Salinomycin nanoparticles interfere with tumor cell growth and the tumor microenvironment in an orthotopic model of pancreatic cancer

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65:5–29.
   PubMed Web of Science ®Google Scholar
• Burris Hr, Moore MJ, Andersen J, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. JCO. 1997;15:2403–2413.
   PubMed Web of Science ®Google Scholar
• Li C-P, Chao Y, Chi K-H, et al. Concurrent chemoradiotherapy treatment of locally advanced pancreatic cancer: gemcitabine versus 5-fluorouracil, a randomized controlled study. Int J Radiat Oncol Biol Phys. 2003;57:98–104.
   PubMed Web of Science ®Google Scholar
• Saif MW. US Food and Drug Administration approves paclitaxel protein-bound particles (Abraxane®) in combination with gemcitabine as first-line treatment of patients with metastatic pancreatic cancer. JOP. 2013;14:686–688.
   PubMedGoogle Scholar
• Miyazaki Y, Shibuya M, Sugawara H, et al. Salinomycin, a new polyether antibiotic. J Antibiot. 1974;27:814–821.
   PubMed Web of Science ®Google Scholar
• Callaway TR, Edrington TS, Rychlik JL, et al. Ionophores: their use as ruminant growth promotants and impact on food safety. Curr Issues Intest Microbiol. 2003;4:43–51.
   PubMedGoogle Scholar
• Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645–659.
   PubMed Web of Science ®Google Scholar
• Fuchs D, Daniel V, Sadeghi M, et al. Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun. 2010;394:1098–1104.
   PubMed Web of Science ®Google Scholar
• Verdoodt B, Vogt M, Schmitz I, et al. Salinomycin induces autophagy in colon and breast cancer cells with concomitant generation of reactive oxygen species. PLoS One. 2012;7:e44132.
   PubMed Web of Science ®Google Scholar
• Ketola K, Hilvo M, Hyötyläinen T, et al. Salinomycin inhibits prostate cancer growth and migration via induction of oxidative stress. Br J Cancer. 2012;106:99–106.
   PubMed Web of Science ®Google Scholar
• Daman Z, Montazeri H, Azizi M, et al. Polymeric micelles of PEG-PLA copolymer as a carrier for salinomycin against gemcitabine-resistant pancreatic cancer [journal article]. Pharm Res. 2015;32:3756–3767.
   PubMed Web of Science ®Google Scholar
• Schenk M, Aykut B, Teske C, et al. Salinomycin inhibits growth of pancreatic cancer and cancer cell migration by disruption of actin stress fiber integrity. Cancer Lett. 2015;358:161–169.
   PubMed Web of Science ®Google Scholar
• He L, Wang F, Dai W-Q, et al. Mechanism of action of salinomycin on growth and migration in pancreatic cancer cell lines. Pancreatology. 2013;13:72–78.
   PubMed Web of Science ®Google Scholar
• Zhang G-N, Liang Y, Zhou L-J, et al. Combination of salinomycin and gemcitabine eliminates pancreatic cancer cells. Cancer Lett. 2011;313:137–144.
   PubMed Web of Science ®Google Scholar
• Pries AR, Höpfner M, Le Noble F, et al. The shunt problem: control of functional shunting in normal and tumour vasculature. Nat Rev Cancer. 2010;10:587–593.
   PubMed Web of Science ®Google Scholar
• Neesse A, Michl P, Frese KK, et al. Stromal biology and therapy in pancreatic cancer. Gut. 2011;60:861–868.
   PubMed Web of Science ®Google Scholar
• Farrell JJ, Elsaleh H, Garcia M, et al. Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology. 2009;136:187–195.
   PubMed Web of Science ®Google Scholar
• Jain RK. Transport of molecules across tumor vasculature. Cancer Metast Rev. 1987;6:559–593.
   PubMed Web of Science ®Google Scholar
• Kumari A, Yadav SK, Yadav SC. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B Biointerfaces. 2010;75:1–18.
   PubMed Web of Science ®Google Scholar
• Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov. 2008;7:771–782.
   PubMed Web of Science ®Google Scholar
• Arao S, Masumoto A, Otsuki M. Beta1 integrins play an essential role in adhesion and invasion of pancreatic carcinoma cells. Pancreas. 2000;20:129–137.
   PubMed Web of Science ®Google Scholar
• Sawai H, Yamamoto M, Okada Y, et al. Alteration of integrins by interleukin-1alpha in human pancreatic cancer cells. Pancreas. 2001;23:399–405.
   PubMed Web of Science ®Google Scholar
• Miknyoczki SJ, Chang H, Klein-Szanto A, et al. The Trk tyrosine kinase inhibitor CEP-701 (KT-5555) exhibits significant antitumor efficacy in preclinical xenograft models of human pancreatic ductal adenocarcinoma. Clin Cancer Res. 1999;5:2205–2212.
   PubMed Web of Science ®Google Scholar
• Collisson EA, Sadanandam A, Olson P, et al. Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy. Nat Med. 2011;17:500–503.
   PubMed Web of Science ®Google Scholar
• Qiu W, Su GH. Development of orthotopic pancreatic tumor mouse models. Methods Mol Biol. 2013;980:215–223.
   PubMedGoogle Scholar
• Erkan M, Hausmann S, Michalski CW, et al. The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat Rev Gastroenterol Hepatol. 2012;9:454–467.
   PubMed Web of Science ®Google Scholar
• Li Y, Kong D, Ahmad A, et al. Pancreatic cancer stem cells: emerging target for designing novel therapy. Cancer Lett. 2013;338:94–100.
   PubMed Web of Science ®Google Scholar
• Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010;29:4741–4751.
   PubMed Web of Science ®Google Scholar
• Jiang J, Chen H, Yu C, et al. The promotion of salinomycin delivery to hepatocellular carcinoma cells through EGFR and CD133 aptamers conjugation by PLGA nanoparticles. Nanomedicine. 2015;10:1863–1879.
   PubMed Web of Science ®Google Scholar
• Tigli Aydin RS, Kaynak G, Gumusderelioglu M. Salinomycin encapsulated nanoparticles as a targeting vehicle for glioblastoma cells. J Biomed Mater Res A. 2016;104:455–464.
   PubMed Web of Science ®Google Scholar
• Aydin RS. Herceptin-decorated salinomycin-loaded nanoparticles for breast tumor targeting. J Biomed Mater Res A. 2013;101:1405–1415.
   PubMed Web of Science ®Google Scholar
• Ni M, Xiong M, Zhang X, et al. Poly(lactic-co-glycolic acid) nanoparticles conjugated with CD133 aptamers for targeted salinomycin delivery to CD133(+) osteosarcoma cancer stem cells. Int J Nanomedicine. 2015;10:2537–2554.
   PubMed Web of Science ®Google Scholar
• Guo S, Lin CM, Xu Z, et al. Co-delivery of cisplatin and rapamycin for enhanced anticancer therapy through synergistic effects and microenvironment modulation. ACS Nano. 2014;8:4996–5009.
   PubMed Web of Science ®Google Scholar
• Graf N, Bielenberg DR, Kolishetti N, et al. α(V)β(3) Integrin-targeted PLGA-PEG nanoparticles for enhanced anti-tumor efficacy of a Pt(IV) prodrug. ACS Nano. 2012;6:4530–4539.
   PubMed Web of Science ®Google Scholar
• Martínez Rivas CJ, Tarhini M, Badri W, et al. Nanoprecipitation process: from encapsulation to drug delivery. Int J Pharm. 2017;532:66–81.
   PubMed Web of Science ®Google Scholar
• Greish K. Enhanced permeability and retention (EPR) effect for anticancer nanomedicine drug targeting. Methods Mol Biol. 2010;624:25–37.
   PubMedGoogle Scholar
• Moghimi SM, Szebeni J. Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties. Prog Lipid Res. 2003;42:463–478.
   PubMed Web of Science ®Google Scholar
• Jaidev L, Krishnan UM, Sethuraman S. Gemcitabine loaded biodegradable PLGA nanospheres for in vitro pancreatic cancer therapy. Mater Sci Eng C. 2015;47:40–47.
   PubMed Web of Science ®Google Scholar
• Zhou H, Qian W, Uckun FM, et al. IGF1 receptor targeted theranostic nanoparticles for targeted and image-guided therapy of pancreatic cancer. ACS Nano. 2015;9:7976–7991.
   PubMed Web of Science ®Google Scholar
• Lee GY, Qian WP, Wang L, et al. Theranostic nanoparticles with controlled release of gemcitabine for targeted therapy and MRI of pancreatic cancer. ACS Nano. 2013;7:2078–2089.
   PubMed Web of Science ®Google Scholar
• Naujokat C, Steinhart R. Salinomycin as a drug for targeting human cancer stem cells. BioMed Res Int. 2012;2012:950658.
   Google Scholar
• Lucero-Acuña A, Jeffery JJ, Abril ER, et al. Nanoparticle delivery of an AKT/PDK1 inhibitor improves the therapeutic effect in pancreatic cancer. Int J Nanomedicine. 2013;9:5653–5665.
   Web of Science ®Google Scholar
• Fonseca C, Simoes S, Gaspar R. Paclitaxel-loaded PLGA nanoparticles: preparation, physicochemical characterization and in vitro anti-tumoral activity. J Control Release. 2002;83:273–286.
   PubMed Web of Science ®Google Scholar
• Provenzano PP, Cuevas C, Chang AE, et al. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell. 2012;21:418–429.
   PubMed Web of Science ®Google Scholar
• Rhim AD, Oberstein PE, Thomas DH, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell. 2014;25:735–747.
   PubMed Web of Science ®Google Scholar
• Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 2005;17:548–558.
   PubMed Web of Science ®Google Scholar
• Thiery JP, Acloque H, Huang RY, et al. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871–890.
   PubMed Web of Science ®Google Scholar
• Ozawa M, Baribault H, Kemler R. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 1989;8:1711–1717.
   PubMed Web of Science ®Google Scholar
• Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell. 2012;149:1192–1205.
   PubMed Web of Science ®Google Scholar
• Morgan RG, Ridsdale J, Tonks A, et al. Factors affecting the nuclear localization of β-catenin in normal and malignant tissue. J Cell Biochem. 2014;115:1351–1361.
   PubMed Web of Science ®Google Scholar
• Tanaka M, Kitajima Y, Edakuni G, et al. Abnormal expression of E-cadherin and beta-catenin may be a molecular marker of submucosal invasion and lymph node metastasis in early gastric cancer. Br J Surg. 2002;89:236–244.
   PubMed Web of Science ®Google Scholar
• Choi YS, Shim YM, Kim SH, et al. Prognostic significance of E-cadherin and beta-catenin in resected stage I non-small cell lung cancer. Eur J Cardiothorac Surg. 2003;24:441–449.
   PubMed Web of Science ®Google Scholar
• Takayama T, Shiozaki H, Shibamoto S, et al. Beta-catenin expression in human cancers. Am J Pathol. 1996;148:39–46.
   PubMed Web of Science ®Google Scholar
• Karayiannakis AJ, Syrigos KN, Polychronidis A, et al. Expression patterns of alpha-, beta- and gamma-catenin in pancreatic cancer: correlation with E-cadherin expression, pathological features and prognosis. Anticancer Res. 2001;21:4127–4134.
   PubMed Web of Science ®Google Scholar
• Bierie B, Moses HL. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer. 2006;6:506–520.
   PubMed Web of Science ®Google Scholar
• Pollard JW. Tumour-stromal interactions. Transforming growth factor-beta isoforms and hepatocyte growth factor/scatter factor in mammary gland ductal morphogenesis. Breast Cancer Res. 2001;3:230–237.
   PubMed Web of Science ®Google Scholar
• Bhowmick NA, Chytil A, Plieth D, et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science. 2004;303:848–851.
   PubMed Web of Science ®Google Scholar
• Cheng N, Bhowmick NA, Chytil A, et al. Loss of TGF-beta type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-alpha-, MSP- and HGF-mediated signaling networks. Oncogene. 2005;24:5053–5068.
   PubMed Web of Science ®Google Scholar
• Franco OE, Jiang M, Strand DW, et al. Altered TGF-beta signaling in a subpopulation of human stromal cells promotes prostatic carcinogenesis. Cancer Res. 2011;71: 1272–1281.
   PubMed Web of Science ®Google Scholar
• Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med. 2013;19:1438–1449.
   PubMed Web of Science ®Google Scholar