MicroRNA-Based Therapy in Animal Models of Selected Gastrointestinal Cancers
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu přehledy, časopisecké články
PubMed
27729862
PubMed Central
PMC5037200
DOI
10.3389/fphar.2016.00329
Knihovny.cz E-zdroje
- Klíčová slova
- animal model, colorectal cancer, gallbladder cancer, gastric cancer, mice, microRNA, pancreatic cancer, preclinical testing,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Gastrointestinal cancer accounts for the 20 most frequent cancer diseases worldwide and there is a constant urge to bring new therapeutics with new mechanism of action into the clinical practice. Quantity of in vitro and in vivo evidences indicate, that exogenous change in pathologically imbalanced microRNAs (miRNAs) is capable of transforming the cancer cell phenotype. This review analyzed preclinical miRNA-based therapy attempts in animal models of gastric, pancreatic, gallbladder, and colorectal cancer. From more than 400 original articles, 26 was found to assess the effect of miRNA mimics, precursors, expression vectors, or inhibitors administered locally or systemically being an approach with relatively high translational potential. We have focused on mapping available information on animal model used (animal strain, cell line, xenograft method), pharmacological aspects (oligonucleotide chemistry, delivery system, posology, route of administration) and toxicology assessments. We also summarize findings in the field pharmacokinetics and toxicity of miRNA-based therapy.
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Adams B. D., Parsons C., Slack F. J. (2015). The tumor-suppressive and potential therapeutic functions of miR-34a in epithelial carcinomas. Expert Opin. Ther. Targets 20, 737–753. 10.1517/14728222.2016.1114102 PubMed DOI PMC
Akinc A., Thomas M., Klibanov A. M., Langer R. (2005). Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis. J. Gene Med. 7, 657–663. 10.1002/jgm.696 PubMed DOI
Aslam M. I., Patel M., Singh B., Jameson J. S., Pringle J. H. (2012). MicroRNA manipulation in colorectal cancer cells: from laboratory to clinical application. J. Transl. Med. 10:128. 10.1186/1479-5876-10-128 PubMed DOI PMC
Axtell M. J., Westholm J. O., Lai E. C. (2011). Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 12:221. 10.1186/gb-2011-12-4-221 PubMed DOI PMC
Bader A. G., Brown D., Winkler M. (2010). The promise of MicroRNA replacement therapy. Cancer Res. 70, 7027–7030. 10.1158/0008-5472.CAN-10-2010 PubMed DOI PMC
Bao Y., Chen Z., Guo Y., Feng Y., Li Z., Han W., et al. . (2014). Tumor suppressor MicroRNA-27a in colorectal carcinogenesis and progression by targeting SGPP1 and Smad2. PLoS ONE 9:e105991. 10.1371/journal.pone.0105991 PubMed DOI PMC
Beyerle A., Braun A., Merkel O., Koch F., Kissel T., Stoeger T. (2011). Comparative in vivo study of poly (ethylene imine)/siRNA complexes for pulmonary delivery in mice. J. Control Release Off. J. Control Release Soc. 151, 51–56. 10.1016/j.jconrel.2010.12.017 PubMed DOI
Bofill-De Ros X., Villanueva E., Fillat C. (2015). Late-phase miRNA-controlled oncolytic adenovirus for selective killing of cancer cells. Oncotarget 6, 6179–6190. 10.18632/oncotarget.3350 PubMed DOI PMC
Bonnet M.-E., Erbacher P., Bolcato-Bellemin A.-L. (2008). Systemic delivery of DNA or siRNA mediated by linear polyethylenimine (L-PEI) does not induce an inflammatory response. Pharm. Res. 25, 2972–2982. 10.1007/s11095-008-9693-1 PubMed DOI
Braasch D. A., Corey D. R. (2001). Locked nucleic acid (LNA): fine-tuning the recognition of DNA and RNA. Chem. Biol. 8, 1–7. 10.1016/S1074-5521(00)00058-2 PubMed DOI
Broderick J. A., Zamore P. D. (2011). MicroRNA therapeutics. Gene Ther. 18, 1104–1110. 10.1038/gt.2011.50 PubMed DOI PMC
Calin G. A., Croce C. M. (2006). MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857–866. 10.1038/nrc1997 PubMed DOI
Chang Y., Liu C., Yang J., Liu G., Feng F., Tang J., et al. . (2013). miR-20a triggers metastasis of gallbladder carcinoma. J. Hepatol. 59, 518–527. 10.1016/j.jhep.2013.04.034 PubMed DOI
Chen L., Lü M.-H., Zhang D., Hao N.-B., Fan Y.-H., Wu Y.-Y., et al. . (2014). miR-1207-5p and miR-1266 suppress gastric cancer growth and invasion by targeting telomerase reverse transcriptase. Cell Death Dis. 5:e1034. 10.1038/cddis.2013.553 PubMed DOI PMC
Chen Y., Gao D.-Y., Huang L. (2015). In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv. Drug Deliv. Rev. 81, 128–141. 10.1016/j.addr.2014.05.009 PubMed DOI PMC
Cheng C. J., Saltzman W. M., Slack F. J. (2013). Canonical and non-canonical barriers facing antimir cancer therapeutics. Curr. Med. Chem. 20, 3582–3593. 10.2174/0929867311320290004 PubMed DOI PMC
Chollet P., Favrot M. C., Hurbin A., Coll J.-L. (2002). Side-effects of a systemic injection of linear polyethylenimine-DNA complexes. J. Gene Med. 4, 84–91. 10.1002/jgm.237 PubMed DOI
Chowdhury E. H., Maruyama A., Kano A., Nagaoka M., Kotaka M., Hirose S., et al. . (2006). pH-sensing nano-crystals of carbonate apatite: effects on intracellular delivery and release of DNA for efficient expression into mammalian cells. Gene 376, 87–94. 10.1016/j.gene.2006.02.028 PubMed DOI
Cong N., Du P., Zhang A., Shen F., Su J., Pu P., et al. . (2013). Downregulated microRNA-200a promotes EMT and tumor growth through the Wnt/beta-catenin pathway by targeting the E-cadherin repressors ZEB1/ZEB2 in gastric adenocarcinoma. Oncol. Rep. 29, 1579–1587. 10.3892/or.2013.2267 PubMed DOI
Crooke S. T. (2007). Antisense Drug Technology: Principles, Strategies, and Applications, 2nd Edn Boca Raton, FL: CRC Press.
Dong Y., Zhao J., Wu C.-W., Zhang L., Liu X., Kang W., et al. . (2013). Tumor suppressor functions of miR-133a in colorectal cancer. Mol. Cancer Res. 11, 1051–1060. 10.1158/1541-7786.MCR-13-0061 PubMed DOI
Esquela-Kerscher A., Slack F. J. (2006). Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259–269. 10.1038/nrc1840 PubMed DOI
Fischer D., Bieber T., Li Y., Elsässer H. P., Kissel T. (1999). A novel non-viral vector for DNA delivery based on low molecular weight, branched polyethylenimine: effect of molecular weight on transfection efficiency and cytotoxicity. Pharm. Res. 16, 1273–1279. 10.1023/A:1014861900478 PubMed DOI
Frampton A. E., Castellano L., Colombo T., Giovannetti E., Krell J., Jacob J., et al. . (2011). MicroRNAs cooperatively inhibit a network of tumor suppressor genes to promote pancreatic tumor growth and progression. Gastroenterology 146, 268.e18–277.e18. 10.1053/j.gastro.2013.10.010 PubMed DOI
Garzon R., Fabbri M., Cimmino A., Calin G. A., Croce C. M. (2006). MicroRNA expression and function in cancer. Trends Mol. Med. 12, 580–587. 10.1016/j.molmed.2006.10.006 PubMed DOI
Geng L., Zhu B., Dai B.-H., Sui C.-J., Xu F., Kan T., et al. . (2011). A let-7/Fas double-negative feedback loop regulates human colon carcinoma cells sensitivity to Fas-related apoptosis. Biochem. Biophys. Res. Commun. 408, 494–499. 10.1016/j.bbrc.2011.04.074 PubMed DOI
Glover J. M., Leeds J. M., Mant T. G. K., Amin D., Kisner D. L., Zuckerman J. E., et al. . (1997). Phase I safety and pharmacokinetic profile of an intercellular adhesion molecule-1 antisense oligodeoxynucleotide (ISIS 2302). J. Pharmacol. Exp. Ther. 282, 1173–1180. PubMed
Grimm D., Streetz K. L., Jopling C. L., Storm T. A., Pandey K., Davis C. R., et al. . (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537–541. 10.1038/nature04791 PubMed DOI
Gu W., Xu Y., Xie X., Wang T., Ko J.-H., Zhou T. (2014). The role of RNA structure at 5′ untranslated region in microRNA-mediated gene regulation. RNA 20, 1369–1375. 10.1261/rna.044792.114 PubMed DOI PMC
Hanahan D., Weinberg R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646–674. 10.1016/j.cell.2011.02.013 PubMed DOI
Hanini A., Schmitt A., Kacem K., Chau F., Ammar S., Gavard J. (2011). Evaluation of iron oxide nanoparticle biocompatibility. Int. J. Nanomed. 6, 787–794. 10.2147/IJN.S17574 PubMed DOI PMC
Hao Z., Fan W., Hao J., Wu X., Zeng G. Q., Zhang L. J., et al. . (2016). Efficient delivery of micro RNA to bone-metastatic prostate tumors by using aptamer-conjugated atelocollagen in vitro and in vivo. Drug Deliv. 23, 874–881. 10.3109/10717544.2014.920059 PubMed DOI
He X., Dong Y., Wu C. W., Zhao Z., Ng S. S. M., Chan F. K. L., et al. . (2012). MicroRNA-218 inhibits cell cycle progression and promotes apoptosis in colon cancer by downregulating BMI1 polycomb ring finger oncogene. Mol. Med. 18, 1491–1498. 10.2119/molmed.2012.00304 PubMed DOI PMC
Henry S. P., Beattie G., Yeh G., Chappel A., Giclas P., Mortari A., et al. . (2002). Complement activation is responsible for acute toxicities in rhesus monkeys treated with a phosphorothioate oligodeoxynucleotide. Int. Immunopharmacol. 2, 1657–1666. 10.1016/S1567-5769(02)00142-X PubMed DOI
Henry S. P., Bolte H., Auletta C., Kornbrust D. J. (1997). Evaluation of the toxicity of ISIS 2302, a phosphorothioate oligonucleotide, in a four-week study in cynomolgus monkeys. Toxicology 120, 145–155. 10.1016/S0300-483X(97)03661-5 PubMed DOI
Hiraki M., Nishimura J., Takahashi H., Wu X., Takahashi Y., Miyo M., et al. . (2015). Concurrent targeting of KRAS and AKT by MiR-4689 is a novel treatment against mutant KRAS colorectal cancer. Mol. Ther. Nucleic Acids 4:e231. 10.1038/mtna.2015.5 PubMed DOI PMC
Höbel S., Aigner A. (2013). Polyethylenimines for siRNA and miRNA delivery in vivo. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 5, 484–501. 10.1002/wnan.1228 PubMed DOI
Ho T. T., Zhou N., Huang J., Koirala P., Xu M., Fung R., et al. . (2015). Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines. Nucleic Acids Res. 43:e17. 10.1093/nar/gku1198 PubMed DOI PMC
Hogg D. R., Harries L. W. (2014). Human genetic variation and its effect on miRNA biogenesis, activity and function. Biochem. Soc. Trans. 42, 1184–1189. 10.1042/BST20140055 PubMed DOI
Hossain S., Stanislaus A., Chua M. J., Tada S., Tagawa Y., Chowdhury E. H., et al. . (2010). Carbonate apatite-facilitated intracellularly delivered siRNA for efficient knockdown of functional genes. J. Control Release Off. J. Control Release Soc. 147, 101–108. 10.1016/j.jconrel.2010.06.024 PubMed DOI
Hu Q. L., Jiang Q. Y., Jin X., Shen J., Wang K., Li Y. B., et al. . (2013). Cationic microRNA-delivering nanovectors with bifunctional peptides for efficient treatment of PANC-1 xenograft model. Biomaterials 34, 2265–2276. 10.1016/j.biomaterials.2012.12.016 PubMed DOI
Hwang H.-W., Wentzel E. A., Mendell J. T. (2007). A hexanucleotide element directs microRNA nuclear import. Science 315, 97–100. 10.1126/science.1136235 PubMed DOI
Ibrahim A. F., Weirauch U., Thomas M., Grünweller A., Hartmann R. K., Aigner A. (2011). MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma. Cancer Res. 71, 5214–5224. 10.1158/0008-5472.CAN-10-4645 PubMed DOI
Ishida T., Ichihara M., Wang X., Yamamoto K., Kimura J., Majima E., et al. . (2006). Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J. Control Release Off. J. Control Release Soc. 112, 15–25. 10.1016/j.jconrel.2006.01.005 PubMed DOI
Jeffries C. D., Fried H. M., Perkins D. O. (2011). Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 17, 675–686. 10.1261/rna.2006511 PubMed DOI PMC
Jin H. Y., Gonzalez-Martin A., Miletic A. V., Lai M., Knight S., Sabouri-Ghomi M., et al. . (2015). Transfection of microRNA mimics should be used with caution. Front. Genet. 6:340. 10.3389/fgene.2015.00340 PubMed DOI PMC
Ju C., Mo R., Xue J., Zhang L., Zhao Z., Xue L., et al. . (2014). Sequential intra-intercellular nanoparticle delivery system for deep tumor penetration. Angew. Chem. Int. Ed. 53, 6253–6258. 10.1002/anie.201311227 PubMed DOI
Kanasty R. L., Whitehead K. A., Vegas A. J., Anderson D. G. (2012). Action and reaction: the biological response to siRNA and its delivery vehicles. Mol. Ther. J. Am. Soc. Gene Ther. 20, 513–524. 10.1038/mt.2011.294 PubMed DOI PMC
Kao S. C., Fulham M., Wong K., Cooper W., Brahmbhatt H., MacDiarmid J., et al. . (2015). A significant metabolic and radiological response after a novel targeted MicroRNA-based treatment approach in malignant pleural mesothelioma. Am. J. Respir. Crit. Care Med. 191, 1467–1469. 10.1164/rccm.201503-0461LE PubMed DOI
Kasinski A. L., Slack F. J. (2011). Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat. Rev. Cancer 11, 849–864. 10.1038/nrc3166 PubMed DOI PMC
Keklikoglou I., Hosaka K., Bender C., Bott A., Koerner C., Mitra D., et al. . (2015). MicroRNA-206 functions as a pleiotropic modulator of cell proliferation, invasion and lymphangiogenesis in pancreatic adenocarcinoma by targeting ANXA2 and KRAS genes. Oncogene 34, 4867–4878. 10.1038/onc.2014.408 PubMed DOI PMC
Kievit F. M., Veiseh O., Bhattarai N., Fang C., Gunn J. W., Lee D., et al. . (2009). PEI-PEG-chitosan copolymer coated iron oxide nanoparticles for safe gene delivery: synthesis, complexation, and transfection. Adv. Funct. Mater. 19, 2244–2251. 10.1002/adfm.200801844 PubMed DOI PMC
Kievit F. M., Zhang M. (2011). Surface engineering of iron oxide nanoparticles for targeted cancer therapy. Acc. Chem. Res. 44, 853–862. 10.1021/ar2000277 PubMed DOI PMC
Komatsu K., Shibata T., Shimada A., Ideno H., Nakashima K., Tabata Y., et al. . (2016). Cationized gelatin hydrogels mixed with plasmid DNA induce stronger and more sustained gene expression than atelocollagen at calvarial bone defects in vivo. J. Biomater. Sci. Polym. Ed. 27, 419–430. 10.1080/09205063.2016.1139486 PubMed DOI
Krieg A. M., Yi A.-K., Matson S., Waldschmidt T. J., Bishop G. A., Teasdale R., et al. . (1995). CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374, 546–549. 10.1038/374546a0 PubMed DOI
Kumar R., Singh S. K., Koshkin A. A., Rajwanshi V. K., Meldgaard M., Wengel J. (1998). The first analogues of LNA (locked nucleic acids): phosphorothioate-LNA and 2′-thio-LNA. Bioorg. Med. Chem. Lett. 8, 2219–2222. 10.1016/S0960-894X(98)00366-7 PubMed DOI
Lahdaoui F., Delpu Y., Vincent A., Renaud F., Messager M., Duchêne B., et al. . (2014). miR-219-1-3p is a negative regulator of the mucin MUC4 expression and is a tumor suppressor in pancreatic cancer. Oncogene 34, 780–788. 10.1038/onc.2014.11 PubMed DOI
Lellouche E., Israel L. L., Bechor M., Attal S., Kurlander E., Asher V. A., et al. . (2015). MagRET nanoparticles: an iron oxide nanocomposite platform for gene silencing from microRNAs to long noncoding RNAs. Bioconjug. Chem. 26, 1692–1701. 10.1021/acs.bioconjchem.5b00276 PubMed DOI
Levin A. A. (1999). A review of the issues in the pharmacokinetics and toxicology of phosphorothioate antisense oligonucleotides. Biochim. Biophys. Acta 1489, 69–84. 10.1016/S0167-4781(99)00140-2 PubMed DOI
Li Z. F., Liang Y. M., Lau P. N., Shen W., Wang D. K., Cheung W. T., et al. . (2013). Dynamic localisation of mature microRNAs in Human nucleoli is influenced by exogenous genetic materials. PLoS ONE 8:e70869. 10.1371/journal.pone.0070869 PubMed DOI PMC
Maeda H. (2015). Toward a full understanding of the EPR effect in primary and metastatic tumors as well as issues related to its heterogeneity. Adv. Drug Deliv. Rev. 91, 3–6. 10.1016/j.addr.2015.01.002 PubMed DOI
Mahmoudi M., Laurent S., Shokrgozar M. A., Hosseinkhani M. (2011). Toxicity evaluations of superparamagnetic iron oxide nanoparticles: cell “vision” versus physicochemical properties of nanoparticles. ACS Nano 5, 7263–7276. 10.1021/nn2021088 PubMed DOI
Malek A., Merkel O., Fink L., Czubayko F., Kissel T., Aigner A. (2009). In vivo pharmacokinetics, tissue distribution and underlying mechanisms of various PEI(-PEG)/siRNA complexes. Toxicol. Appl. Pharmacol. 236, 97–108. 10.1016/j.taap.2009.01.014 PubMed DOI
Mallick S., Choi J. S. (2014). Liposomes: versatile and biocompatible nanovesicles for efficient biomolecules delivery. J. Nanosci. Nanotechnol. 14, 755–765. 10.1166/jnn.2014.9080 PubMed DOI
Matsumura Y., Maeda H. (1986). A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 46(12 Part 1):6387–6392. PubMed
Merkel O. M., Beyerle A., Beckmann B. M., Zheng M., Hartmann R. K., Stöger T., et al. . (2011). Polymer-related off-target effects in non-viral siRNA delivery. Biomaterials 32, 2388–2398. 10.1016/j.biomaterials.2010.11.081 PubMed DOI
Mittal A., Chitkara D., Behrman S. W., Mahato R. I. (2014). Efficacy of gemcitabine conjugated and miRNA-205 complexed micelles for treatment of advanced pancreatic cancer. Biomaterials 35, 7077–7087. 10.1016/j.biomaterials.2014.04.053 PubMed DOI
Narayanan A., Hill-Teran G., Moro A., Ristori E., Kasper D. M., Roden C., et al. . (2016). In vivo mutagenesis of miRNA gene families using a scalable multiplexed CRISPR/Cas9 nuclease system. Sci. Rep. 6:32386. 10.1038/srep32386 PubMed DOI PMC
Nchinda G., Uberla K., Zschörnig O. (2002). Characterization of cationic lipid DNA transfection complexes differing in susceptability to serum inhibition. BMC Biotechnol. 2:12. 10.1186/1472-6750-2-12 PubMed DOI PMC
Ochiya T., Nagahara S., Sano A., Itoh H., Terada M. (2001). Biomaterials for gene delivery: atelocollagen-mediated controlled release of molecular medicines. Curr. Gene Ther. 1, 31–52. 10.2174/1566523013348887 PubMed DOI
Ochiya T., Takahama Y., Nagahara S., Sumita Y., Hisada A., Itoh H., et al. . (1999). New delivery system for plasmid DNA in vivo using atelocollagen as a carrier material: the Minipellet. Nat. Med. 5, 707–710. 10.1038/9560 PubMed DOI
Ott C. E., Grünhagen J., Jäger M., Horbelt D., Schwill S., Kallenbach K., et al. . (2011). MicroRNAs differentially expressed in postnatal aortic development downregulate elastin via 3′ UTR and coding-sequence binding sites. PLoS ONE 6:e16250. 10.1371/journal.pone.0016250 PubMed DOI PMC
Park C. W., Zeng Y., Zhang X., Subramanian S., Steer C. J. (2010). Mature microRNAs identified in highly purified nuclei from HCT116 colon cancer cells. RNA Biol. 7, 606–614. 10.4161/rna.7.5.13215 PubMed DOI PMC
Pathak K., Keshri L., Shah M. (2011). Lipid nanocarriers: influence of lipids on product development and pharmacokinetics. Crit. Rev. Ther. Drug Carrier Syst. 28, 357–393. 10.1615/CritRevTherDrugCarrierSyst.v28.i4.20 PubMed DOI
Pramanik D., Campbell N. R., Karikari C., Chivukula R., Kent O. A., Mendell J. T., et al. . (2011). Restitution of tumor suppressor microRNAs using a systemic nanovector inhibits pancreatic cancer growth in mice. Mol. Cancer Ther. 10, 1470–1480. 10.1158/1535-7163.MCT-11-0152 PubMed DOI PMC
Quinn L., Finn S. P., Cuffe S., Gray S. G. (2015). Non-coding RNA repertoires in malignant pleural mesothelioma. Lung Cancer Amst. Neth. 90, 417–426. 10.1016/j.lungcan.2015.11.002 PubMed DOI
RG-101 , (2016). Regulus Therapeutics. Available online at: http://regulusrx.com/programs/clinical-pipeline/rg-101/
Romero-Cordoba S. L., Salido-Guadarrama I., Rodriguez-Dorantes M., Hidalgo-Miranda A. (2014). miRNA biogenesis: biological impact in the development of cancer. Cancer Biol. Ther. 15, 1444–1455. 10.4161/15384047.2014.955442 PubMed DOI PMC
Ruan K., Fang X., Ouyang G. (2009). MicroRNAs: novel regulators in the hallmarks of human cancer. Cancer Lett. 285, 116–126. 10.1016/j.canlet.2009.04.031 PubMed DOI
Seto A. G. (2010). The road toward microRNA therapeutics. Int. J. Biochem. Cell Biol. 42, 1298–1305. 10.1016/j.biocel.2010.03.003 PubMed DOI
Sheehan J. P., Lan H.-C. (1998). Phosphorothioate oligonucleotides inhibit the intrinsic tenase complex. Blood 92, 1617–1625. PubMed
Sicard F., Gayral M., Lulka H., Buscail L., Cordelier P. (2013). Targeting miR-21 for the therapy of pancreatic cancer. Mol. Ther. 21, 986–994. 10.1038/mt.2013.35 PubMed DOI PMC
Søkilde R., Newie I., Persson H., Borg Å., Rovira C. (2015). Passenger strand loading in overexpression experiments using microRNA mimics. RNA Biol. 12, 787–791. 10.1080/15476286.2015.1020270 PubMed DOI PMC
Soriano A., Jubierre L., Almazán-Moga A., Molist C., Roma J., de Toledo J. S., et al. . (2013). microRNAs as pharmacological targets in cancer. Pharmacol. Res. 75, 3–14. 10.1016/j.phrs.2013.03.006 PubMed DOI
Suk J. S., Xu Q., Kim N., Hanes J., Ensign L. M. (2016). PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv. Drug Deliv. Rev. 99(Pt A):28–51. 10.1016/j.addr.2015.09.012 PubMed DOI PMC
Sun Y., Shen S., Liu X., Tang H., Wang Z., Yu Z., et al. . (2014). MiR-429 inhibits cells growth and invasion and regulates EMT-related marker genes by targeting Onecut2 in colorectal carcinoma. Mol. Cell. Biochem. 390, 19–30. 10.1007/s11010-013-1950-x PubMed DOI PMC
Sun Z., Song X., Li X., Su T., Qi S., Qiao R., et al. . (2014). In vivo multimodality imaging of miRNA-16 iron nanoparticle reversing drug resistance to chemotherapy in a mouse gastric cancer model. Nanoscale 6, 14343–14353. 10.1039/C4NR03003F PubMed DOI
Tan Y., Huang L. (2002). Overcoming the inflammatory toxicity of cationic gene vectors. J. Drug Target 10, 153–160. 10.1080/10611860290016757 PubMed DOI
Tang R., Li L., Zhu D., Hou D., Cao T., Gu H., et al. . (2012). Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Cell Res. 22, 504–515. 10.1038/cr.2011.137 PubMed DOI PMC
Tréhoux S., Lahdaoui F., Delpu Y., Renaud F., Leteurtre E., Torrisani J., et al. . (2015). Micro-RNAs miR-29a and miR-330-5p function as tumor suppressors by targeting the MUC1 mucin in pancreatic cancer cells. Biochim. Biophys. Acta Mol. Cell Res. 1853, 2392–2403. 10.1016/j.bbamcr.2015.05.033 PubMed DOI
van der Ree M. H., van der Meer A. J., van Nuenen A. C., de Bruijne J., Ottosen S., Janssen H. L., et al. . (2016). Miravirsen dosing in chronic hepatitis C patients results in decreased microRNA-122 levels without affecting other microRNAs in plasma. Aliment. Pharmacol. Ther. 43, 102–113. 10.1111/apt.13432 PubMed DOI
van Rooij E., Purcell A. L., Levin A. A. (2012). Developing microRNA therapeutics. Circ. Res. 110, 496–507. 10.1161/CIRCRESAHA.111.247916 PubMed DOI
Vidic S., Markelc B., Sersa G., Coer A., Kamensek U., Tevz G., et al. . (2010). MicroRNAs targeting mutant K-ras by electrotransfer inhibit human colorectal adenocarcinoma cell growth in vitro and in vivo. Cancer Gene Ther. 17, 409–419. 10.1038/cgt.2009.87 PubMed DOI
Wang J., Chen Y., Chen B., Ding J., Xia G., Gao C., et al. . (2010). Pharmacokinetic parameters and tissue distribution of magnetic Fe(3)O(4) nanoparticles in mice. Int. J. Nanomed. 5, 861–866. 10.2147/IJN.S13662 PubMed DOI PMC
Wang M., Gu H., Qian H., Zhu W., Zhao C., Zhang X., et al. . (2013). miR-17-5p/20a are important markers for gastric cancer and murine double minute 2 participates in their functional regulation. Eur. J. Cancer 49, 2010–2021. 10.1016/j.ejca.2012.12.017 PubMed DOI
Wei Y., Li L., Wang D., Zhang C.-Y., Zen K. (2014). Importin 8 regulates the transport of mature microRNAs into the cell nucleus. J. Biol. Chem. 289, 10270–10275. 10.1074/jbc.C113.541417 PubMed DOI PMC
Wen D., Danquah M., Chaudhary A. K., Mahato R. I. (2015). Small molecules targeting microRNA for cancer therapy: promises and obstacles. J. Control Release 219, 237–247. 10.1016/j.jconrel.2015.08.011 PubMed DOI PMC
Wu J., Lizarzaburu M. E., Kurth M. J., Liu L., Wege H., Zern M. A., et al. . (2001). Cationic lipid polymerization as a novel approach for constructing new DNA delivery agents. Bioconjug. Chem. 12, 251–257. 10.1021/bc000097e PubMed DOI
Wu X., Yamamoto H., Nakanishi H., Yamamoto Y., Inoue A., Tei M., et al. . (2015). Innovative delivery of siRNA to solid tumors by super carbonate apatite. PLoS ONE 10:e0116022. 10.1371/journal.pone.0116022 PubMed DOI PMC
Xie J., Huang J., Li X., Sun S., Chen X. (2009). Iron oxide nanoparticle platform for biomedical applications. Curr. Med. Chem. 16, 1278–1294. 10.2174/092986709787846604 PubMed DOI
Xue H., Guo P., Wen W.-C., Wong H. (2015). Lipid-based nanocarriers for RNA delivery. Curr. Pharm. Des. 21, 3140–3147. 10.2174/1381612821666150531164540 PubMed DOI PMC
Ye J., Wu X., Wu D., Wu P., Ni C., Zhang Z., et al. . (2013). miRNA-27b targets vascular endothelial growth factor c to inhibit tumor progression and angiogenesis in colorectal cancer. PLoS ONE 8:e60687. 10.1371/journal.pone.0060687 PubMed DOI PMC
Zelphati O., Szoka F. C. (1996). Mechanism of oligonucleotide release from cationic liposomes. Proc. Natl. Acad. Sci. U.S.A. 93, 11493–11498. 10.1073/pnas.93.21.11493 PubMed DOI PMC
Zhang J.-S., Liu F., Huang L. (2005). Implications of pharmacokinetic behavior of lipoplex for its inflammatory toxicity. Adv. Drug Deliv. Rev. 57, 689–698. 10.1016/j.addr.2004.12.004 PubMed DOI
Zhang X.-X., McIntosh T. J., Grinstaff M. W. (2012). Functional lipids and lipoplexes for improved gene delivery. Biochimie 94, 42–58. 10.1016/j.biochi.2011.05.005 PubMed DOI PMC
Zhang Y., Qu X., Li C., Fan Y., Che X., Wang X., et al. . (2015). miR-103/107 modulates multidrug resistance in human gastric carcinoma by downregulating Cav-1. Tumor Biol. 36, 2277–2285. 10.1007/s13277-014-2835-7 PubMed DOI
Zhang Y., Wang Z., Gemeinhart R. A. (2013). Progress in microRNA delivery. J. Control Release Off. J. Control Release Soc. 172, 962–974. 10.1016/j.jconrel.2013.09.015 PubMed DOI PMC
Zhao W.-G., Yu S.-N., Lu Z.-H., Ma Y.-H., Gu Y.-M., Chen J. (2010). The miR-217 microRNA functions as a potential tumor suppressor in pancreatic ductal adenocarcinoma by targeting KRAS. Carcinogenesis 31, 1726–1733. 10.1093/carcin/bgq160 PubMed DOI
Zisoulis D. G., Kai Z. S., Chang R. K., Pasquinelli A. E. (2012). Autoregulation of microRNA biogenesis by let-7 and argonaute. Nature 486, 541–544. 10.1038/nature11134 PubMed DOI PMC
Zou Y., Li J., Chen Z., Li X., Zheng S., Yi D., et al. . (2015). miR-29c suppresses pancreatic cancer liver metastasis in an orthotopic implantation model in nude mice and affects survival in pancreatic cancer patients. Carcinogenesis 36, 676–684. 10.1093/carcin/bgv027 PubMed DOI