In Vitro and In Vivo evaluation of a novel folate-targeted theranostic nanoemulsion of docetaxel for imaging and improved anticancer activity against ovarian cancers

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.
   PubMed Web of Science ®Google Scholar
• Parker SL, Tong T, Bolden S, Wingo PA. Cancer statistics, 1996. CA Cancer J Clin. 1996;46:5–27.
   PubMed Web of Science ®Google Scholar
• Ganta S, Talekar M, Singh A, Coleman TP, Amiji MM. Nanoemulsions in Translational Research-Opportunities and Challenges in Targeted Cancer Therapy. AAPS Pharm Sci Tech. 2014;15:694–708.
   PubMed Web of Science ®Google Scholar
• Ganta S, Singh A, Patel NR, Cacaccio J, Rawal YH, Davis BJ, Amiji MM, Coleman TP. Development of EGFR-Targeted Nanoemulsion for Imaging and Novel Platinum Therapy of Ovarian Cancer. Pharm Res. 2014;31:2490–502.
   PubMed Web of Science ®Google Scholar
• Ganta S, Singh A, Kulkarni P, Keeler AW, Piroyan A, Sawant RR, Patel NR, Davis B, Ferris C, O'Neal S, et al. EGFR Targeted Theranostic Nanoemulsion for Image-Guided Ovarian Cancer Therapy. Pharm Res. 2015;32:2753–63.
   PubMed Web of Science ®Google Scholar
• Goren D, Horowitz AT, Tzemach D, Tarshish M, Zalipsky S, Gabizon A. Nuclear delivery of doxorubicin via folate-targeted liposomes with bypass of multidrug-resistance efflux pump. Clin Cancer Res. 2000;6:1949–57.
   PubMed Web of Science ®Google Scholar
• Gabizon A, Tzemach D, Gorin J, Mak L, Amitay Y, Shmeeda H, Zalipsky S. Improved therapeutic activity of folate-targeted liposomal doxorubicin in folate receptor-expressing tumor models. Cancer Chemother Pharmacol. 2010;66:43–52.
   PubMed Web of Science ®Google Scholar
• Shmeeda H, Mak L, Tzemach D, Astrahan P, Tarshish M, Gabizon A. Intracellular uptake and intracavitary targeting of folate-conjugated liposomes in a mouse lymphoma model with up-regulated folate receptors. Mol Cancer Ther. 2006;5:818–24.
   PubMed Web of Science ®Google Scholar
• Kim D, Gao ZG, Lee ES, Bae YH. In vivo evaluation of doxorubicin-loaded polymeric micelles targeting folate receptors and early endosomal pH in drug-resistant ovarian cancer. Mol Pharm. 2009;6:1353–62.
   PubMed Web of Science ®Google Scholar
• Kim D, Lee ES, Oh KT, Gao ZG, Bae YH. Doxorubicin-loaded polymeric micelle overcomes multidrug resistance of cancer by double-targeting folate receptor and early endosomal pH. Small. 2008;4:2043–50.
   PubMed Web of Science ®Google Scholar
• Ganta S, Singh A, Rawal Y, Cacaccio J, Patel NR, Kulkarni P, Ferris CF, Amiji MM, Coleman TP. Formulation development of a novel targeted theranostic nanoemulsion of docetaxel to overcome multidrug resistance in ovarian cancer. Drug Deliv. 2014:1–13.
   Google Scholar
• Patel NR, Piroyan A, Nack AH, Galati CA, McHugh M, Orosz S, Keeler AW, O'Neal S, Zamboni WC, Davis B, et al. Design, Synthesis, and Characterization of Folate-Targeted Platinum-Loaded Theranostic Nanoemulsions for Therapy and Imaging of Ovarian Cancer. Mol Pharm. 2016;13:1996–2009.
   PubMed Web of Science ®Google Scholar
• Swanson SD, Kukowska-Latallo JF, Patri AK, Chen C, Ge S, Cao Z, Kotlyar A, East AT, Baker JR. Targeted gadolinium-loaded dendrimer nanoparticles for tumor-specific magnetic resonance contrast enhancement. Int J Nanomedicine. 2008;3:201–10.
   PubMed Web of Science ®Google Scholar
• Fisher RE, Siegel BA, Edell SL, Oyesiku NM, Morgenstern DE, Messmann RA, Amato RJ. Exploratory study of 99 mTc-EC20 imaging for identifying patients with folate receptor-positive solid tumors. J Nucl Med. 2008;49:899–906.
   PubMed Web of Science ®Google Scholar
• Leamon CP, Low PS. Delivery of macromolecules into living cells: a method that exploits folate receptor endocytosis. Proc Natl Acad Sci USA. 1991;88:5572–6.
   PubMed Web of Science ®Google Scholar
• Bandara NA, Hansen MJ, Low PS. Effect of receptor occupancy on folate receptor internalization. Mol Pharm. 2014;11:1007–13.
   PubMedGoogle Scholar
• Tiwari SB, Tan Y, Amiji M. Preparation and In Vitro Characterization of Multifunctional Nanoemulsions for Simultaneous MR Imaging and Targeted Drug Delivery. J Biomed Nanotechnol. 2006;2:1–8.
   Web of Science ®Google Scholar
• Connolly DC, Bao R, Nikitin AY, Stephens KC, Poole TW, Hua X, Harris SS, Vanderhyden BC, Hamilton TC. Female mice chimeric for expression of the simian virus 40 TAg under control of the MISIIR promoter develop epithelial ovarian cancer. Cancer Res. 2003;63:1389–97.
   PubMed Web of Science ®Google Scholar
• Hensley H, Quinn BA, Wolf RL, Litwin SL, Mabuchi S, Williams SJ, Williams C, Hamilton TC, Connolly DC. Magnetic resonance imaging for detection and determination of tumor volume in a genetically engineered mouse model of ovarian cancer. Cancer Biol Ther. 2007;6:1717–25.
   PubMed Web of Science ®Google Scholar
• Mabuchi S, Altomare DA, Connolly DC, Klein-Szanto A, Litwin S, Hoelzle MK, Hensley HH, Hamilton TC, Testa JR. RAD001 (Everolimus) delays tumor onset and progression in a transgenic mouse model of ovarian cancer. Cancer Res. 2007;67:2408–13.
   PubMed Web of Science ®Google Scholar
• Reddy J, Abburi C, Hofland H, Howard S, Vlahov I, Wils P, Leamon C. Folate-targeted, cationic liposome-mediated gene transfer into disseminated peritoneal tumors. Gene Therapy. 2002:9.
   Web of Science ®Google Scholar
• Gabizon A, Horowitz AT, Goren D, Tzemach D, Mandelbaum-Shavit F, Qazen MM, Zalipsky S. Targeting folate receptor with folate linked to extremities of poly (ethylene glycol)-grafted liposomes: in vitro studies. Bioconjug Chem. 1999;10:289–98.
   PubMed Web of Science ®Google Scholar
• Wang S, Lee RJ, Mathias CJ, Green MA, Low PS. Synthesis, purification, and tumor cell uptake of 67 Ga-deferoxamine-folate, a potential radiopharmaceutical for tumor imaging. Bioconjug Chem. 1996;7:56–62.
   PubMed Web of Science ®Google Scholar
• Garbuzenko O, Zalipsky S, Qazen M, Barenholz Y. Electrostatics of PEGylated micelles and liposomes containing charged and neutral lipopolymers. Langmuir. 2005;21:2560–8.
   PubMed Web of Science ®Google Scholar
• Reddy JA, Xu L-C, Parker N, Vetzel M, Leamon CP. Preclinical Evaluation of 99 mTc-EC20 for Imaging Folate Receptor–Positive Tumors. J Nucl Med. 2004;45:857–66.
   PubMed Web of Science ®Google Scholar
• Chu KS, Hasan W, Rawal S, Walsh MD, Enlow EM, Luft JC, Bridges AS, Kuijer JL, Napier ME, Zamboni WC, et al. Plasma, tumor and tissue pharmacokinetics of Docetaxel delivered via nanoparticles of different sizes and shapes in mice bearing SKOV-3 human ovarian carcinoma xenograft. Nanomed: Nanotechnol, Biol, Med. 2013;9:686–93.
   PubMed Web of Science ®Google Scholar
• Luyckx M, Votino R, Squifflet JL, Baurain JF. Profile of vintafolide (EC145) and its use in the treatment of platinum-resistant ovarian cancer. Int J Womens Health. 2014;6:351–8.
   PubMedGoogle Scholar
• Vergote IB, Marth C, Coleman RL. Role of the folate receptor in ovarian cancer treatment: evidence, mechanism, and clinical implications. Cancer Metastasis Rev. 2015;34:41–52.
   PubMed Web of Science ®Google Scholar
• Wen Y, Graybill WS, Previs RA, Hu W, Ivan C, Mangala LS, Zand B, Nick AM, Jennings NB, Dalton HJ, et al. Immunotherapy targeting folate receptor induces cell death associated with autophagy in ovarian cancer. Clin Cancer Res. 2015;21:448–59.
   PubMed Web of Science ®Google Scholar
• Kobel M, Madore J, Ramus SJ, Clarke BA, Pharoah PD, Deen S, Bowtell DD, Odunsi K, Menon U, Morrison C, et al. Evidence for a time-dependent association between FOLR1 expression and survival from ovarian carcinoma: implications for clinical testing. An Ovarian Tumour Tissue Analysis Consortium Study. Br J Cancer. 2014;111:2297–307.
   Google Scholar
• Brunelle JK, Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci. 2009;122:437–41.
   PubMed Web of Science ®Google Scholar
• Gligorov J, Lotz JP. Preclinical pharmacology of the taxanes: implications of the differences. Oncologist. 2004;9(Suppl 2).3–8.
   PubMed Web of Science ®Google Scholar
• Parker N, Turk MJ, Westrick E, Lewis JD, Low PS, Leamon CP. Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay. Anal Biochem. 2005;338:284–93.
   PubMed Web of Science ®Google Scholar
• Sato S, Itamochi H. Profile of farletuzumab and its potential in the treatment of solid tumors. Onco Targets Ther. 2016;9:1181–8.
   PubMed Web of Science ®Google Scholar
• Vergote I, Leamon CP. Vintafolide: a novel targeted therapy for the treatment of folate receptor expressing tumors. Ther Adv Med Oncol. 2015;7:206–18.
   PubMed Web of Science ®Google Scholar
• Leamon CP, Reddy JA, Dorton R, Bloomfield A, Emsweller K, Parker N, Westrick E. Impact of high and low folate diets on tissue folate receptor levels and antitumor responses toward folate-drug conjugates. J Pharmacol Exp Ther. 2008;327:918–25.
   PubMed Web of Science ®Google Scholar
• Li T, Gendelman HE, Zhang G, Puligujja P, McMillan JM, Bronich TK, Edagwa B, Liu XM, Boska MD. Magnetic resonance imaging of folic acid-coated magnetite nanoparticles reflects tissue biodistribution of long-acting antiretroviral therapy. Int J Nanomed. 2015;10:3779–90.
   PubMed Web of Science ®Google Scholar
• Ganta S, Singh A, Rawal Y, Cacaccio J, Patel NR, Kulkarni P, Ferris CF, Amiji MM, Coleman TP. Formulation development of a novel targeted theranostic nanoemulsion of docetaxel to overcome multidrug resistance in ovarian cancer. Drug delivery. 2014:1–13.
   Google Scholar
• Hensley HH, Roder NA, O'Brien SW, Bickel LE, Xiao F, Litwin S, Connolly DC. Combined in vivo molecular and anatomic imaging for detection of ovarian carcinoma-associated protease activity and integrin expression in mice. Neoplasia. 2012;14:451–62.
   PubMed Web of Science ®Google Scholar
• Liu M, Mor G, Cheng H, Xiang X, Hui P, Rutherford T, Yin G, Rimm DL, Holmberg J, Alvero A, et al. High frequency of putative ovarian cancer stem cells with CD44/CK19 coexpression is associated with decreased progression-free intervals in patients with recurrent epithelial ovarian cancer. Reprod Sci. 2013;20:605–15.
   PubMed Web of Science ®Google Scholar