Targeting Membrane Receptors of Ovarian Cancer Cells for Therapy

Author(s): Zhiquan Liang, Ziwen Lu, Yafei Zhang, Dongsheng Shang, Ruyan Li, Lanlan Liu, Zhicong Zhao, Peishan Zhang, Qiong Lin, Chunlai Feng, Yibang Zhang, Peng Liu, Zhigang Tu*, Hanqing Liu*.

Journal Name: Current Cancer Drug Targets

Volume 19 , Issue 6 , 2019

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Abstract:

Ovarian cancer is a leading cause of death worldwide from gynecological malignancies, mainly because there are few early symptoms and the disease is generally diagnosed at an advanced stage. In addition, despite the effectiveness of cytoreductive surgery for ovarian cancer and the high response rates to chemotherapy, survival has improved little over the last 20 years. The management of patients with ovarian cancer also remains similar despite studies showing striking differences and heterogeneity among different subtypes. It is therefore clear that novel targeted therapeutics are urgently needed to improve clinical outcomes for ovarian cancer. To that end, several membrane receptors associated with pivotal cellular processes and often aberrantly overexpressed in ovarian cancer cells have emerged as potential targets for receptor-mediated therapeutic strategies including specific agents and multifunctional delivery systems based on ligand-receptor binding. This review focuses on the profiles and potentials of such strategies proposed for ovarian cancer treatment and imaging.

Keywords: Ovarian cancer, membrane receptors, targeted therapy, ligand-receptor binding, peptide vaccination, PD-L1.

[1]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2018. CA Cancer J. Clin., 2018, 68(1), 7-30.
[2]
Marchetti, C.; Pisano, C.; Facchini, G.; Bruni, G.S.; Magazzino, F.P.; Losito, S.; Pignata, S. First-line treatment of advanced ovarian cancer: current research and perspectives. Expert Rev. Anticancer Ther., 2010, 10(1), 47-60.
[3]
Tempfer, C.B.; Celik, I.; Solass, W.; Buerkle, B.; Pabst, U.G.; Zieren, J.; Strumberg, D.; Reymond, M.A. Activity of pressurized intraperitoneal aerosol chemotherapy (PIPAC) with cisplatin and doxorubicin in women with recurrent, platinum-resistant ovarian cancer: preliminary clinical experience. Gynecol. Oncol., 2014, 132(2), 307-311.
[4]
Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2016. CA Cancer J. Clin., 2016, 66(1), 7-30.
[5]
Ullrich, A.; Schlessinger, J. Signal transduction by receptors with tyrosine kinase activity. Cell, 1990, 61(2), 203-212.
[6]
Schneider, G.; Fechner, U. Computer-based de novo design of drug-like molecules. Nat. Rev. Drug Discov., 2005, 4(8), 649-663.
[7]
Sillanpaa, S.; Anttila, M.A.; Voutilainen, K.; Tammi, R.H.; Tammi, M.I.; Saarikoski, S.V.; Kosma, V.M. CD44 expression indicates favorable prognosis in epithelial ovarian cancer. Clin. Cancer Res., 2003, 9(14), 5318-2534.
[8]
Dharap, S.S.; Wang, Y.; Chandna, P.; Khandare, J.J.; Qiu, B.; Gunaseelan, S.; Sinko, P.J.; Stein, S.; Farmanfarmaian, A.; Minko, T. Tumor-specific targeting of an anticancer drug delivery system by LHRH peptide. Proc. Natl. Acad. Sci. USA, 2005, 102(36), 12962-12967.
[9]
Assaraf, Y.G.; Leamon, C.P.; Reddy, J.A. The folate receptor as a rational therapeutic target for personalized cancer treatment. Drug Resist. Updat., 2014, 17(4-6), 89-95.
[10]
Wang, K.; Li, D.; Sun, L. High levels of EGFR expression in tumor stroma are associated with aggressive clinical features in epithelial ovarian cancer. OncoTargets Ther., 2016, 9, 377-386.
[11]
Bublil, E.M.; Yarden, Y. The EGF receptor family: spearheading a merger of signaling and therapeutics. Curr. Opin. Cell Biol., 2007, 19(2), 124-134.
[12]
Akhtar, S.; Chandrasekhar, B.; Attur, S.; Dhaunsi, G.S.; Yousif, M.H.; Benter, I.F. Transactivation of ErbB family of receptor tyrosine kinases is inhibited by angiotensin-(1-7) via its Mas receptor. PLoS One, 2015, 10(11)e0141657
[13]
Ceresa, B.P.; Vanlandingham, P.A. Molecular mechanisms that regulate epidermal growth factor receptor inactivation. Clin. Med. Oncol., 2008, 2, 47-61.
[14]
Lafky, J.M.; Wilken, J.A.; Baron, A.T.; Maihle, N.J. Clinical implications of the ErbB/epidermal growth factor (EGF) receptor family and its ligands in ovarian cancer. Biochim. Biophys. Acta, 2008, 1785(2), 232-265.
[15]
Moscatello, D.K.; Holgado-Madruga, M.; Godwin, A.K.; Ramirez, G.; Gunn, G.; Zoltick, P.W.; Biegel, J.A.; Hayes, R.L.; Wong, A.J. Frequent expression of a mutant epidermal growth factor receptor in multiple human tumors. Cancer Res., 1995, 55(23), 5536-5539.
[16]
Alper, O.; Bergmann-Leitner, E.S.; Bennett, T.A.; Hacker, N.F.; Stromberg, K.; Stetler-Stevenson, W.G. Epidermal growth factor receptor signaling and the invasive phenotype of ovarian carcinoma cells. J. Natl. Cancer Inst., 2001, 93(18), 1375-1384.
[17]
Olayioye, M.A. Update on HER-2 as a target for cancer therapy: intracellular signaling pathways of ErbB2/HER-2 and family members. Breast Cancer Res., 2001, 3(6), 385-389.
[18]
Nagy, P.; Jenei, A.; Kirsch, A.K.; Szollosi, J.; Damjanovich, S.; Jovin, T.M. Activation-dependent clustering of the erbB2 receptor tyrosine kinase detected by scanning near-field optical microscopy. J. Cell Sci., 1999, 112(Pt 11), 1733-1741.
[19]
Kaufmann, R.; Muller, P.; Hildenbrand, G.; Hausmann, M.; Cremer, C. Analysis of Her2/neu membrane protein clusters in different types of breast cancer cells using localization microscopy. J. Microsc., 2011, 242(1), 46-54.
[20]
Hellstrom, I.; Goodman, G.; Pullman, J.; Yang, Y.; Hellstrom, K.E. Overexpression of HER-2 in ovarian carcinomas. Cancer Res., 2001, 61(6), 2420-2423.
[21]
McAlpine, J.N.; Wiegand, K.C.; Vang, R.; Ronnett, B.M.; Adamiak, A.; Kobel, M.; Kalloger, S.E.; Swenerton, K.D.; Huntsman, D.G.; Gilks, C.B.; Miller, D.M. HER2 overexpression and amplification is present in a subset of ovarian mucinous carcinomas and can be targeted with trastuzumab therapy. BMC Cancer, 2009, 9, 433.
[22]
Holmes, K.; Roberts, O.L.; Thomas, A.M.; Cross, M.J. Vascular endothelial growth factor receptor-2: Structure, function, intracellular signalling and therapeutic inhibition. Cell. Signal., 2007, 19(10), 2003-2012.
[23]
Brown, M.R.; Blanchette, J.O.; Kohn, E.C. Angiogenesis in ovarian cancer. Bailliere's best practice & research Clin. Obstet. Gynaecol., 2000, 14(6), 901-918.
[24]
Klasa-Mazurkiewicz, D.; Jarzab, M.; Milczek, T.; Lipinska, B.; Emerich, J. Clinical significance of VEGFR-2 and VEGFR-3 expression in ovarian cancer patients. Pol. J. Pathol., 2011, 62(1), 31-40.
[25]
Tomasina, J.; Lheureux, S.; Gauduchon, P.; Rault, S.; Malzert-Freon, A. Nanocarriers for the targeted treatment of ovarian cancers. Biomaterials, 2013, 34(4), 1073-1101.
[26]
Liefers-Visser, J.A.L.; Meijering, R.A.M.; Reyners, A.K.L.; van der Zee, A.G.J.; de Jong, S. IGF system targeted therapy: Therapeutic opportunities for ovarian cancer. Cancer Treat. Rev., 2017, 60, 90-99.
[27]
King, E.R.; Zu, Z.; Tsang, Y.T.; Deavers, M.T.; Malpica, A.; Mok, S.C.; Gershenson, D.M.; Wong, K.K. The insulin-like growth factor 1 pathway is a potential therapeutic target for low-grade serous ovarian carcinoma. Gynecol. Oncol., 2011, 123(1), 13-18.
[28]
Ouban, A.; Muraca, P.; Yeatman, T.; Coppola, D. Expression and distribution of insulin-like growth factor-1 receptor in human carcinomas. Hum. Pathol., 2003, 34(8), 803-808.
[29]
Wang, Y.; Hailey, J.; Williams, D.; Wang, Y.; Lipari, P.; Malkowski, M.; Wang, X.; Xie, L.; Li, G.; Saha, D.; Ling, W.L.; Cannon-Carlson, S.; Greenberg, R.; Ramos, R.A.; Shields, R.; Presta, L.; Brams, P.; Bishop, W.R.; Pachter, J.A. Inhibition of insulin-like growth factor-I receptor (IGF-IR) signaling and tumor cell growth by a fully human neutralizing anti-IGF-IR antibody. Mol. Cancer Ther., 2005, 4(8), 1214-1221.
[30]
Beltran, P.J.; Calzone, F.J.; Mitchell, P.; Chung, Y.A.; Cajulis, E.; Moody, G.; Belmontes, B.; Li, C.M.; Vonderfecht, S.; Velculescu, V.E.; Yang, G.; Qi, J.; Slamon, D.J.; Konecny, G.E. Ganitumab (AMG 479) inhibits IGF-II-dependent ovarian cancer growth and potentiates platinum-based chemotherapy. Clin. Cancer Res., 2014, 20(11), 2947-2958.
[31]
Henriksen, R.; Funa, K.; Wilander, E.; Backstrom, T.; Ridderheim, M.; Oberg, K. Expression and prognostic significance of platelet-derived growth factor and its receptors in epithelial ovarian neoplasms. Cancer Res., 1993, 53(19), 4550-4554.
[32]
Matei, D.; Graeber, T.G.; Baldwin, R.L.; Karlan, B.Y.; Rao, J.; Chang, D.D. Gene expression in epithelial ovarian carcinoma. Oncogene, 2002, 21(41), 6289-6298.
[33]
Bhaw-Luximon, A.; Jhurry, D. Artemisinin and its derivatives in cancer therapy: status of progress, mechanism of action, and future perspectives. Cancer Chemother. Pharmacol., 2017, 79(3), 451-466.
[34]
Li, X.; Ba, Q.; Liu, Y.; Yue, Q.; Chen, P.; Li, J.; Zhang, H.; Ying, H.; Ding, Q.; Song, H.; Liu, H.; Zhang, R.; Wang, H. Dihydroartemisinin selectively inhibits PDGFRalpha-positive ovarian cancer growth and metastasis through inducing degradation of PDGFRalpha protein. Cell Discov., 2017, 3, 17042.
[35]
Liu, H.; Kiseleva, A.A.; Golemis, E.A. Ciliary signalling in cancer. Nat. Rev. Cancer, 2018, 18(8), 511-524.
[36]
Ledermann, J.A.; Canevari, S.; Thigpen, T. Targeting the folate receptor: Diagnostic and therapeutic approaches to personalize cancer treatments. Ann. Oncol., 2015, 26(10), 2034-2043.
[37]
Elnakat, H.; Ratnam, M. Distribution, functionality and gene regulation of folate receptor isoforms: Implications in targeted therapy. Adv. Drug Deliv. Rev., 2004, 56(8), 1067-1084.
[38]
Toffoli, G.; Cernigoi, C.; Russo, A.; Gallo, A.; Bagnoli, M.; Boiocchi, M. Overexpression of folate binding protein in ovarian cancers. Int. J. Cancer, 1997, 74(2), 193-198.
[39]
Parker, N.; Turk, M.J.; Westrick, E.; Lewis, J.D.; Low, P.S.; Leamon, C.P. Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay. Anal. Biochem., 2005, 338(2), 284-293.
[40]
Sasaki, Y.; Miwa, K.; Yamashita, K.; Sunakawa, Y.; Shimada, K.; Ishida, H.; Hasegawa, K.; Fujiwara, K.; Kodaira, M.; Fujiwara, Y.; Namiki, M.; Matsuda, M.; Takeuchi, Y.; Katsumata, N. A phase I study of farletuzumab, a humanized anti-folate receptor alpha monoclonal antibody, in patients with solid tumors. Invest. New Drugs, 2015, 33(2), 332-340.
[41]
Wen, Y.; Graybill, W.S.; Previs, R.A.; Hu, W.; Ivan, C.; Mangala, L.S.; Zand, B.; Nick, A.M.; Jennings, N.B.; Dalton, H.J.; Sehgal, V.; Ram, P.; Lee, J.S.; Vivas-Mejia, P.E.; Coleman, R.L.; Sood, A.K. Immunotherapy targeting folate receptor induces cell death associated with autophagy in ovarian cancer. Clin. Cancer Res., 2015, 21(2), 448-459.
[42]
Vergote, I.; Armstrong, D.; Scambia, G.; Teneriello, M.; Sehouli, J.; Schweizer, C.; Weil, S.C.; Bamias, A.; Fujiwara, K.; Ochiai, K.; Poole, C.; Gorbunova, V.; Wang, W.; O’Shannessy, D.; Herzog, T.J. A randomized, double-blind, placebo-controlled, phase III study to assess efficacy and safety of weekly farletuzumab in combination with carboplatin and taxane in patients with ovarian cancer in first platinum-sensitive relapse. J. Clin. Oncol., 2016, 34(19), 2271-2278.
[43]
Ando, M.; Nagata, K.; Nihira, K.; Suzuki, Y.; Kanda, Y.; Adachi, M.; Kubota, T.; Kameyama, N.; Nakano, M.; Ando, H.; Yamano, K.; Ishii, T.; Nakai, R.; Nakamura, K. Potent therapeutic activity against peritoneal dissemination and malignant ascites by the novel anti-folate receptor alpha antibody KHK2805. Transl. Oncol., 2017, 10(5), 707-718.
[44]
Kalli, K.R.; Block, M.S.; Kasi, P.M.; Erskine, C.L.; Hobday, T.J.; Dietz, A.; Padley, D.; Gustafson, M.P.; Shreeder, B.; Puglisi-Knutson, D.; Visscher, D.W.; Mangskau, T.K.; Wilson, G.; Knutson, K.L. Folate receptor alpha peptide vaccine generates immunity in breast and ovarian cancer patients. Clin. Cancer Res., 2018, 24(13), 3014-3025.
[45]
Jones, S.K.; Lizzio, V.; Merkel, O.M. Folate receptor targeted delivery of siRNA and paclitaxel to ovarian cancer cells via folate conjugated triblock copolymer to overcome TLR4 driven chemotherapy resistance. Biomacromolecules, 2016, 17(1), 76-87.
[46]
Lee, J.Y.; Termsarasab, U.; Park, J.H.; Lee, S.Y.; Ko, S.H.; Shim, J.S.; Chung, S.J.; Cho, H.J.; Kim, D.D. Dual CD44 and folate receptor-targeted nanoparticles for cancer diagnosis and anticancer drug delivery. J. Control. Release, 2016, 236, 38-46.
[47]
Ak, G.; Yilmaz, H.; Gunes, A.; Hamarat Sanlier, S. In vitro and in vivo evaluation of folate receptor-targeted a novel magnetic drug delivery system for ovarian cancer therapy. Artif. Cells Nanomed. Biotechnol., 2018, 1-12.
[48]
Vergote, I.; Leamon, C.P. Vintafolide: A novel targeted therapy for the treatment of folate receptor expressing tumors. Ther. Adv. Med. Oncol., 2015, 7(4), 206-218.
[49]
Moore, K.N.; Martin, L.P.; O’Malley, D.M.; Matulonis, U.A.; Konner, J.A.; Perez, R.P.; Bauer, T.M.; Ruiz-Soto, R.; Birrer, M.J. Safety and activity of mirvetuximab soravtansine (IMGN853), a folate receptor alpha-targeting antibody-drug conjugate, in platinum-resistant ovarian, fallopian tube, or primary peritoneal cancer: a phase i expansion study. J. Clin. Oncol., 2017, 35(10), 1112-1118.
[50]
Moore, K.N.; Borghaei, H.; O’Malley, D.M.; Jeong, W.; Seward, S.M.; Bauer, T.M.; Perez, R.P.; Matulonis, U.A.; Running, K.L.; Zhang, X.; Ponte, J.F.; Ruiz-Soto, R.; Birrer, M.J. Phase 1 dose-escalation study of mirvetuximab soravtansine (IMGN853), a folate receptor alpha-targeting antibody-drug conjugate, in patients with solid tumors. Cancer, 2017, 123(16), 3080-3087.
[51]
Riabov, V.; Gudima, A.; Wang, N.; Mickley, A.; Orekhov, A.; Kzhyshkowska, J. Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front. Physiol., 2014, 5, 75.
[52]
Penn, C.A.; Yang, K.; Zong, H.; Lim, J.Y.; Cole, A.; Yang, D.; Baker, J.; Goonewardena, S.N.; Buckanovich, R.J. Therapeutic impact of nanoparticle therapy targeting tumor-associated macrophages. Mol. Cancer Ther., 2018, 17(1), 96-106.
[53]
Hou, Z.; Gattoc, L.; O’Connor, C.; Yang, S.; Wallace-Povirk, A.; George, C.; Orr, S.; Polin, L.; White, K.; Kushner, J.; Morris, R.T.; Gangjee, A.; Matherly, L.H. Dual targeting of epithelial ovarian cancer via folate receptor alpha and the proton-coupled folate transporter with 6-Substituted Pyrrolo[2,3-d]pyrimidine antifolates. Mol. Cancer Ther., 2017, 16(5), 819-830.
[54]
Ravindra, M.; Wilson, M.R.; Tong, N.; O’Connor, C.; Karim, M.; Polin, L.; Wallace-Povirk, A.; White, K.; Kushner, J.; Hou, Z.; Matherly, L.H.; Gangjee, A. Fluorine-substituted pyrrolo[2,3- d]pyrimidine analogues with tumor targeting via cellular uptake by folate receptor alpha and the proton-coupled folate transporter and inhibition of de novo purine nucleotide biosynthesis. J. Med. Chem., 2018, 61(9), 4228-4248.
[55]
Goodison, S.; Urquidi, V.; Tarin, D. CD44 cell adhesion molecules. Mol. Pathol., 1999, 52(4), 189-196.
[56]
Assimakopoulos, D.; Kolettas, E.; Patrikakos, G.; Evangelou, A. The role of CD44 in the development and prognosis of head and neck squamous cell carcinomas. Histol. Histopathol., 2002, 17(4), 1269-1281.
[57]
Wang, S.J.; Wong, G.; de Heer, A.M.; Xia, W.; Bourguignon, L.Y. CD44 variant isoforms in head and neck squamous cell carcinoma progression. Laryngoscope, 2009, 119(8), 1518-1530.
[58]
Griffith, J.S.; Liu, Y.G.; Tekmal, R.R.; Binkley, P.A.; Holden, A.E.; Schenken, R.S. Menstrual endometrial cells from women with endometriosis demonstrate increased adherence to peritoneal cells and increased expression of CD44 splice variants. Fertil. Steril., 2010, 93(6), 1745-1749.
[59]
Yan, Y.; Zuo, X.; Wei, D. Concise review: Emerging role of CD44 in cancer stem cells: a promising biomarker and therapeutic target. Stem Cells Transl. Med., 2015, 4(9), 1033-1043.
[60]
Gao, Y.; Foster, R.; Yang, X.; Feng, Y.; Shen, J.K.; Mankin, H.J.; Hornicek, F.J.; Amiji, M.M.; Duan, Z. Up-regulation of CD44 in the development of metastasis, recurrence and drug resistance of ovarian cancer. Oncotarget, 2015, 6(11), 9313-9326.
[61]
Elzarkaa, A.A.; Sabaa, B.E.; Abdelkhalik, D.; Mansour, H.; Melis, M.; Shaalan, W.; Farouk, M.; Malik, E.; Soliman, A.A. Clinical relevance of CD44 surface expression in advanced stage serous epithelial ovarian cancer: a prospective study. J. Cancer Res. Clin. Oncol., 2016, 142(5), 949-958.
[62]
Lee, S.J.; Ghosh, S.C.; Han, H.D.; Stone, R.L.; Bottsford-Miller, J.; Shen, D.Y.; Auzenne, E.J.; Lopez-Araujo, A.; Lu, C.; Nishimura, M.; Pecot, C.V.; Zand, B.; Thanapprapasr, D.; Jennings, N.B.; Kang, Y.; Huang, J.; Hu, W.; Klostergaard, J.; Sood, A.K. Metronomic activity of CD44-targeted hyaluronic acid-paclitaxel in ovarian carcinoma. Clin. Cancer Res., 2012, 18(15), 4114-4121.
[63]
Dreaden, E.C.; Morton, S.W.; Shopsowitz, K.E.; Choi, J.H.; Deng, Z.J.; Cho, N.J.; Hammond, P.T. Bimodal tumor-targeting from microenvironment responsive hyaluronan layer-by-layer (LbL) nanoparticles. ACS Nano, 2014, 8(8), 8374-8382.
[64]
Wang, L.; Jia, E. Ovarian cancer targeted hyaluronic acid-based nanoparticle system for paclitaxel delivery to overcome drug resistance. Drug Deliv., 2016, 23(5), 1810-1817.
[65]
Bae, K.H.; Tan, S.; Yamashita, A.; Ang, W.X.; Gao, S.J.; Wang, S.; Chung, J.E.; Kurisawa, M. Hyaluronic acid-green tea catechin micellar nanocomplexes: Fail-safe cisplatin nanomedicine for the treatment of ovarian cancer without off-target toxicity. Biomaterials, 2017, 148, 41-53.
[66]
Bai, M.Y.; Liu, S.Z. A simple and general method for preparing antibody-PEG-PLGA sub-micron particles using electrospray technique: an in vitro study of targeted delivery of cisplatin to ovarian cancer cells. Colloids surfaces. B Biointerfaces, 2014, 117, 346-353.
[67]
Brandsma, M.E.; Jevnikar, A.M.; Ma, S. Recombinant human transferrin: beyond iron binding and transport. Biotechnol. Adv., 2011, 29(2), 230-238.
[68]
Aisen, P.; Leibman, A.; Zweier, J. Stoichiometric and site characteristics of the binding of iron to human transferrin. J. Biol. Chem., 1978, 253(6), 1930-1937.
[69]
Li, H.; Qian, Z.M. Transferrin/transferrin receptor-mediated drug delivery. Med. Res. Rev., 2002, 22(3), 225-250.
[70]
Calzolari, A.; Oliviero, I.; Deaglio, S.; Mariani, G.; Biffoni, M.; Sposi, N.M.; Malavasi, F.; Peschle, C.; Testa, U. Transferrin receptor 2 is frequently expressed in human cancer cell lines. Blood Cells Mol. Dis., 2007, 39(1), 82-91.
[71]
Prutki, M.; Poljak-Blazi, M.; Jakopovic, M.; Tomas, D.; Stipancic, I.; Zarkovic, N. Altered iron metabolism, transferrin receptor 1 and ferritin in patients with colon cancer. Cancer Lett., 2006, 238(2), 188-196.
[72]
Kondo, K.; Noguchi, M.; Mukai, K.; Matsuno, Y.; Sato, Y.; Shimosato, Y.; Monden, Y. Transferrin receptor expression in adenocarcinoma of the lung as a histopathologic indicator of prognosis. Chest, 1990, 97(6), 1367-1371.
[73]
Ryschich, E.; Huszty, G.; Knaebel, H.P.; Hartel, M.; Buchler, M.W.; Schmidt, J. Transferrin receptor is a marker of malignant phenotype in human pancreatic cancer and in neuroendocrine carcinoma of the pancreas. Eur. J. Cancer, 2004, 40(9), 1418-1422.
[74]
Basuli, D.; Tesfay, L.; Deng, Z.; Paul, B.; Yamamoto, Y.; Ning, G.; Xian, W.; McKeon, F.; Lynch, M.; Crum, C.P.; Hegde, P.; Brewer, M.; Wang, X.; Miller, L.D.; Dyment, N.; Torti, F.M.; Torti, S.V. Iron addiction: A novel therapeutic target in ovarian cancer. Oncogene, 2017, 36(29), 4089-4099.
[75]
Oh, K.S.; Engler, J.A.; Joung, I. Enhancement of gene delivery to cancer cells by a retargeted adenovirus. J. Microbiol., 2005, 43(2), 179-182.
[76]
Cardoso, A.L.; Simoes, S.; de Almeida, L.P.; Pelisek, J.; Culmsee, C.; Wagner, E.; Pedroso de Lima, M.C. siRNA delivery by a transferrin-associated lipid-based vector: a non-viral strategy to mediate gene silencing. J. Gene Med., 2007, 9(3), 170-183.
[77]
Krieger, M.L.; Eckstein, N.; Schneider, V.; Koch, M.; Royer, H.D.; Jaehde, U.; Bendas, G. Overcoming cisplatin resistance of ovarian cancer cells by targeted liposomes in vitro. Int. J. Pharm., 2010, 389(1-2), 10-17.
[78]
Peng, H.; Jin, H.; Zhuo, H.; Huang, H. Enhanced antitumor efficacy of cisplatin for treating ovarian cancer in vitro and in vivo via transferrin binding. Oncotarget, 2017, 8(28), 45597-45611.
[79]
Deshpande, P.; Jhaveri, A.; Pattni, B.; Biswas, S.; Torchilin, V. Transferrin and octaarginine modified dual-functional liposomes with improved cancer cell targeting and enhanced intracellular delivery for the treatment of ovarian cancer. Drug Deliv., 2018, 25(1), 517-532.
[80]
Bast, R.C. Jr.; Xu, F.J.; Yu, Y.H.; Barnhill, S.; Zhang, Z.; Mills, G.B. CA 125: The past and the future. Int. J. Biol. Markers, 1998, 13(4), 179-187.
[81]
Gordon, A.N.; Schultes, B.C.; Gallion, H.; Edwards, R.; Whiteside, T.L.; Cermak, J.M.; Nicodemus, C.F. CA125- and tumor-specific T-cell responses correlate with prolonged survival in oregovomab-treated recurrent ovarian cancer patients. Gynecol. Oncol., 2004, 94(2), 340-351.
[82]
Berek, J.; Taylor, P.; McGuire, W.; Smith, L.M.; Schultes, B.; Nicodemus, C.F. Oregovomab maintenance monoimmunotherapy does not improve outcomes in advanced ovarian cancer. J. Clin. Oncol., 2009, 27(3), 418-425.
[83]
Pfisterer, J.; Harter, P.; Simonelli, C.; Peters, M.; Berek, J.; Sabbatini, P.; du Bois, A. Abagovomab for ovarian cancer. Expert Opin. Biol. Ther., 2011, 11(3), 395-403.
[84]
Battaglia, A.; Fossati, M.; Buzzonetti, A.; Scambia, G.; Fattorossi, A. A robust immune system conditions the response to abagovomab (anti-idiotypic monoclonal antibody mimicking the CA125 protein) vaccination in ovarian cancer patients. Immunol. Lett., 2017, 191, 35-39.
[85]
Armstrong, A.; Eck, S.L. EpCAM: A new therapeutic target for an old cancer antigen. Cancer Biol. Ther., 2003, 2(4), 320-326.
[86]
Patriarca, C.; Macchi, R.M.; Marschner, A.K.; Mellstedt, H. Epithelial cell adhesion molecule expression (CD326) in cancer: A short review. Cancer Treat. Rev., 2012, 38(1), 68-75.
[87]
Linke, R.; Klein, A.; Seimetz, D. Catumaxomab: Clinical development and future directions. MAbs, 2010, 2(2), 129-136.
[88]
Seimetz, D.; Lindhofer, H.; Bokemeyer, C. Development and approval of the trifunctional antibody catumaxomab (anti-EpCAM x anti-CD3) as a targeted cancer immunotherapy. Cancer treat. Rev., 2010, 36(6), 458-467.
[89]
Ohtani, K.; Sakamoto, H.; Kikuchi, A.; Nakayama, Y.; Idei, T.; Igarashi, N.; Matukawa, T.; Satoh, K. Follicle-stimulating hormone promotes the growth of human epithelial ovarian cancer cells through the protein kinase C-mediated system. Cancer Lett., 2001, 166(2), 207-213.
[90]
Huang, Y.; Jin, H.; Liu, Y.; Zhou, J.; Ding, J.; Cheng, K.W.; Yu, Y.; Feng, Y. FSH inhibits ovarian cancer cell apoptosis by up-regulating survivin and down-regulating PDCD6 and DR5. Endocr. Relat. Cancer, 2011, 18(1), 13-26.
[91]
Yang, Y.; Zhang, J.; Zhu, Y.; Zhang, Z.; Sun, H.; Feng, Y. Follicle-stimulating hormone induced epithelial-mesenchymal transition of epithelial ovarian cancer cells through follicle-stimulating hormone receptor PI3K/Akt-Snail signaling pathway. Int. J. Gynecol. Cancer, 2014, 24(9), 1564-1574.
[92]
Wang, J.; Lin, L.; Parkash, V.; Schwartz, P.E.; Lauchlan, S.C.; Zheng, W. Quantitative analysis of follicle-stimulating hormone receptor in ovarian epithelial tumors: A novel approach to explain the field effect of ovarian cancer development in secondary mullerian systems. Int. J. Cancer, 2003, 103(3), 328-334.
[93]
Choi, J.H.; Wong, A.S.; Huang, H.F.; Leung, P.C. Gonadotropins and ovarian cancer. Endocr. Rev., 2007, 28(4), 440-461.
[94]
Gartrell, B.A.; Tsao, C.K.; Galsky, M.D. The follicle-stimulating hormone receptor: A novel target in genitourinary malignancies. Urol. Oncol., 2013, 31(8), 1403-1407.
[95]
Radu, A.; Pichon, C.; Camparo, P.; Antoine, M.; Allory, Y.; Couvelard, A.; Fromont, G.; Hai, M.T.; Ghinea, N. Expression of follicle-stimulating hormone receptor in tumor blood vessels. N. Engl. J. Med., 2010, 363(17), 1621-1630.
[96]
Agris, P.F.; Guenther, R.H.; Sierzputowska-Gracz, H.; Easter, L.; Smith, W.; Hardin, C.C.; Santa-Coloma, T.A.; Crabb, J.W.; Reichert, L.E., Jr Solution structure of a synthetic peptide corresponding to a receptor binding region of FSH (hFSH-beta 33-53). J. Protein Chem., 1992, 11(5), 495-507.
[97]
Zhang, X.; Chen, J.; Kang, Y.; Hong, S.; Zheng, Y.; Sun, H.; Xu, C. Targeted paclitaxel nanoparticles modified with follicle-stimulating hormone beta 81-95 peptide show effective antitumor activity against ovarian carcinoma. Int. J. Pharm., 2013, 453(2), 498-505.
[98]
Hong, S.S.; Zhang, M.X.; Zhang, M.; Yu, Y.; Chen, J.; Zhang, X.Y.; Xu, C.J. Follicle-stimulating hormone peptide-conjugated nanoparticles for targeted shRNA delivery lead to effective gro-alpha silencing and antitumor activity against ovarian cancer. Drug Deliv., 2018, 25(1), 576-584.
[99]
Lee, C.W.; Guo, L.; Matei, D.; Stantz, K. Development of follicle-stimulating hormone receptor binding probes to image ovarian xenografts. J. Biotechnol. Biomater., 2015, 5(3), 198.
[100]
Hong, H.; Yan, Y.; Shi, S.; Graves, S.A.; Krasteva, L.K.; Nickles, R.J.; Yang, M.; Cai, W. PET of follicle-stimulating hormone receptor: broad applicability to cancer imaging. Mol. Pharm., 2015, 12(2), 403-410.
[101]
Urbanska, K.; Stashwick, C.; Poussin, M.; Powell, D.J., Jr Follicle-stimulating hormone receptor as a target in the redirected t-cell therapy for cancer. Cancer Immunol. Res., 2015, 3(10), 1130-1137.
[102]
Millar, R.P. GnRHs and GnRH receptors. Anim. Reprod. Sci., 2005, 88(1-2), 5-28.
[103]
Layman, L.C.; Cohen, D.P.; Jin, M.; Xie, J.; Li, Z.; Reindollar, R.H.; Bolbolan, S.; Bick, D.P.; Sherins, R.R.; Duck, L.W.; Musgrove, L.C.; Sellers, J.C.; Neill, J.D. Mutations in gonadotropin-releasing hormone receptor gene cause hypogonadotropic hypogonadism. Nat. Genet., 1998, 18(1), 14-15.
[104]
Volker, P.; Grundker, C.; Schmidt, O.; Schulz, K.D.; Emons, G. Expression of receptors for luteinizing hormone-releasing hormone in human ovarian and endometrial cancers: Frequency, autoregulation, and correlation with direct antiproliferative activity of luteinizing hormone-releasing hormone analogues. Am. J. Obstet. Gynecol., 2002, 186(2), 171-179.
[105]
Nagy, A.; Plonowski, A.; Schally, A.V. Stability of cytotoxic luteinizing hormone-releasing hormone conjugate (AN-152) containing doxorubicin 14-O-hemiglutarate in mouse and human serum in vitro: Implications for the design of preclinical studies. Proc. Natl. Acad. Sci. USA, 2000, 97(2), 829-834.
[106]
Shah, V.; Taratula, O.; Garbuzenko, O.B.; Taratula, O.R.; Rodriguez-Rodriguez, L.; Minko, T. Targeted nanomedicine for suppression of CD44 and simultaneous cell death induction in ovarian cancer: an optimal delivery of siRNA and anticancer drug. Clin. Cancer Res., 2013, 19(22), 6193-6204.
[107]
Li, X.; Shen, B.; Chen, Q.; Zhang, X.; Ye, Y.; Wang, F.; Zhang, X. Antitumor effects of cecropin B-LHRH’ on drug-resistant ovarian and endometrial cancer cells. BMC Cancer, 2016, 16, 251.
[108]
Ye, H.; Liu, X.; Sun, J.; Zhu, S.; Zhu, Y.; Chang, S. Enhanced therapeutic efficacy of LHRHa-targeted brucea javanica oil liposomes for ovarian cancer. BMC Cancer, 2016, 16(1), 831.
[109]
Murer, H.; Forster, I.; Biber, J. The sodium phosphate cotransporter family SLC34. Eur. J. Phys., 2004, 447(5), 763-767.
[110]
Hilfiker, H.; Hattenhauer, O.; Traebert, M.; Forster, I.; Murer, H.; Biber, J. Characterization of a murine type II sodium-phosphate cotransporter expressed in mammalian small intestine. Proc. Natl. Acad. Sci. USA, 1998, 95(24), 14564-14569.
[111]
Yin, B.W.; Kiyamova, R.; Chua, R.; Caballero, O.L.; Gout, I.; Gryshkova, V.; Bhaskaran, N.; Souchelnytskyi, S.; Hellman, U.; Filonenko, V.; Jungbluth, A.A.; Odunsi, K.; Lloyd, K.O.; Old, L.J.; Ritter, G. Monoclonal antibody MX35 detects the membrane transporter NaPi2b (SLC34A2) in human carcinomas. Cancer Immun., 2008, 8, 3.
[112]
Gryshkova, V.; Goncharuk, I.; Gurtovyy, V.; Khozhayenko, Y.; Nespryadko, S.; Vorobjova, L.; Usenko, V.; Gout, I.; Filonenko, V.; Kiyamova, R. The study of phosphate transporter NAPI2B expression in different histological types of epithelial ovarian cancer. Exp. Oncol., 2009, 31(1), 37-42.
[113]
Shyian, M.; Gryshkova, V.; Kostianets, O.; Gorshkov, V.; Gogolev, Y.; Goncharuk, I.; Nespryadko, S.; Vorobjova, L.; Filonenko, V.; Kiyamova, R. Quantitative analysis of SLC34A2 expression in different types of ovarian tumors. Exp. Oncol., 2011, 33(2), 94-98.
[114]
Lin, K.; Rubinfeld, B.; Zhang, C.; Firestein, R.; Harstad, E.; Roth, L.; Tsai, S.P.; Schutten, M.; Xu, K.; Hristopoulos, M.; Polakis, P. Preclinical development of an anti-NaPi2b (SLC34A2) antibody-drug conjugate as a therapeutic for non-small cell lung and ovarian cancers. Clin. Cancer Res., 2015, 21(22), 5139-5150.
[115]
Banerjee, S.; Oza, A.M.; Birrer, M.J.; Hamilton, E.P.; Hasan, J.; Leary, A.; Moore, K.N.; Mackowiak-Matejczyk, B.; Pikiel, J.; Ray-Coquard, I.; Trask, P.; Lin, K.; Schuth, E.; Vaze, A.; Choi, Y.; Marsters, J.C.; Maslyar, D.J.; Lemahieu, V.; Wang, Y.; Humke, E.W.; Liu, J.F. Anti-NaPi2b antibody-drug conjugate lifastuzumab vedotin (DNIB0600A) compared with pegylated liposomal doxorubicin in patients with platinum-resistant ovarian cancer in a randomized, open-label, phase II study. Ann. Oncol., 2018, 29(4), 917-923.
[116]
Lopes dos Santos, M.; Yeda, F.P.; Tsuruta, L.R.; Horta, B.B.; Pimenta, A.A., Jr; Degaki, T.L.; Soares, I.C.; Tuma, M.C.; Okamoto, O.K.; Alves, V.A.; Old, L.J.; Ritter, G.; Moro, A.M. Rebmab200, a humanized monoclonal antibody targeting the sodium phosphate transporter NaPi2b displays strong immune mediated cytotoxicity against cancer: a novel reagent for targeted antibody therapy of cancer. PLoS One, 2013, 8(7)e70332
[117]
Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer, 2012, 12(4), 252-264.
[118]
Dong, H.; Strome, S.E.; Salomao, D.R.; Tamura, H.; Hirano, F.; Flies, D.B.; Roche, P.C.; Lu, J.; Zhu, G.; Tamada, K.; Lennon, V.A.; Celis, E.; Chen, L. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med., 2002, 8(8), 793-800.
[119]
Drerup, J.M.; Liu, Y.; Padron, A.S.; Murthy, K.; Hurez, V.; Zhang, B.; Curiel, T.J. Immunotherapy for ovarian cancer. Curr. Treat. Options Oncol., 2015, 16(1), 317.
[120]
Bose, C.K. Immune checkpoint blockers and ovarian cancer. Indian J. Med. Paediatr. Oncol., 2017, 38(2), 182-189.
[121]
Syn, N.L.; Teng, M.W.L.; Mok, T.S.K.; Soo, R.A. De-novo and acquired resistance to immune checkpoint targeting. Lancet Oncol., 2017, 18(12), e731-e741.
[122]
Hu, Z.; Gao, S.; Gao, J.; Hou, R.; Liu, C.; Liu, J.; Li, B.; Liu, D.; Zhang, S.; Lin, B. Elevated levels of Lewis y and integrin alpha5beta1 correlate with chemotherapeutic drug resistance in epithelial ovarian carcinoma. Int. J. Mol. Sci., 2012, 13(12), 15588-15600.
[123]
Wang, Y.; Liu, J.; Lin, B.; Wang, C.; Li, Q.; Liu, S.; Yan, L.; Zhang, S.; Iwamori, M. Study on the expression and clinical significances of lewis y antigen and integrin alphav, beta3 in epithelial ovarian tumors. Int. J. Mol. Sci., 2011, 12(6), 3409-3421.
[124]
Szender, J.B.; Papanicolau-Sengos, A.; Eng, K.H.; Miliotto, A.J.; Lugade, A.A.; Gnjatic, S.; Matsuzaki, J.; Morrison, C.D.; Odunsi, K. NY-ESO-1 expression predicts an aggressive phenotype of ovarian cancer. Gynecol. Oncol., 2017, 145(3), 420-425.
[125]
Hodge, J.W.; Tsang, K.Y.; Poole, D.J.; Schlom, J. General keynote: vaccine strategies for the therapy of ovarian cancer. Gynecol. Oncol., 2003, 881 Pt 2 S97-104; discussion. , S110-3.
[126]
Maeda, D.; Ota, S.; Takazawa, Y.; Aburatani, H.; Nakagawa, S.; Yano, T.; Taketani, Y.; Kodama, T.; Fukayama, M. Glypican-3 expression in clear cell adenocarcinoma of the ovary. Mod. Pathol., 2009, 22(6), 824-832.
[127]
Zwick, E.; Bange, J.; Ullrich, A. Receptor tyrosine kinase signalling as a target for cancer intervention strategies. Endocr. Relat. Cancer, 2001, 8(3), 161-173.
[128]
Lemmon, M.A.; Schlessinger, J. Cell signaling by receptor tyrosine kinases. Cell, 2010, 141(7), 1117-1134.
[129]
Brahmer, J.R.; Tykodi, S.S.; Chow, L.Q.; Hwu, W.J.; Topalian, S.L.; Hwu, P.; Drake, C.G.; Camacho, L.H.; Kauh, J.; Odunsi, K.; Pitot, H.C.; Hamid, O.; Bhatia, S.; Martins, R.; Eaton, K.; Chen, S.; Salay, T.M.; Alaparthy, S.; Grosso, J.F.; Korman, A.J.; Parker, S.M.; Agrawal, S.; Goldberg, S.M.; Pardoll, D.M.; Gupta, A.; Wigginton, J.M. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med., 2012, 366(26), 2455-2465.
[130]
Pfisterer, J.; du Bois, A.; Sehouli, J.; Loibl, S.; Reinartz, S.; Reuss, A.; Canzler, U.; Belau, A.; Jackisch, C.; Kimmig, R.; Wollschlaeger, K.; Heilmann, V.; Hilpert, F. The anti-idiotypic antibody abagovomab in patients with recurrent ovarian cancer. A phase I trial of the AGO-OVAR. Ann. Oncol., 2006, 17(10), 1568-1577.
[131]
Kobayashi, M.; Sawada, K.; Kimura, T. Potential of integrin inhibitors for treating ovarian cancer: A literature review. Cancers , 2017, 9(7)E83
[132]
Odunsi, K.; Matsuzaki, J.; Karbach, J.; Neumann, A.; Mhawech-Fauceglia, P.; Miller, A.; Beck, A.; Morrison, C.D.; Ritter, G.; Godoy, H.; Lele, S.; duPont, N.; Edwards, R.; Shrikant, P.; Old, L.J.; Gnjatic, S.; Jager, E. Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc. Natl. Acad. Sci. USA, 2012, 109(15), 5797-5802.
[133]
Gulley, J.L.; Arlen, P.M.; Tsang, K.Y.; Yokokawa, J.; Palena, C.; Poole, D.J.; Remondo, C.; Cereda, V.; Jones, J.L.; Pazdur, M.P.; Higgins, J.P.; Hodge, J.W.; Steinberg, S.M.; Kotz, H.; Dahut, W.L.; Schlom, J. Pilot study of vaccination with recombinant CEA-MUC-1-TRICOM poxviral-based vaccines in patients with metastatic carcinoma. Clin. Cancer Res., 2008, 14(10), 3060-3069.
[134]
Suzuki, S.; Shibata, K.; Kikkawa, F.; Nakatsura, T. Significant clinical response of progressive recurrent ovarian clear cell carcinoma to glypican-3-derived peptide vaccine therapy: Two case reports. Hum. Vaccin. Immunother., 2014, 10(2), 338-343.
[135]
Jayson, G.C.; Kohn, E.C.; Kitchener, H.C.; Ledermann, J.A. Ovarian cancer. Lancet, 2014, 384(9951), 1376-1388.
[136]
Li, F.; Emmerton, K.K.; Jonas, M.; Zhang, X.; Miyamoto, J.B.; Setter, J.R.; Nicholas, N.D.; Okeley, N.M.; Lyon, R.P.; Benjamin, D.R.; Law, C.L. Intracellular released payload influences potency and bystander-killing effects of antibody-drug conjugates in preclinical models. Cancer Res., 2016, 76(9), 2710-2719.
[137]
Staudacher, A.H.; Brown, M.P. Antibody drug conjugates and bystander killing: is antigen-dependent internalisation required? Br. J. Cancer, 2017, 117(12), 1736-1742.
[138]
Ponte, J.F.; Ab, O.; Lanieri, L.; Lee, J.; Coccia, J.; Bartle, L.M.; Themeles, M.; Zhou, Y.; Pinkas, J.; Ruiz-Soto, R. Mirvetuximab soravtansine (IMGN853), a folate receptor alpha-targeting antibody-drug conjugate, potentiates the activity of standard of care therapeutics in ovarian cancer models. Neoplasia, 2016, 18(12), 775-784.
[139]
Naumann, R.W.; Coleman, R.L.; Burger, R.A.; Sausville, E.A.; Kutarska, E.; Ghamande, S.A.; Gabrail, N.Y.; Depasquale, S.E.; Nowara, E.; Gilbert, L.; Gersh, R.H.; Teneriello, M.G.; Harb, W.A.; Konstantinopoulos, P.A.; Penson, R.T.; Symanowski, J.T.; Lovejoy, C.D.; Leamon, C.P.; Morgenstern, D.E.; Messmann, R.A. PRECEDENT: A randomized phase II trial comparing vintafolide (EC145) and pegylated liposomal doxorubicin (PLD) in combination versus PLD alone in patients with platinum-resistant ovarian cancer. J. Clin. Oncol., 2013, 31(35), 4400-4406.
[140]
Martin, L.P.; Konner, J.A.; Moore, K.N.; Seward, S.M.; Matulonis, U.A.; Perez, R.P.; Su, Y.; Berkenblit, A.; Ruiz-Soto, R.; Birrer, M.J. Characterization of folate receptor alpha (FRalpha) expression in archival tumor and biopsy samples from relapsed epithelial ovarian cancer patients: A phase I expansion study of the FRalpha-targeting antibody-drug conjugate mirvetuximab soravtansine. Gynecol. Oncol., 2017, 147(2), 402-407.
[141]
Quici, S.; Casoni, A.; Foschi, F.; Armelao, L.; Bottaro, G.; Seraglia, R.; Bolzati, C.; Salvarese, N.; Carpanese, D.; Rosato, A. Folic acid-conjugated europium complexes as luminescent probes for selective targeting of cancer cells. J. Med. Chem., 2015, 58(4), 2003-2014.
[142]
Sun, Y.; Shi, T.; Zhou, L.; Zhou, Y.; Sun, B.; Liu, X. Folate-decorated and NIR-activated nanoparticles based on platinum(IV) prodrugs for targeted therapy of ovarian cancer. J. Microencapsul., 2017, 34(7), 675-686.
[143]
Desale, S.S.; Soni, K.S.; Romanova, S.; Cohen, S.M.; Bronich, T.K. Targeted delivery of platinum-taxane combination therapy in ovarian cancer. J. Control. Release, 2015, 220(Pt B). , 651-659.
[144]
He, Z.Y.; Wei, X.W.; Luo, M.; Luo, S.T.; Yang, Y.; Yu, Y.Y.; Chen, Y.; Ma, C.C.; Liang, X.; Guo, F.C.; Ye, T.H.; Shi, H.S.; Shen, G.B.; Wang, W.; Gong, F.M.; He, G.; Yang, L.; Zhao, X.; Song, X.R.; Wei, Y.Q. Folate-linked lipoplexes for short hairpin RNA targeting claudin-3 delivery in ovarian cancer xenografts. J. Control. Release, 2013, 172(3), 679-689.
[145]
Luong, D.; Kesharwani, P.; Alsaab, H.O.; Sau, S.; Padhye, S.; Sarkar, F.H.; Iyer, A.K. Folic acid conjugated polymeric micelles loaded with a curcumin difluorinated analog for targeting cervical and ovarian cancers. Colloids and surfaces. B Biointerfaces, 2017, 157, 490-502.
[146]
Luo, T.; Sun, J.; Zhu, S.; He, J.; Hao, L.; Xiao, L.; Zhu, Y.; Wang, Q.; Pan, X.; Wang, Z.; Chang, S. Ultrasound-mediated destruction of oxygen and paclitaxel loaded dual-targeting microbubbles for intraperitoneal treatment of ovarian cancer xenografts. Cancer Lett., 2017, 391, 1-11.
[147]
Modi, D.A.; Sunoqrot, S.; Bugno, J.; Lantvit, D.D.; Hong, S.; Burdette, J.E. Targeting of follicle stimulating hormone peptide-conjugated dendrimers to ovarian cancer cells. Nanoscale, 2014, 6(5), 2812-2820.
[148]
Hong, S.; Zhang, X.; Chen, J.; Zhou, J.; Zheng, Y.; Xu, C. Targeted gene silencing using a follicle-stimulating hormone peptide-conjugated nanoparticle system improves its specificity and efficacy in ovarian clear cell carcinoma in vitro. J. Ovarian Res., 2013, 6(1), 80.
[149]
Zhang, M.; Zhang, M.; Wang, J.; Cai, Q.; Zhao, R.; Yu, Y.; Tai, H.; Zhang, X.; Xu, C. Retro-inverso follicle-stimulating hormone peptide-mediated polyethylenimine complexes for targeted ovarian cancer gene therapy. Drug Deliv., 2018, 25(1), 995-1003.
[150]
Zhang, X.Y.; Chen, J.; Zheng, Y.F.; Gao, X.L.; Kang, Y.; Liu, J.C.; Cheng, M.J.; Sun, H.; Xu, C.J. Follicle-stimulating hormone peptide can facilitate paclitaxel nanoparticles to target ovarian carcinoma in vivo. Cancer Res., 2009, 69(16), 6506-6514.
[151]
Milane, L.; Duan, Z.; Amiji, M. Development of EGFR-targeted polymer blend nanocarriers for combination paclitaxel/lonidamine delivery to treat multi-drug resistance in human breast and ovarian tumor cells. Mol. Pharm., 2011, 8(1), 185-203.
[152]
Talekar, M.; Ganta, S.; Singh, A.; Amiji, M.; Kendall, J.; Denny, W.A.; Garg, S. Phosphatidylinositol 3-kinase inhibitor (PIK75) containing surface functionalized nanoemulsion for enhanced drug delivery, cytotoxicity and pro-apoptotic activity in ovarian cancer cells. Pharm. Res., 2012, 29(10), 2874-2886.
[153]
Ganta, S.; Singh, A.; Patel, N.R.; Cacaccio, J.; Rawal, Y.H.; Davis, B.J.; Amiji, M.M.; Coleman, T.P. Development of EGFR-targeted nanoemulsion for imaging and novel platinum therapy of ovarian cancer. Pharm. Res., 2014, 31(9), 2490-2502.
[154]
Uusi-Kerttula, H.; Legut, M.; Davies, J.; Jones, R.; Hudson, E.; Hanna, L.; Stanton, R.J.; Chester, J.D.; Parker, A.L. Incorporation of peptides targeting EGFR and FGFR1 into the adenoviral fiber knob domain and their evaluation as targeted cancer therapies. Hum. Gene Ther., 2015, 26(5), 320-329.
[155]
Chen, J.; Ouyang, J.; Chen, Q.; Deng, C.; Meng, F.; Zhang, J.; Cheng, R.; Lan, Q.; Zhong, Z. EGFR and CD44 dual-targeted multifunctional hyaluronic acid nanogels boost protein delivery to ovarian and breast cancers in vitro and in vivo. ACS Appl. Mater. Interfaces, 2017, 9(28), 24140-24147.
[156]
Zou, Y.; Xia, Y.; Meng, F.; Zhang, J.; Zhong, Z. GE11-directed functional polymersomal doxorubicin as an advanced alternative to clinical liposomal formulation for ovarian cancer treatment. Mol. Pharm., 2018, 15(9), 3664-3671.
[157]
Abu-Yousif, A.O.; Moor, A.C.; Zheng, X.; Savellano, M.D.; Yu, W.; Selbo, P.K.; Hasan, T. Epidermal growth factor receptor-targeted photosensitizer selectively inhibits EGFR signaling and induces targeted phototoxicity in ovarian cancer cells. Cancer Lett., 2012, 321(2), 120-127.
[158]
Mir, Y.; Elrington, S.A.; Hasan, T. A new nanoconstruct for epidermal growth factor receptor-targeted photo-immunotherapy of ovarian cancer. Nanomedicine , 2013, 9(7), 1114-1122.
[159]
Wang, Y.; Zhou, J.; Qiu, L.; Wang, X.; Chen, L.; Liu, T.; Di, W. Cisplatin-alginate conjugate liposomes for targeted delivery to EGFR-positive ovarian cancer cells. Biomaterials, 2014, 35(14), 4297-4309.
[160]
Jiang, J.; Dong, L.; Wang, L.; Wang, L.; Zhang, J.; Chen, F.; Zhang, X.; Huang, M.; Li, S.; Ma, W.; Xu, Q.; Huang, C.; Fang, J.; Wang, C. HER2-targeted antibody drug conjugates for ovarian cancer therapy. Eur. J. Pharm. Sci., 2016, 93, 274-286.
[161]
Gianolio, D.A.; Rouleau, C.; Bauta, W.E.; Lovett, D.; Cantrell, W.R., Jr; Recio, A., 3rd; Wolstenholme-Hogg, P.; Busch, M.; Pan, P.; Stefano, J.E.; Kramer, H.M.; Goebel, J.; Krumbholz, R.D.; Roth, S.; Schmid, S.M.; Teicher, B.A. Targeting HER2-positive cancer with dolastatin 15 derivatives conjugated to trastuzumab, novel antibody-drug conjugates. Cancer Chemother. Pharmacol., 2012, 70(3), 439-449.
[162]
Sato, K.; Hanaoka, H.; Watanabe, R.; Nakajima, T.; Choyke, P.L.; Kobayashi, H. Near infrared photoimmunotherapy in the treatment of disseminated peritoneal ovarian cancer. Mol. Cancer Ther., 2015, 14(1), 141-150.
[163]
Yao, Y.; Yu, L.; Su, X.; Wang, Y.; Li, W.; Wu, Y.; Cheng, X.; Zhang, H.; Wei, X.; Chen, H.; Zhang, R.; Gou, L.; Chen, X.; Xie, Y.; Zhang, B.; Zhang, Y.; Yang, J.; Wei, Y. Synthesis, characterization and targeting chemotherapy for ovarian cancer of trastuzumab-SN-38 conjugates. J. Control. Release., 2015, 220(Pt A). , 5-17.
[164]
Cirstoiu-Hapca, A.; Buchegger, F.; Lange, N.; Bossy, L.; Gurny, R.; Delie, F. Benefit of anti-HER2-coated paclitaxel-loaded immuno-nanoparticles in the treatment of disseminated ovarian cancer: Therapeutic efficacy and biodistribution in mice. J. Control. Release, 2010, 144(3), 324-331.
[165]
Li, J.; Cheng, D.; Yin, T.; Chen, W.; Lin, Y.; Chen, J.; Li, R.; Shuai, X. Copolymer of poly(ethylene glycol) and poly(L-lysine) grafting polyethylenimine through a reducible disulfide linkage for siRNA delivery. Nanoscale, 2014, 6(3), 1732-1740.
[166]
Jiang, D.; Im, H.J.; Sun, H.; Valdovinos, H.F.; England, C.G.; Ehlerding, E.B.; Nickles, R.J.; Lee, D.S.; Cho, S.Y.; Huang, P.; Cai, W. Radiolabeled pertuzumab for imaging of human epidermal growth factor receptor 2 expression in ovarian cancer. Eur. J. Nucl. Med. Mol. Imaging, 2017, 44(8), 1296-1305.
[167]
Liu, P.; Boyle, A.J.; Lu, Y.; Adams, J.; Chi, Y.; Reilly, R.M.; Winnik, M.A. Metal-chelating polymers (MCPs) with zwitterionic pendant groups complexed to trastuzumab exhibit decreased liver accumulation compared to polyanionic MCP immunoconjugates. Biomacromolecules, 2015, 16(11), 3613-3623.
[168]
Govindarajan, S.; Sivakumar, J.; Garimidi, P.; Rangaraj, N.; Kumar, J.M.; Rao, N.M.; Gopal, V. Targeting human epidermal growth factor receptor 2 by a cell-penetrating peptide-affibody bioconjugate. Biomaterials, 2012, 33(8), 2570-2582.
[169]
El-Dakdouki, M.H.; Pure, E.; Huang, X. Development of drug loaded nanoparticles for tumor targeting. Part 1: Synthesis, characterization, and biological evaluation in 2D cell cultures. Nanoscale, 2013, 5(9), 3895-3903.
[170]
Yang, X.; Iyer, A.K.; Singh, A.; Choy, E.; Hornicek, F.J.; Amiji, M.M.; Duan, Z. MDR1 siRNA loaded hyaluronic acid-based CD44 targeted nanoparticle systems circumvent paclitaxel resistance in ovarian cancer. Sci. Rep., 2015, 5, 8509.
[171]
Kim, J.E.; Park, Y.J. Paclitaxel-loaded hyaluronan solid nanoemulsions for enhanced treatment efficacy in ovarian cancer. Int. J. Nanomed, 2017, 12, 645-658.
[172]
Zhou, H.; Xu, H.; Li, X.; Lv, Y.; Ma, T.; Guo, S.; Huang, Z.; Wang, X.; Xu, P. Dual targeting hyaluronic acid - RGD mesoporous silica coated gold nanorods for chemo-photothermal cancer therapy. Mater. Sci. Eng. C Mater. Biol. Appl, 2017, 81, 261-270.
[173]
Chang, S.; Guo, J.; Sun, J.; Zhu, S.; Yan, Y.; Zhu, Y.; Li, M.; Wang, Z.; Xu, R.X. Targeted microbubbles for ultrasound mediated gene transfection and apoptosis induction in ovarian cancer cells. Ultrason. Sonochem., 2013, 20(1), 171-179.
[174]
Nukolova, N.V.; Oberoi, H.S.; Zhao, Y.; Chekhonin, V.P.; Kabanov, A.V.; Bronich, T.K. LHRH-targeted nanogels as a delivery system for cisplatin to ovarian cancer. Mol. Pharm., 2013, 10(10), 3913-3921.
[175]
Akhtar, S.; Benter, I.F. Nonviral delivery of synthetic siRNAs in vivo. J. Clin. Invest., 2007, 117(12), 3623-3632.
[176]
He, Z.Y.; Deng, F.; Wei, X.W.; Ma, C.C.; Luo, M.; Zhang, P.; Sang, Y.X.; Liang, X.; Liu, L.; Qin, H.X.; Shen, Y.L.; Liu, T.; Liu, Y.T.; Wang, W.; Wen, Y.J.; Zhao, X.; Zhang, X.N.; Qian, Z.Y.; Wei, Y.Q. Ovarian cancer treatment with a tumor-targeting and gene expression-controllable lipoplex. Sci. Rep., 2016, 6, 23764.
[177]
Zhu, X.; Cai, H.; Zhao, L.; Ning, L.; Lang, J. CAR-T cell therapy in ovarian cancer: from the bench to the bedside. Oncotarget, 2017, 8(38), 64607-64621.
[178]
Wickham, T.J. Targeting adenovirus. Gene Ther., 2000, 7(2), 110-114.
[179]
Krasnykh, V.; Dmitriev, I.; Navarro, J.G.; Belousova, N.; Kashentseva, E.; Xiang, J.; Douglas, J.T.; Curiel, D.T. Advanced generation adenoviral vectors possess augmented gene transfer efficiency based upon coxsackie adenovirus receptor-independent cellular entry capacity. Cancer Res., 2000, 60(24), 6784-6787.
[180]
Kanerva, A.; Zinn, K.R.; Chaudhuri, T.R.; Lam, J.T.; Suzuki, K.; Uil, T.G.; Hakkarainen, T.; Bauerschmitz, G.J.; Wang, M.; Liu, B.; Cao, Z.; Alvarez, R.D.; Curiel, D.T.; Hemminki, A. Enhanced therapeutic efficacy for ovarian cancer with a serotype 3 receptor-targeted oncolytic adenovirus. Mol. Ther., 2003, 8(3), 449-458.
[181]
Bartnik, A.; Nirmal, A.J.; Yang, S.Y. Peptide vaccine therapy in colorectal cancer. Vaccines , 2012, 1(1), 1-16.
[182]
Yamada, A.; Sasada, T.; Noguchi, M.; Itoh, K. Next-generation peptide vaccines for advanced cancer. Cancer Sci., 2013, 104(1), 15-21.


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Article Details

VOLUME: 19
ISSUE: 6
Year: 2019
Page: [449 - 467]
Pages: 19
DOI: 10.2174/1568009618666181010091246
Price: $58

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