olaparib versus olaparib alone for women with recurrent platinum-sensitive ovarian cancer: a randomised phase 2 study. Lancet Oncol (2014) 15(11):1207-14. doi:10.1016/S1470-2045(14)70391-2