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Review

The Emerging Role of Tyrosine Kinase Inhibitors in Ovarian Cancer Treatment: A Systematic Review

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Pages 313-339 | Received 26 Mar 2016, Accepted 22 Jun 2016, Published online: 03 Aug 2016

References

  • Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015;136(5):E359–E386.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015;65(1):5–29.
  • Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 2013;49(6):1374–1403.
  • Prat J. New insights into ovarian cancer pathology. Ann Oncol 2012;23(Suppl 10):x111–x117.
  • Ricciardelli C, Oehler MK. Diverse molecular pathways in ovarian cancer and their clinical significance. Maturitas 2009;62(3):270–275.
  • Sopik V, Iqbal J, Rosen B, Narod SA. Why have ovarian cancer mortality rates declined? Part I. Incidence. Gynecol Oncol 2015a;138(3, Sep):741–749.
  • Sopik V, Rosen B, Giannakeas V, Narod SA. Why have ovarian cancer mortality rates declined? Part III. Prospects for the future. Gynecol Oncol 2015b;138(3):757–61.
  • World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Report. Food N, Physical Activity, and the Prevention of Ovarian Cancer 2014. Available from http://www.dietandcancerreport.org/cup/cup_resources.php
  • Colombo N, Peiretti M, Parma G, Lapresa M, Mancari R, Carinelli S, et al. Newly diagnosed and relapsed epithelial ovarian carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010;21(Suppl 5):v23–v30.
  • National_Comprehensive_Cancer_Network. Epithelial Ovarian Cancer (Including Fallopian Tube Cancer and Primary Peritoneal Cancer), version 3.2012. Fort Washington, PA: NCCN; 2012.
  • Jayson GC, Kohn EC, Kitchener HC, Ledermann JA. Ovarian cancer. Lancet 2014;384(9951):1376–1388.
  • Lheureux S, Karakasis K, Kohn EC, Oza AM. Ovarian cancer treatment: the end of empiricism? Cancer 2015;121(18):3203–3211..
  • Schmid BC, Oehler MK. New perspectives in ovarian cancer treatment. Maturitas 2014;77(2):128–136.
  • Jackson AL, Eisenhauer EL, Herzog TJ. Emerging therapies: angiogenesis inhibitors for ovarian cancer. Expert Opin Emerg Drugs 2015;20(2):331–346.
  • Morotti M, Becker CM, Menada MV, Ferrero S. Targeting tyrosine-kinases in ovarian cancer. Expert Opin Investig Drugs 2013;22(10):1265–1279.
  • Vergoulidou M. More than a decade of tyrosine kinase inhibitors in the treatment of solid tumors: what we have learned and what the future holds. Biomark Insights 2015;10(Suppl 3):33–40.
  • Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6(7):e1000097.
  • Masoumi Moghaddam S, Amini A, Morris DL, Pourgholami MH. Significance of vascular endothelial growth factor in growth and peritoneal dissemination of ovarian cancer. Cancer Metastasis Rev 2012;31(1–2):143–162.
  • Gomez-Raposo C, Mendiola M, Barriuso J, Casado E, Hardisson D, Redondo A. Angiogenesis and ovarian cancer. Clin Transl Oncol 2009;11(9):564–571.
  • Hui G, Meng M. Prognostic value of vascular endothelial growth factor expression in women with ovarian cancer: a meta-analysis. J BUON 2015;20(3):870–878.
  • du Bois A, Kristensen G, Ray Coquard I, Reuss A, Pignata S, Colombo N EA. AGO-OVAR 12: a randomized placebo-controlled GCIG/ENGOTintergroup phase III trial of standard frontline chemotherapy+/− nintedanib for advanced ovarian cancer. Int J Gynaecol Cancer 2013;2013:23.
  • Ledermann JA, Hackshaw A, Kaye S, Jayson G, Gabra H, McneishI, 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):3798–3804.
  • Buckanovich RJ, Berger R, Sella A, Sikic BI, Shen X, Ramies DA, et al. Activity of cabozantinib (XL184) in advanced ovarian cancer patients: results from a phase 2 randomized discontinuation trial (RDT). J Clin Oncol 2011;29:2011 ( suppl; abstr 5008).
  • Hirte H, Lheureux S, Fleming GF, Sugimoto A, Morgan R, Biagi J, et al. A phase 2 study of cediranib in recurrent or persistent ovarian, peritoneal or fallopian tube cancer: a trial of the Princess Margaret, Chicago and California phase II consortia. Gynecol Oncol 2015;138(1):55–61.
  • 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):5601–5606.
  • Ledermann J, Perren TJ, Raja Fa, Embleton A, Rustin GJS, Al JGE. Randomised double-blind phase III trial of cediranib (AZD 2171) in relapsed platinum sensitive ovarian cancer: results of the ICON6 trial. Amsterdam: European Cancer Congress (ECCO-ESMOESTRO); 2013.
  • Liu JF, Barry WT, Birrer M, Lee JM, Buckanovich RJ, FlemingGF, 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):1207–1214.
  • Schilder RJ, Sill MW, Lankes HA, Gold MA, Mannel RS, Modesitt SC, et al. A phase II evaluation of motesanib (AMG 706) in the treatment of persistent or recurrent ovarian, fallopian tube and primary peritoneal carcinomas: a Gynecologic Oncology Group study. Gynecol Oncol 2013;129(1):86–91.
  • Bodnar L, Gornas M, Szczylik C. Sorafenib as a third line therapy in patients with epithelial ovarian cancer or primary peritoneal cancer: a phase II study. Gynecol Oncol 2011;123(1):33–36.
  • Herzog TJ, Scambia G, Kim BG, Lhomme C, MarkowskaJ, Ray-CoquardI, et al.A randomized phase II trial of maintenance therapy with Sorafenib in front-line ovarian carcinoma. Gynecol Oncol 2013;130(1):25–30.
  • Kohn EC, Lee J, Annunziata CM, Minasian LM, Zujewski J, Prindiville SA, et al. A phase II study of intermittent sorafenib with bevacizumab in bevacizumab-naïve epithelial ovarian cancer (EOC) patients. J. Clin. Oncol. 2011;29 [Abstract 5019].
  • Matei D, Sill MW, Lankes HA, Degeest K, Bristow RE, Mutch D, et al. Activity of sorafenib in recurrent ovarian cancer and primary peritoneal carcinomatosis: a gynecologic oncology group trial. J Clin Oncol 2011;29(1):69–75.
  • Pölcher M, Eckhardt M, Coch C, WolfgartenM, KublerK, HartmannG, et al. Sorafenib in combination with carboplatin and paclitaxel as neoadjuvant chemotherapy in patients with advanced ovarian cancer. Cancer Chemother Pharmacol 2010;66(1):203–207.
  • Ramasubbaiah R, Perkins SM, Schilder J, Whalen C, Johnson CS, Callahan M, et al. Sorafenib in combination with weekly topotecan in recurrent ovarian cancer, a phase I/II study of the Hoosier Oncology Group. Gynecol Oncol 2011;123(3):499–504.
  • Welch SA, Hirte HW, Elit L, Schilder RJ, Wang L, MacalpineK, et al. Sorafenib in combination with gemcitabine in recurrent epithelial ovarian cancer: a study of the Princess Margaret Hospital Phase II Consortium. Int J Gynecol Cancer 2010;20(5):787–793.
  • 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):2265–2271.
  • Biagi JJ, Oza AM, Chalchal HI, Grimshaw R, Ellard SL, Lee U, et al. A phase II study of sunitinib in patients with recurrent epithelial ovarian and primary peritoneal carcinoma: an NCIC Clinical Trials Group Study. Ann Oncol 2011;22(2):335–340.
  • Campos SM, Penson RT, Matulonis U, Horowitz NS, Whalen C, PereiraL, et al. A phase II trial of Sunitinib malate in recurrent and refractory ovarian, fallopian tube and peritoneal carcinoma. Gynecol Oncol 2013;128(2):215–220.
  • 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):3374–3382.
  • Friedlander M, Hancock KC, Rischin D, Messing MJ, Stringer CA, Matthys GM et al. A phase II, open-label study evaluating pazopanib in patients with recurrent ovarian cancer. Gynecol Oncol 2010;119(1):32–37.
  • Pignata S, Lorusso D, Scambia G, Sambataro D, Tamberi S, Cinieri S et al. Pazopanib plus weekly paclitaxel versus weekly paclitaxel alone for platinum-resistant or platinum-refractory advanced ovarian cancer (MITO 11): a randomised, open-label, phase 2 trial. Lancet Oncol 2015;16(5):561–568.
  • Annunziata CM, Walker AJ, Minasian L, Yu M, Kotz H, Wood BJ et al. Vandetanib, designed to inhibit VEGFR2 and EGFR signaling, had no clinical activity as monotherapy for recurrent ovarian cancer and no detectable modulation of VEGFR2. Clin Cancer Res 2010;16(2):664–672.
  • Coleman RL, Moon J, Sood AK, Hu W, Delmore JE, Bonebrake AJ et al. Randomised phase II study of docetaxel plus vandetanib versus docetaxel followed by vandetanib in patients with persistent or recurrent epithelial ovarian, fallopian tube or primary peritoneal carcinoma: SWOG S0904. Eur J Cancer 2014;50(9):1638–1648.
  • Sahade M, Caparelli F, Hoff PM. Cediranib: a VEGF receptor tyrosine kinase inhibitor. Future Oncol 2012;8(7):775–781.
  • Roth GJ, Binder R, Colbatzky F, Dallinger C, Schlenker-Herceg R, Hilberg F et al. Nintedanib: from discovery to the clinic. J Med Chem 2015;58(3):1053–1063.
  • Davidson BA, Secord AA. Profile of pazopanib and its potential in the treatment of epithelial ovarian cancer. Int J Womens Health 2014;6:289–300.
  • Jovelet C, Benard J, Forestier F, Farinotti R, Bidart JM, Gil S. Inhibition of P-glycoprotein functionality by vandetanib may reverse cancer cell resistance to doxorubicin. Eur J Pharm Sci 2012;46(5):484–491.
  • Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001;2(2):127–137.
  • Ciardiello F. Epidermal growth factor receptor inhibitors in cancer treatment. Future Oncol 2005;1(2):221–234.
  • Gui T, Shen K. The epidermal growth factor receptor as a therapeutic target in epithelial ovarian cancer. Cancer Epidemiol 2012;36(5):490–496.
  • Sheng Q, Liu J. The therapeutic potential of targeting the EGFR family in epithelial ovarian cancer. Br J Cancer 2011;104(8):1241–1245.
  • Campos S, Hamid O, Seiden MV, Oza A, Plante M, Potkul RK et al. Multicenter, randomized phase II trial of oral CI-1033 for previously treated advanced ovarian cancer. J Clin Oncol 2005;23(24):5597–5604.
  • Blank SV, Christos P, Curtin JP, Goldman N, Runowicz CD, Sparano JA et al. Erlotinib added to carboplatin and paclitaxel as first-line treatment of ovarian cancer: a phase II study based on surgical reassessment. Gynecol Oncol 2010;119(3):451–456.
  • Chambers SK, Clouser MC, Baker AF, Roe DJ, Cui H, Brewer MA et al. Overexpression of tumor vascular endothelial growth factor A may portend an increased likelihood of progression in a phase II trial of bevacizumab and erlotinib in resistant ovarian cancer. Clin Cancer Res 2010;16(21):5320–5328.
  • Gordon AN, Finkler N, Edwards RP, Garcia AA, Crozier M, Irwin DH et al. Efficacy and safety of erlotinib HCl, an epidermal growth factor receptor (HER1/EGFR) tyrosine kinase inhibitor in patients with advanced ovarian carcinoma: results from a phase II multicenter study. Int J Gynecol Cancer 2005;15(5):785–792.
  • Hirte H, Oza A, Swenerton K, Ellard SL, Grimshaw R, Fisher B, et al. A phase II study of erlotinib (OSI-774) given in combination with carboplatin in patients with recurrent epithelial ovarian cancer (NCIC CTG IND.149). Gynecol Oncol 2010;118(3):308–312.
  • Nimeiri HS, Oza AM, Morgan RJ, Friberg G, Kasza K, Faoro L, et al. Efficacy and safety of bevacizumab plus erlotinib for patients with recurrent ovarian, primary peritoneal, and fallopian tube cancer: a trial of the Chicago, PMH, and California Phase II Consortia. Gynecol Oncol 2008;110(1):49–55.
  • Vergote IB, Jimeno A, Joly F, Katsaros D, Coens C, Despierre E, et al. Randomized phase III study of erlotinib versus observation in patients with no evidence of disease progression after first-line platin-based chemotherapy for ovarian carcinoma: a European Organisation for Research and Treatment of Cancer-Gynaecological Cancer Group, and Gynecologic Cancer Intergroup study. J Clin Oncol 2014;32(4):320–326.
  • Pautier P, Joly F, Kerbrat P, Bougnoux P, Fumoleau P, Petit T, et al. Phase II study of gefitinib in combination with paclitaxel (P) and carboplatin (C) as second-line therapy for ovarian, tubal or peritoneal adenocarcinoma (1839IL/0074). Gynecol Oncol 2010;116(2):157–162.
  • Posadas EM, Liel MS, Kwitkowski V, Minasian L, Godwin AK, Hussain MM, et al. A phase II and pharmacodynamic study of gefitinib in patients with refractory or recurrent epithelial ovarian cancer. Cancer 2007;109(7):1323–1330.
  • Schilder RJ, Sill MW, Chen X, Darcy KM, Decesare SL, Lewandowski G, et al. Phase II study of gefitinib in patients with relapsed or persistent ovarian or primary peritoneal carcinoma and evaluation of epidermal growth factor receptor mutations and immunohistochemical expression: a Gynecologic Oncology Group study. Clin Cancer Res 2005;11(15):5539–5548.
  • Wagner U, Du Bois A, Pfisterer J, Huober J, Loibl S, Luck HJ, et al. Gefitinib in combination with tamoxifen in patients with ovarian cancer refractory or resistant to platinum-taxane based therapy—a phase II trial of the AGO Ovarian Cancer Study Group (AGO-OVAR 2.6). Gynecol Oncol 2007;105(1):132–137.
  • Garcia AA, Sill MW, Lankes HA, Godwin AK, Mannel RS, Armstrong DK, et al. A phase II evaluation of lapatinib in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a gynecologic oncology group study. Gynecol Oncol 2012;124(3):569–574.
  • Lheureux S, Krieger S, Weber B, Pautier P, Fabbro M, Selle F, et al. Expected benefits of topotecan combined with lapatinib in recurrent ovarian cancer according to biological profile: a phase 2 trial. Int J Gynecol Cancer 2012;22(9):1483–1488.
  • Rivkin SE, Muller C, Iriarte D, Arthur J, Canoy A, Reid H. Phase I/II lapatinib plus carboplatin and paclitaxel in stage III or IV relapsed ovarian cancer patients. J Clin Oncol 2008;26(15S(May 20 supplement)):5556.
  • Weroha SJ, Oberg AL, Ziegler KL, Dakhilm SR, Rowland KM, Hartmann LC, et al. Phase II trial of lapatinib and topotecan (LapTop) in patients with platinum-refractory/resistant ovarian and primary peritoneal carcinoma. Gynecol Oncol 2011;122(1):116–120.
  • Hellberg C, Ostman A, Heldin CH. PDGF and vessel maturation. Recent Results Cancer Res 2010;180:103–114.
  • Matsuo K, Nishimura M, Komurov K, Shahzad MM, Ali-Fehmi R, Roh JW, et al. Platelet-derived growth factor receptor alpha (PDGFRalpha) targeting and relevant biomarkers in ovarian carcinoma. Gynecol Oncol 2014;132(1):166–175.
  • Alberts DS, Liu PY, Wilczynski SP, Jang A, Moon J, Ward JH, et al. Phase II trial of imatinib mesylate in recurrent, biomarker positive, ovarian cancer (Southwest Oncology Group Protocol S0211). Int J Gynecol Cancer 2007;17(4):784–788.
  • Matei D, Emerson RE, Schilder J, Menning N, Baldridge LA, Johnson CS, et al. Imatinib mesylate in combination with docetaxel for the treatment of patients with advanced, platinum-resistant ovarian cancer and primary peritoneal carcinomatosis : a Hoosier Oncology Group trial. Cancer 2008;113(4):723–732.
  • Noguera IR, Sun CC, Broaddus RR, Branham D, Levenback CF, Ramirez PT, et al. Phase II trial of imatinib mesylate in patients with recurrent platinum- and taxane-resistant low-grade serous carcinoma of the ovary, peritoneum, or fallopian tube. Gynecol Oncol 2012;125(3):640–645.
  • 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):3243–3247.
  • Schilder RJ, Sill MW, Lee RB, Shaw TJ, Senterman MK, Klein-Szanto AJ, et al. Phase II evaluation of imatinib mesylate in the treatment of recurrent or persistent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. J Clin Oncol 2008;26(20):3418–3425.
  • Puls LN, Eadens M, Messersmith W. Current status of SRC inhibitors in solid tumor malignancies. Oncologist 2011;16(5):566–578.
  • Wiener JR, Windham TC, Estrella VC, Parikh NU, Thall PF, Deavers MT, et al. Activated SRC protein tyrosine kinase is overexpressed in late-stage human ovarian cancers. Gynecol Oncol 2003;88(1):73–79.
  • Schilder RJ, Brady WE, Lankes HA, Fiorica JV, Shahin MS, Zhou XC, et al. Phase II evaluation of dasatinib in the treatment of recurrent or persistent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol 2012;127(1):70–74.
  • Mcneish IA, Ledermann JA, Webber L, James L, Kaye SB, Hall M, et al. A randomised, placebo-controlled trial of weekly paclitaxel and saracatinib (AZD0530) in platinum-resistant ovarian, fallopian tube or primary peritoneal cancerdagger. Ann Oncol 2014;25(10):1988–1995.
  • Yap TA, Carden CP, Kaye SB. Beyond chemotherapy: targeted therapies in ovarian cancer. Nat Rev Cancer 2009;9(3):167–181.
  • Yap TA, Sandhu SK, Workman P, De Bono JS. Envisioning the future of early anticancer drug development. Nat Rev Cancer 2010;10(7):514–523.
  • Gasparri ML, Savone D, Besharat RA, Farooqi AA, Bellati F, Ruscito I, et al. Circulating tumor cells as trigger to hematogenous spreads and potential biomarkers to predict the prognosis in ovarian cancer. Tumour Biol 2016;37(1):71–75. doi:10.1007/s13277-015-4299-9
  • Lheureux S, Oza AM. Targeting the microenvironment in ovarian cancer. Lancet Oncol 2015;16(5):485–486.
  • Jackson A, Davenport S, Herzog T, Coleman R. Targeting angiogenesis: vascular endothelial growth factor and related signaling pathways. Transl Cancer Res 2015;4(1):70–83.
  • Damaraju VL, Kuzma M, Mowles D, Cass CE, Sawyer MB. Interactions of multitargeted kinase inhibitors and nucleoside drugs: Achilles heel of combination therapy? Mol Cancer Ther 2015;14(1):236–245.
  • Stone RL, Sood AK, Coleman RL. Collateral damage: toxic effects of targeted antiangiogenic therapies in ovarian cancer. Lancet Oncol 2010;11(5):465–475.

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