Clinical outcome of treatment with serine-threonine kinase inhibitors in recurrent epithelial ovarian cancer: a systematic review of literature

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65(1):5–29.
   PubMed Web of Science ®Google Scholar
• Herzog TJ, Pothuri B. Ovarian cancer: a focus on management of recurrent disease. Nat Clin Prac Oncol. 2006;3(11):604–611.
   PubMedGoogle Scholar
• Matsuo K, Lin YG, Roman LD, et al. Overcoming platinum resistance in ovarian carcinoma. Expert Opin Investig Drugs. 2010;19(11):1339–1354.
   PubMed Web of Science ®Google Scholar
• Dancey J. mTOR signaling and drug development in cancer. Nat Rev Clin Oncol. 2010;7:209–219.
   PubMed Web of Science ®Google Scholar
• Faivre S, Kroemer G, Raymond E. Current development of mTOR inhibitors as anticancer agents. Nat Rev Drug Discov. 2006;5(8):671–688.
   PubMed Web of Science ®Google Scholar
• Ducat D, Zheng Y. Aurora kinases in spindle assembly and chromosome segregation. Exp Cell Res. 2004;301(1):60–67.
   PubMed Web of Science ®Google Scholar
• Capra M, Nuciforo PG, Confalonieri S, et al. Frequent alterations in the expression of serine/threonine kinases in human cancers. Cancer Res. 2006;66(16):8147–8154.
   PubMed Web of Science ®Google Scholar
• Liaw D, Marsh DJ, Li J, et al. Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat Genet. 1997;16(1):64–67.
   PubMed Web of Science ®Google Scholar
• Dinulescu DM, Ince TA, Quade BJ, et al. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med. 2005;11(1):63–70.
   PubMed Web of Science ®Google Scholar
• Hemminki A, Tomlisnson I, Markie D, et al. Localization of a susceptibility locus for Peutz-Jeghers syndrome to 19p using comparative genomic hybridization and targeted linkage analysis. Nat Genet. 1997;15(1):87–90.
   PubMed Web of Science ®Google Scholar
• Jenne DE, Reimann H, Nezu J, et al. Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat Genet. 1998;18(1):38–43.
   PubMed Web of Science ®Google Scholar
• Connolly DC, Katabuchi H, Cliby WA, et al. Somatic mutations in the STK11/LKB1 gene are uncommon in rare gynecological tumor types associated with Peutz-Jegher’s syndrome. Am J Pathol. 2000;156(1):339–345.
   PubMed Web of Science ®Google Scholar
• Altomare DA, Wang HQ, Skele KL, et al. AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene. 2004;23(34):5853–5857.
   PubMed Web of Science ®Google Scholar
• Mabuchi S, Sasano T, Kawano M, et al. Targeting mTOR Signaling in Ovarian Cancer. Curr Obstet Gynecol Rep. 2015;4(1):11–17.
   Google Scholar
• Pallet N, Legendre C. Adverse events associated with mTOR inhibitors. Expert Opin Drug Saf. 2013;12(2):177–186.
   PubMed Web of Science ®Google Scholar
• Robinson MJ, Cobb MH. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol. 1997;9(2):180–186.
   PubMed Web of Science ®Google Scholar
• Burotto M, Chiou VL, Lee J-M, et al. The MAPK pathway across different malignancies: a new perspective. Cancer. 2014;120(22):3446–3456.
   PubMed Web of Science ®Google Scholar
• Singer G, Oldt R, Cohen Y, et al. Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst. 2003;95(6):484–486.
   PubMed Web of Science ®Google Scholar
• Long GV, Stroyakovskiy D, Gogas H, et al. Dabrafenib and trametinib versus dabrafenib and placebo for Val600 BRAF-mutant melanoma: a multicentre, double-blind, phase 3 randomised controlled trial. Lancet. 2015;386(9992):444–451.
   PubMed Web of Science ®Google Scholar
• Miller CR, Oliver KE, Farley JH. MEK1/2 inhibitors in the treatment of gynecologic malignancies. Gynecol Oncol. 2014;133(1):128–137.
   PubMed Web of Science ®Google Scholar
• Wang D, Boerner SA, Winkler JD, et al. Clinical experience of MEK inhibitors in cancer therapy. Biochim Biophys Acta (BBA) Mol Cell Res. 2007;1773(8):1248–1255.
   PubMed Web of Science ®Google Scholar
• Malumbres M, Pérez de Castro I. Aurora kinase A inhibitors: promising agents in antitumoral therapy. Expert Opin Ther Targets. 2014;18(12):1377–1393.
   PubMed Web of Science ®Google Scholar
• Landen CN, Lin YG, Immaneni A, et al. Overexpression of the centrosomal protein aurora-a kinase is associated with poor prognosis in epithelial ovarian cancer patients. Clin Cancer Res. 2007;13(14):4098–4104.
   PubMed Web of Science ®Google Scholar
• Green MR, Woolery JE, Mahadevan D. Update on aurora kinase targeted therapeutics in oncology. Expert Opin Drug Discov. 2011;6(3):291–307.
   PubMed Web of Science ®Google Scholar
• Fu S, Hu W, Kavanagh JJ, et al. Targeting aurora kinases in ovarian cancer. Expert Opin Ther Targets. 2006;10(1):77–85.
   PubMed Web of Science ®Google Scholar
• Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA. 2000;283(15):2008–2012.
   PubMed Web of Science ®Google Scholar
• Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009 Jan;45(2):228–247.
   PubMed Web of Science ®Google Scholar
• Common Terminology Criteria for Adverse Events (CTCAE) Guidelines. National Cancer Institute. 2015. [cited 2015 Dec 8]. Available from: http://ctep.cancer.gov/protocolDevelopment/electronic_applications/ctc.htm#ctc_40
   Google Scholar
• Falchook GS, Long GV, Kurzrock R, et al. Dabrafenib in patients with melanoma, untreated brain metastases, and other solid tumours: a phase 1 dose-escalation trial. Lancet. 2012;379(9829):1893–1901.
   PubMed Web of Science ®Google Scholar
• Welch SA, Hirte HW, Elit L, 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.
   PubMed Web of Science ®Google Scholar
• Schwandt A, von Gruenigen VE, Wenham RM, et al. Randomized phase II trial of sorafenib alone or in combination with carboplatin/paclitaxel in women with recurrent platinum sensitive epithelial ovarian, peritoneal, or fallopian tube cancer. Invest New Drugs. 2014;32(4):729–738.
   PubMed Web of Science ®Google Scholar
• Bedard PL, Tabernero J, Janku F, et al. A phase Ib dose-escalation study of the oral pan-PI3K inhibitor buparlisib (BKM120) in combination with the oral MEK1/2 inhibitor trametinib (GSK1120212) in patients with selected advanced solid tumors. Clin Cancer Res. 2015;21(4):730–738.
   PubMed Web of Science ®Google Scholar
• Diamond JR, Bastos BR, Hansen RJ, et al. Phase I safety, pharmacokinetic, and pharmacodynamic study of ENMD-2076, a novel angiogenic and aurora kinase inhibitor, in patients with advanced solid tumors. Clin Cancer Res. 2011;17(4):849–860.
   PubMed Web of Science ®Google Scholar
• Farley J, Brady WE, Vathipadiekal V, et al. Selumetinib in women with recurrent low-grade serous carcinoma of the ovary or peritoneum: an open-label, single-arm, phase 2 study. Lancet Oncol. 2013;14(2):134–140.
   PubMed Web of Science ®Google Scholar
• Ganesan P, Piha-Paul S, Naing A, et al. Phase I clinical trial of lenalidomide in combination with sorafenib in patients with advanced cancer. Invest New Drugs. 2014;32(2):279–286.
   PubMed Web of Science ®Google Scholar
• Lee JM, Sarosy GA, Annunziata CM, et al. Combination therapy: intermittent sorafenib with bevacizumab yields activity and decreased toxicity. Br J Cancer. 2010;102(3):495–499.
   PubMed Web of Science ®Google Scholar
• Matulonis UA, Sharma S, Ghamande S, et al. Phase II study of MLN8237 (alisertib), an investigational aurora A kinase inhibitor, in patients with platinum-resistant or -refractory epithelial ovarian, fallopian tube, or primary peritoneal carcinoma. Gynecol Oncol. 2012;127(1):63–69.
   PubMed Web of Science ®Google Scholar
• Ramasubbaiah R, Perkins SM, Schilder J, 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.
   PubMed Web of Science ®Google Scholar
• Brana I, Berger R, Golan T, et al. A parallel-arm phase I trial of the humanised anti-IGF-1R antibody dalotuzumab in combination with the AKT inhibitor MK-2206, the mTOR inhibitor ridaforolimus, or the NOTCH inhibitor MK-0752, in patients with advanced solid tumours. Br J Cancer. 2014;111(10):1932–1944.
   PubMed Web of Science ®Google Scholar
• Wheler JJ, Moulder SL, Naing A, et al. Anastrozole and everolimus in advanced gynecologic and breast malignancies: activity and molecular alterations in the PI3K/AKT/mTOR pathway. Oncotarget. 2014;5(10):3029–3038.
   PubMed Web of Science ®Google Scholar
• Matei D, Sill MW, Lankes HA, 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Oza AM, Elit L, Swenerton K, et al. Phase II study of CGP 69846A (ISIS 5132) in recurrent epithelial ovarian cancer: an NCIC clinical trials group study (NCIC IND.116). Gynecol Oncol. 2003;89(1):129–133.
   PubMed Web of Science ®Google Scholar
• Fu S, Hennessy BT, Ng CS, et al. Perifosine plus docetaxel in patients with platinum and taxane resistant or refractory high-grade epithelial ovarian cancer. Gynecol Oncol. 2012;126(1):47–53.
   PubMed Web of Science ®Google Scholar
• Behbakht K, Sill MW, Darcy KM, et al. Phase II trial of the mTOR inhibitor, temsirolimus and evaluation of circulating tumor cells and tumor biomarkers in persistent and recurrent epithelial ovarian and primary peritoneal malignancies: a gynecologic oncology group study. Gynecol Oncol. 2011;123(1):19–26.
   PubMed Web of Science ®Google Scholar
• Schoffski P, Besse B, Gauler T, et al. Efficacy and safety of biweekly i.v. administrations of the aurora kinase inhibitor danusertib hydrochloride in independent cohorts of patients with advanced or metastatic breast, ovarian, colorectal, pancreatic, small-cell and non-small-cell lung cancer: a multi-tumour, multi-institutional phase II study. Ann Oncol. 2015;26(3):598–607.
   PubMed Web of Science ®Google Scholar
• Romero IL, McCormick A, McEwen KA, et al. Relationship of type II diabetes and metformin use to ovarian cancer progression, survival, and chemosensitivity. Obstet Gynecol. 2012;119(1):61–67.
   PubMed Web of Science ®Google Scholar
• Kumar S, Meuter A, Thapa P, et al. Metformin intake is associated with better survival in ovarian cancer: a case-control study. Cancer. 2013;119(3):555–562.
   PubMed Web of Science ®Google Scholar
• Shah MM, Erickson BK, Matin T, et al. Diabetes mellitus and ovarian cancer: more complex than just increasing risk. Gynecol Oncol. 2014;135(2):273–277.
   PubMed Web of Science ®Google Scholar
• Barakat RR, Berchuck A, Markman M, et al. Principles and practice of gynecologic oncology. 6th ed. Philadelphpia (PA): Lippincott Williams & Wilkins; 2013.
   Google Scholar
• Herzog TJ, Scambia G, Kim BG, et al. A randomized phase II trial of maintenance therapy with Sorafenib in front-line ovarian carcinoma. Gynecol Oncol. 2013;130(1):25–30.
   PubMed Web of Science ®Google Scholar
• Hainsworth JD, Thompson DS, Bismayer JA, 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):673–681.
   PubMed Web of Science ®Google Scholar
• Polcher M, Eckhardt M, Coch C, 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.
   PubMed Web of Science ®Google Scholar
• Della Pepa C, Tonini G, Santini D, et al. Low grade serous ovarian carcinoma: from the molecular characterization to the best therapeutic strategy. Cancer Treat Rev. 2015;41(2):136–143.
   PubMed Web of Science ®Google Scholar
• Gershenson DM, Sun CC, Wong -K-K. Impact of mutational status on survival in low-grade serous carcinoma of the ovary or peritoneum. Br J Cancer. 2015;113(9):1254–1258.
   PubMed Web of Science ®Google Scholar
• Grisham RN, Sylvester BE, Won H, et al. Extreme outlier analysis identifies occult mitogen-activated protein kinase pathway mutations in patients with low-grade serous ovarian cancer. J Clin Oncol. 2015;33(34):4099–4105.
   PubMed Web of Science ®Google Scholar
• Mabuchi S, Kawase C, Altomare DA, et al. mTOR is a promising therapeutic target both in cisplatin-sensitive and cisplatin-resistant clear cell carcinoma of the ovary. Clin Cancer Res. 2009;15(17):5404–5413.
   PubMed Web of Science ®Google Scholar
• Janku F, Wheler JJ, Westin SN, et al. PI3K/AKT/mTOR inhibitors in patients with breast and gynecologic malignancies harboring PIK3CA mutations. J Clin Oncol. 2012;30(8):777–782.
   PubMed Web of Science ®Google Scholar
• Carracedo A, Ma L, Teruya-Feldstein J, et al. Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest. 2008;118(9):3065–3074.
   PubMed Web of Science ®Google Scholar
• Azad NS, Posadas EM, Kwitkowski VE, et al. Combination targeted therapy with sorafenib and bevacizumab results in enhanced toxicity and antitumor activity. J Clin Oncol. 2008;26(22):3709–3714.
   PubMed Web of Science ®Google Scholar
• Pal SK, He M, Tong T, et al. RNA-seq reveals aurora kinase driven-mTOR pathway activation in patients with sarcomatoid metastatic renal cell carcinoma. Mol Cancer Res. 2015;13(1):130–137.
   PubMed Web of Science ®Google Scholar
• Taga MHE, Ouchi T. Essential roles of mTOR/akt pathway in aurora-a cell transformation. Int J Biol Sci. 2009;5(5):444–450.
   PubMed Web of Science ®Google Scholar
• Song J, Salek-Ardakani S, So T, et al. The kinases aurora B and mTOR regulate the G1-S cell cycle progression of T lymphocytes. Nat Immunol. 2007;8(1):64–73.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhou W, Wei L, et al. The effect of aurora kinases on cell proliferation, cell cycle regulation and metastasis in renal cell carcinoma. Int J Oncol. 2012;41(6):2139–2149.
   PubMed Web of Science ®Google Scholar
• Zhang S, Balch C, Chan MW, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008;68(11):4311–4320.
   PubMed Web of Science ®Google Scholar
• Silva IA, Bai S, McLean K, et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res. 2011;71(11):3991–4001.
   PubMed Web of Science ®Google Scholar
• Kolev VN, Wright QG, Vidal CM, et al. PI3K/mTOR dual inhibitor VS-5584 preferentially targets cancer stem cells. Cancer Res. 2015;75(2):446–455.
   PubMed Web of Science ®Google Scholar
• Francipane MG, Lagasse E. Therapeutic potential of mTOR inhibitors for targeting cancer stem cells. Br J Clin Pharmacol. 2015 Nov 26. [Epub ahead of print].
   PubMedGoogle Scholar
• Alvero AB, Montagna MK, Holmberg JC, et al. Targeting the mitochondria activates two independent cell death pathways in ovarian cancer stem cells. Mol Cancer Ther. 2011;10(8):1385–1393.
   PubMed Web of Science ®Google Scholar
• Bodmer M, Becker C, Meier C, et al. Use of metformin and the risk of ovarian cancer: a case–control analysis. Gynecol Oncol. 2011;123(2):200–204.
   PubMed Web of Science ®Google Scholar
• Tseng C-H. Metformin reduces ovarian cancer risk in Taiwanese women with type 2 diabetes mellitus. Diabetes Metab Res Rev. 2015;31(6):619–626.
   PubMed Web of Science ®Google Scholar
• Shi WY, Xiao D, Wang L, et al. Therapeutic metformin/AMPK activation blocked lymphoma cell growth via inhibition of mTOR pathway and induction of autophagy. Cell Death Dis. 2012;3:e275.
   PubMed Web of Science ®Google Scholar
• Vallianou NG, Evangelopoulos A, Kazazis C. Metformin and cancer. Rev Diabet Stud. 2013;10(4):228–235.
   PubMedGoogle Scholar
• Gotlieb WH, Saumet J, Beauchamp M-C, et al. In vitro metformin anti-neoplastic activity in epithelial ovarian cancer. Gynecol Oncol. 2008;110(2):246–250.
   PubMed Web of Science ®Google Scholar
• Rattan R, Giri S, Hartmann LC, et al. Metformin attenuates ovarian cancer cell growth in an AMP-kinase dispensable manner. J Cell Mol Med. 2011;15(1):166–178.
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov. U.S. National Institutes of Health. [cited 2015 Dec 24]. Available from: https://clinicaltrials.gov
   Google Scholar
• Koh YW, Shah MH, Agarwal K, et al. Sorafenib and Mek inhibition is synergistic in medullary thyroid carcinoma in vitro. Endocr Relat Cancer. 2012;19(1):29–38.
   PubMed Web of Science ®Google Scholar
• Adnane LTP, Wilhelm SM. Sorafenib (BAY 43-9006, Nexvar), a dual-action inhibitor that targets RAF/MEK/ERK pathway in tumor cells and tyrosine kinases VEGFR/PDGFR in tumor vasculature. Methods Enzymol. 2006;407:597–612.
   PubMed Web of Science ®Google Scholar
• Holderfield MNT, Stuart DD. Mechanism and consequences of RAF kinase activation by small-molecule inhibitors. Br J Cancer. 2014;111(4):640–645.
   PubMed Web of Science ®Google Scholar