Lipid-Based Self-Microemulsion of Niclosamide Achieved Enhanced Oral Delivery and Anti-Tumor Efficacy in Orthotopic Patient-Derived Xenograft of Hepatocellular Carcinoma in Mice

References

• Chen B, Wei W, Ma L., et al. Computational discovery of niclosamide ethanolamine, a repurposed drug candidate that reduces growth of hepatocellular carcinoma cells in vitro and in mice by inhibiting cell division cycle 37 signaling. Gastroenterology. 2017;152(8):2022–2036. doi:10.1053/j.gastro.2017.02.039
   PubMed Web of Science ®Google Scholar
• Corbel MJ, Das RG, Lei D, et al. WHO working group on revision of the manual of laboratory methods for testing dtp vaccines-report of two meetings held on 20-21 July 2006 and 28-30 march 2007, Geneva, Switzerland. Vaccine. 2008;26(16):1913–1921. doi:10.1016/j.vaccine.2008.02.013
   PubMed Web of Science ®Google Scholar
• Pearson RD, Hewlett EL. Niclosamide therapy for tapeworm infections. Ann Intern Med. 1985;102(4):550–551. doi:10.7326/0003-4819-102-4-550
   PubMed Web of Science ®Google Scholar
• Chen W, Mook RA, Premont RT, et al. Niclosamide: beyond an antihelminthic drug. Cell Signal. 2018;41:89–96. doi:10.1016/j.cellsig.2017.04.001
   PubMed Web of Science ®Google Scholar
• Shi L, Zheng H, Hu W, et al. Niclosamide inhibition of STAT3 synergizes with erlotinib in human colon cancer. Onco Targets Ther. 2017;10:1767–1776. doi:10.2147/OTT.S129449
   PubMed Web of Science ®Google Scholar
• Schweizer MT, Haugk K, McKiernan JS, et al. A phase I study of niclosamide in combination with enzalutamide in men with castration-resistant prostate cancer. PLoS One. 2018;13(6):e0198389. doi:10.1371/journal.pone.0198389
   PubMed Web of Science ®Google Scholar
• Liu C, Lou W, Armstrong C, et al. Niclosamide suppresses cell migration and invasion in enzalutamide resistant prostate cancer cells via Stat3-AR axis inhibition. Prostate. 2015;75(13):1341–1353. doi:10.1002/pros.23015
   PubMed Web of Science ®Google Scholar
• Werle M. Polymeric and low molecular mass efflux pump inhibitors for oral drug delivery. J Pharm Sci. 2008;97(1):60–70. doi:10.1002/jps.21090
   PubMed Web of Science ®Google Scholar
• Werle M. Natural and synthetic polymers as inhibitors of drug efflux pumps. Pharm Res. 2008;25(3):500–511. doi:10.1007/s11095-007-9347-8
   PubMed Web of Science ®Google Scholar
• Shen H, Zhong M. Preparation and evaluation of self-microemulsifying drug delivery systems (SMEDDS) containing atorvastatin. J Pharm Pharmacol. 2006;58(9):1183–1191. doi:10.1211/jpp.58.9.0004
   PubMed Web of Science ®Google Scholar
• Koolen SL, Oostendorp RL, Beijnen JH, et al. Population pharmacokinetics of intravenously and orally administered docetaxel with or without co-administration of ritonavir in patients with advanced cancer. Br J Clin Pharmacol. 2010;69(5):465–474. doi:10.1111/j.1365-2125.2010.03621.x
   PubMed Web of Science ®Google Scholar
• Andre T, Meyerhardt J, Iveson T, et al. Effect of duration of adjuvant chemotherapy for patients with stage III colon cancer (IDEA collaboration): final results from a prospective, pooled analysis of six randomised, Phase 3 trials. Lancet Oncol. 2020;21(12):1620–1629. doi:10.1016/S1470-2045(20)30527-1
   PubMed Web of Science ®Google Scholar
• Liston DR, Davis M. Clinically relevant concentrations of anticancer drugs: a guide for nonclinical studies. Clin Cancer Res. 2017;23(14):3489–3498. doi:10.1158/1078-0432.CCR-16-3083
   PubMed Web of Science ®Google Scholar
• Di Maio M, Perrone F, Chiodini P, et al. Individual patient data meta-analysis of docetaxel administered once every 3 weeks compared with once every week second-line treatment of advanced non-small-cell lung cancer. J Clin Oncol. 2007;25(11):1377–1382. doi:10.1200/JCO.2006.09.8251
   PubMed Web of Science ®Google Scholar
• Elnaggar YS, El-Massik MA, Abdallah OY. Self-nanoemulsifying drug delivery systems of tamoxifen citrate: design and optimization. Int J Pharm. 2009;380(1–2):133–141. doi:10.1016/j.ijpharm.2009.07.015
   PubMed Web of Science ®Google Scholar
• Date AA, Nagarsenker MS. Design and evaluation of self-nanoemulsifying drug delivery systems (SNEDDS) for cefpodoxime proxetil. Int J Pharm. 2007;329(1–2):166–172. doi:10.1016/j.ijpharm.2006.08.038
   PubMed Web of Science ®Google Scholar
• Zhang P, Liu Y, Feng N, et al. Preparation and evaluation of self-microemulsifying drug delivery system of oridonin. Int J Pharm. 2008;355(1–2):269–276. doi:10.1016/j.ijpharm.2007.12.026
   PubMed Web of Science ®Google Scholar
• Llera-Rojas VG, Del Real L. A, Mendoza-Muñoz N, et al. Feasibility of obtaining in situ nanocapsules through modified self-microemulsifying drug delivery systems. A new manufacturing approach for oral route administration. Drug Dev Ind Pharm. 2017;43(6):925–931. doi:10.1080/03639045.2017.1285308
   PubMed Web of Science ®Google Scholar
• Wei W, Wu S, Wang X, et al. Novel celastrol derivatives inhibit the growth of hepatocellular carcinoma patient-derived xenografts. Oncotarget. 2014;5(14):5819–5831. doi:10.18632/oncotarget.2171
   PubMedGoogle Scholar
• Liu Y, Sukumar UK, Jugniot N, et al. Inhaled gold nano-star carriers for targeted delivery of triple suicide gene therapy and therapeutic microRNAs to lung metastases: development and validation in a small animal model. Adv Ther. 2022;5(8):2200018.
   Google Scholar
• Crowe AR, Yue W. Semi-quantitative determination of protein expression using immunohistochemistry staining and analysis: an integrated protocol. Biol Protoc. 2019;9(24). doi:10.21769/BioProtoc.3465
   Web of Science ®Google Scholar
• Law AMK, Yin JXM, Castillo L, et al. Andy’s Algorithms: new automated digital image analysis pipelines for Fiji. Sci Rep. 2017;7(1):15717. doi:10.1038/s41598-017-15885-6
   PubMedGoogle Scholar
• Komesli Y, Burak Ozkaya A, Ugur Ergur B, et al. Design and development of a self-microemulsifying drug delivery system of olmesartan medoxomil for enhanced bioavailability. Drug Dev Ind Pharm. 2019;45(8):1292–1305. doi:10.1080/03639045.2019.1607868
   PubMed Web of Science ®Google Scholar
• Liu Y, Huang P, Hou X, et al. Hybrid curcumin-phospholipid complex-near-infrared dye oral drug delivery system to inhibit lung metastasis of breast cancer. Int J Nanomed. 2019;14:3311–3330. doi:10.2147/IJN.S200847
   PubMed Web of Science ®Google Scholar
• Dahan A, Hoffman A. Evaluation of a chylomicron flow blocking approach to investigate the intestinal lymphatic transport of lipophilic drugs. Eur J Pharm Sci. 2005;24(4):381–388. doi:10.1016/j.ejps.2004.12.006
   PubMed Web of Science ®Google Scholar
• Sabesin SM, Isselbacher KJ. Protein synthesis inhibition: mechanism for the production of impaired fat absorption. Science. 1965;147(3662):1149–1151. doi:10.1126/science.147.3662.1149
   PubMed Web of Science ®Google Scholar
• Tao H, Zhang Y, Zeng X, et al. Niclosamide ethanolamine-induced mild mitochondrial uncoupling improves diabetic symptoms in mice. Nat Med. 2014;20(11):1263–1269. doi:10.1038/nm.3699
   PubMed Web of Science ®Google Scholar
• Menon SS, Guruvayoorappan C, Sakthivel KM, et al. Ki-67 protein as a tumour proliferation marker. Clin Chim Acta. 2019;491:39–45. doi:10.1016/j.cca.2019.01.011
   PubMed Web of Science ®Google Scholar
• Silva F, Padín-Iruegas M, Caponio V, et al. Caspase 3 and cleaved caspase 3 expression in tumorogenesis and its correlations with prognosis in head and neck cancer: a systematic review and meta-analysis. Int J Mol Sci. 2022;23(19):11937. doi:10.3390/ijms231911937
   PubMed Web of Science ®Google Scholar
• Li Y, Li P-K, Roberts MJ, et al. Multi-targeted therapy of cancer by niclosamide: a new application for an old drug. Cancer Lett. 2014;349(1):8–14. doi:10.1016/j.canlet.2014.04.003
   PubMed Web of Science ®Google Scholar
• Singh S, Weiss A, Goodman J, et al. Niclosamide-A promising treatment for COVID-19. Br J Pharmacol. 2022;179(13):3250–3267. doi:10.1111/bph.15843
   PubMed Web of Science ®Google Scholar
• Taubes A, Nova P, Zalocusky KA, et al. Experimental and real-world evidence supporting the computational repurposing of bumetanide for APOE4-related alzheimer’s disease. Nat Aging. 2021;1(10):932–947. doi:10.1038/s43587-021-00122-7
   PubMedGoogle Scholar
• Akula S, Gurram AK, Devireddy SR. Self-microemulsifying drug delivery systems: an attractive strategy for enhanced therapeutic profile. Int Sch Res Notices. 2014;2014:964051. doi:10.1155/2014/964051
   PubMedGoogle Scholar
• O’Driscoll CM. Lipid-based formulations for intestinal lymphatic delivery. Eur J Pharm Sci. 2002;15(5):405–415. doi:10.1016/S0928-0987(02)00051-9
   PubMed Web of Science ®Google Scholar
• Porter CJ, Charman WN. Intestinal lymphatic drug transport: an update. Adv Drug Deliv Rev. 2001;50(1–2):61–80. doi:10.1016/S0169-409X(01)00151-X
   PubMed Web of Science ®Google Scholar
• Lupo N, Steinbring C, Friedl JD, et al. Impact of bile salts and a medium chain fatty acid on the physical properties of self-emulsifying drug delivery systems. Drug Dev Ind Pharm. 2021;47(1):22–35. doi:10.1080/03639045.2020.1851241
   PubMed Web of Science ®Google Scholar
• Marwah H, Garg T, Goyal AK, et al. Permeation enhancer strategies in transdermal drug delivery. Drug Deliv. 2016;23(2):564–578. doi:10.3109/10717544.2014.935532
   PubMed Web of Science ®Google Scholar
• Lind ML, Jacobsen J, Holm R, et al. Intestinal lymphatic transport of halofantrine in rats assessed using a chylomicron flow blocking approach: the influence of polysorbate 60 and 80. Eur J Pharm Sci. 2008;35(3):211–218. doi:10.1016/j.ejps.2008.07.003
   PubMed Web of Science ®Google Scholar
• Redgrave TG. Chylomicron metabolism. Biochem Soc Trans. 2004;32(Pt 1):79–82. doi:10.1042/bst0320079
   PubMedGoogle Scholar
• Bisgaier CL, Glickman RM. Intestinal synthesis, secretion, and transport of lipoproteins. Annu Rev Physiol. 1983;45(1):625–636. doi:10.1146/annurev.ph.45.030183.003205
   PubMedGoogle Scholar
• Ahmad J, Amin S, Rahman M, et al. Solid matrix based lipidic nanoparticles in oral cancer chemotherapy: applications and pharmacokinetics. Curr Drug Metab. 2015;16(8):633–644. doi:10.2174/1389200216666150812122128
   PubMed Web of Science ®Google Scholar
• Porter CJ, Trevaskis NL, Charman WN. Lipids and lipid-based formulations: optimizing the oral delivery of lipophilic drugs. Nat Rev Drug Discov. 2007;6(3):231–248. doi:10.1038/nrd2197
   PubMed Web of Science ®Google Scholar
• Park SJ, Shin J-H, Kang H, et al. Niclosamide induces mitochondria fragmentation and promotes both apoptotic and autophagic cell death. BMB Rep. 2011;44(8):517–522. doi:10.5483/BMBRep.2011.44.8.517
   PubMed Web of Science ®Google Scholar
• Peng SW, Ngo M-HT, Kuo Y-C, et al. Niclosamide revitalizes sorafenib through insulin-like growth factor 1 receptor (IGF-1R)/stemness and metabolic changes in hepatocellular carcinoma. Cancers. 2023;15(3):931. doi:10.3390/cancers15030931
   PubMed Web of Science ®Google Scholar
• Soini Y, Virkajarvi N, Raunio H, et al. Expression of P-glycoprotein in hepatocellular carcinoma: a potential marker of prognosis. J Clin Pathol. 1996;49(6):470–473. doi:10.1136/jcp.49.6.470
   PubMed Web of Science ®Google Scholar
• Takanishi K, Miyazaki M, Ohtsuka M, et al. Inverse relationship between P-glycoprotein expression and its proliferative activity in hepatocellular carcinoma. Oncology. 1997;54(3):231–237. doi:10.1159/000227694
   PubMed Web of Science ®Google Scholar
• Ng IO, Liu CL, Fan ST, et al. Expression of P-glycoprotein in hepatocellular carcinoma. A determinant of chemotherapy response. Am J Clin Pathol. 2000;113(3):355–363. doi:10.1309/AC1M-4TY4-U0TN-EN7T
   PubMed Web of Science ®Google Scholar
• Parikh M, Liu C, Wu C-Y, et al. Phase Ib trial of reformulated niclosamide with abiraterone/prednisone in men with castration-resistant prostate cancer. Sci Rep. 2021;11(1):6377. doi:10.1038/s41598-021-85969-x
   PubMed Web of Science ®Google Scholar
• Kohli K, Chopra S, Dhar D, et al. Self-emulsifying drug delivery systems: an approach to enhance oral bioavailability. Drug Discov Today. 2010;15(21–22):958–965. doi:10.1016/j.drudis.2010.08.007
   PubMed Web of Science ®Google Scholar
• Gibaud S, Attivi D. Microemulsions for oral administration and their therapeutic applications. Expert Opin Drug Deliv. 2012;9(8):937–951. doi:10.1517/17425247.2012.694865
   PubMed Web of Science ®Google Scholar