ORBi: Detailled Reference

Article (Scientific journals)

Versatile electrostatically assembled polymeric siRNA nanovectors: Can they overcome the limits of siRNA tumor delivery?

Ben Djemaa, Sanaa; Munnier, E; Chourpa, I et al.

2019 • In International Journal of Pharmaceutics, 567, p. 118432

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/290875

DOI
10.1016/j.ijpharm.2019.06.023

PubMed
31199995

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Versatile electrostatically assembled polymeric siRNA nanovectors Can they overcome the limits of siRNA tumor delivery.pdf

Author postprint (1.61 MB)

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Electrostatically assembled polymeric siRNA nanovectors (EPSN); Intracellular trafficking; Nanovector design; Protein down-regulation; siRNA delivery

Abstract :

[en] The application of small interfering RNA (siRNA) cancer therapeutics is limited by several extra- and intracellular barriers including the presence of ribonucleases that degrade siRNA, the premature clearance, the impermeability of the cell membrane, or the difficulty to escape endo-lysosomal degradation. Therefore, several delivery systems have emerged to overcome these limitations and to successfully deliver siRNA to the tumor site. This review is focused on polymer-based siRNA nanovectors which exploit the negative charge of siRNA, representing a major challenge for siRNA delivery, to their advantage by loading siRNA via electrostatic assembly. These nanovectors are easy to prepare and to adapt for an optimal gene silencing efficiency. The ability of electrostatically assembled polymeric siRNA nanovectors (EPSN) to improve the half-life of siRNA, to favor the specificity of the delivery and the accumulation in tumor and to enhance the cellular uptake and endosomal escape for an efficient siRNA delivery will be discussed. Finally, the influence of the versatility of the structure of these nanovectors on the protein down-regulation will be evaluated.

Disciplines :

Human health sciences: Multidisciplinary, general & others

Author, co-author :

Ben Djemaa, Sanaa ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques ; Université de Tours, EA6295 Nanomédicaments et Nanosondes, 31 Avenue Monge, 37200 Tours, France

Munnier, E; Université de Tours, EA6295 Nanomédicaments et Nanosondes, 31 Avenue Monge, 37200 Tours, France

Chourpa, I; Université de Tours, EA6295 Nanomédicaments et Nanosondes, 31 Avenue Monge, 37200 Tours, France

Allard-Vannier, E; Université de Tours, EA6295 Nanomédicaments et Nanosondes, 31 Avenue Monge, 37200 Tours, France

David, S; Université de Tours, EA6295 Nanomédicaments et Nanosondes, 31 Avenue Monge, 37200 Tours, France. Electronic address: stephanie.david@univ-tours.fr

Language :

English

Title :

Versatile electrostatically assembled polymeric siRNA nanovectors: Can they overcome the limits of siRNA tumor delivery?

Publication date :

15 August 2019

Journal title :

International Journal of Pharmaceutics

ISSN :

0378-5173

eISSN :

1873-3476

Publisher :

Elsevier B.V., Netherlands

Volume :

567

Pages :

118432

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0378517319304661?httpAccept=text/xml

Funders :

Ligue Contre le Cancer

Funding text :

This work was supported by the “Institut National du Cancer ( INCa )”, the “Fondation ARC” and the “Ligue Nationale Contre le Cancer (LNCC)”, France (ARC_INCa_LNCC_7636, EVASION project and INTERACTION project), the “Région Centre-Val de Loire” and the “Cancéropole Grand Ouest” (MATURE project).

Available on ORBi :

since 18 May 2022

Statistics

Number of views

37 (0 by ULiège)

Number of downloads

37 (0 by ULiège)

More statistics

Scopus citations^®

20

Scopus citations^®
without self-citations

16

OpenCitations

13

OpenAlex citations

22

Bibliography

Aagaard, L., Rossi, J.J., RNAi therapeutics: principles, prospects and challenges. Adv. Drug Deliv. Rev. 59 (2007), 75–86, 10.1016/j.addr.2007.03.005.
Al Shaer, D., Al Musaimi, O., Albericio, F., de la Torre, B., Al Shaer, D., Al Musaimi, O., Albericio, F., de la Torre, B.G., 2018 FDA tides harvest. Pharmaceuticals, 12, 2019, 52, 10.3390/ph12020052.
Allen, T.M., Ligand-targeted therapeutics in anticancer therapy. Nat. Rev. Cancer 2 (2002), 750–763, 10.1038/nrc903.
An, S., He, D., Wagner, E., Jiang, C., Peptide-like polymers exerting effective glioma-targeted siRNA delivery and release for therapeutic application. Small 11 (2015), 5142–5150, 10.1002/smll.201501167.
Arnold, A.E., Czupiel, P., Shoichet, M., Engineered polymeric nanoparticles to guide the cellular internalization and trafficking of small interfering ribonucleic acids. J. Control. Release 259 (2017), 3–15, 10.1016/j.jconrel.2017.02.019.
Azevedo, C., Macedo, M.H., Sarmento, B., Strategies for the enhanced intracellular delivery of nanomaterials. Drug Discov. Today 23 (2018), 944–959, 10.1016/J.DRUDIS.2017.08.011.
Bareford, L.M., Swaan, P.W., Endocytic mechanisms for targeted drug delivery. Adv. Drug Deliv. Rev. 59 (2007), 748–758, 10.1016/j.addr.2007.06.008.
Behlke, M.A., Progress towards in vivo use of siRNAs. Mol. Ther. 13 (2006), 644–670, 10.1016/J.YMTHE.2006.01.001.
Behr, J.-P., The proton sponge: a trick to enter cells the viruses did not exploit. Chim. Int. J. Chem. 51 (1997), 34–36.
Ben Djemaa, S., David, S., Hervé-Aubert, K., Falanga, A., Galdiero, S., Allard-Vannier, E., Chourpa, I., Munnier, E., Formulation and in vitro evaluation of a siRNA delivery nanosystem decorated with gH625 peptide for triple negative breast cancer theranosis. Eur. J. Pharm. Biopharm. 131 (2018), 99–108, 10.1016/j.ejpb.2018.07.024.
Boussif, O., Lezoualc'ht, F., Zanta, M.A., Mergnyt, D., Schermant, D., Demeneixt, B., Behr, J.-P., A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Biochemistry, 1995.
Bruniaux, J., Djemaa, S. Ben, Hervé-Aubert, K., Marchais, H., Chourpa, I., David, S., Ben Djemaa, S., Hervé-Aubert, K., Marchais, H., Chourpa, I., David, S., Stealth magnetic nanocarriers of siRNA as platform for breast cancer theranostics. Int. J. Pharm. 532 (2017), 660–668, 10.1016/j.ijpharm.2017.05.022.
Carthew, Richard W., Sontheimer, E.J., Carthew, R.W., Sontheimer, E.J., Origins and mechanisms of miRNAs and siRNAs. Cell 136 (2009), 642–655, 10.1016/j.cell.2009.01.035.
Cavalieri, F., Beretta, G.L., Cui, J., Braunger, J.A., Yan, Y., Richardson, J.J., Tinelli, S., Folini, M., Zaffaroni, N., Caruso, F., Redox-sensitive PEG-polypeptide nanoporous particles for survivin silencing in prostate cancer cells. Biomacromolecules 16 (2015), 2168–2178, 10.1021/acs.biomac.5b00562.
Cavallaro, G., Sardo, C., Craparo, E.F., Porsio, B., Giammona, G., Polymeric nanoparticles for siRNA delivery: production and applications. Int. J. Pharm. 525 (2017), 313–333, 10.1016/J.IJPHARM.2017.04.008.
Chen, M., Gao, S., Dong, M., Song, J., Yang, C., Howard, K.A., Al, C.E.T., Chitosan/siRNA nanoparticles encapsulated in PLGA nanofibers for siRNA delivery. ACS Nano, 2012, 4835–4844.
Chen, Y., Gu, H., Zhang, D.S.-Z., Li, F., Liu, T., Xia, W., Highly effective inhibition of lung cancer growth and metastasis by systemic delivery of siRNA via multimodal mesoporous silica-based nanocarrier. Biomaterials 35 (2014), 10058–10069, 10.1016/J.BIOMATERIALS.2014.09.003.
Chiper, M., Tounsi, N., Kole, R., Kichler, A., Zuber, G., Self-aggregating 1.8 kDa polyethylenimines with dissolution switch at endosomal acidic pH are delivery carriers for plasmid DNA, mRNA, siRNA and exon-skipping oligonucleotides. J. Control. Release 246 (2017), 60–70, 10.1016/J.JCONREL.2016.12.005.
Conde, J., Dias, J.T., Grazú, V., Moros, M., Baptista, P.V., de la Fuente, J.M., Revisiting 30 years of biofunctionalization and surface chemistry of inorganic nanoparticles for nanomedicine. Front. Chem. 2 (2014), 1–27, 10.3389/fchem.2014.00048.
Conner, S.D., Schmid, S.L., Regulated portals of entry into the cell. Nature 422 (2003), 37–44, 10.1038/nature01451.
Corbet, C., Ragelle, H., Pourcelle, V., Vanvarenberg, K., Marchand-Brynaert, J., Préat, V., Feron, O., Delivery of siRNA targeting tumor metabolism using non-covalent PEGylated chitosan nanoparticles: identification of an optimal combination of ligand structure, linker and grafting method. J. Control. Release 223 (2016), 53–63, 10.1016/j.jconrel.2015.12.020.
Creusat, G., Rinaldi, A.S., Weiss, E., Elbaghdadi, R., Remy, J.S., Mulherkar, R., Zuber, G., Proton sponge trick for ph-sensitive disassembly of polyethylenimine-based sirna delivery systems. Bioconjug. Chem. 21 (2010), 994–1002, 10.1021/bc100010k.
Creusat, G., Thomann, J.-S., Maglott, A., Pons, B., Dontenwill, M., Guérin, E., Frisch, B., Zuber, G., Pyridylthiourea-grafted polyethylenimine offers an effective assistance to siRNA-mediated gene silencing in vitro and in vivo. J. Control. Release 157 (2012), 418–426, 10.1016/J.JCONREL.2011.10.007.
Creusat, G., Zuber, G., Self-Assembling polyethylenimine derivatives mediate efficient siRNA delivery in mammalian cells. ChemBioChem 9 (2008), 2787–2789, 10.1002/cbic.200800540.
David, S., Resnier, P., Guillot, A., Pitard, B., Benoit, J.-P., Passirani, C., siRNA LNCs – a novel platform of lipid nanocapsules for systemic siRNA administration. Eur. J. Pharm. Biopharm. 81 (2012), 448–452, 10.1016/J.EJPB.2012.02.010.
Derfus, A.M., Chen, A.A., Min, D.-H., Ruoslahti, E., Bhatia, S.N., Targeted quantum dot conjugates for siRNA delivery. Bioconjug. Chem. 18 (2007), 1391–1396, 10.1021/bc060367e.
Ding, Y., Wang, W., Feng, M., Wang, Y., Zhou, J., Ding, X., Zhou, X., Liu, C., Wang, R., Zhang, Q., A biomimetic nanovector-mediated targeted cholesterol-conjugated siRNA delivery for tumor gene therapy. Biomaterials 33 (2012), 8893–8905, 10.1016/j.biomaterials.2012.08.057.
Ding, Y., Wang, Y., Zhou, J., Gu, X., Wang, W., Liu, C., Bao, X., Wang, C., Li, Y., Zhang, Q., Direct cytosolic siRNA delivery by reconstituted high density lipoprotein for target-specific therapy of tumor angiogenesis. Biomaterials 35 (2014), 7214–7227, 10.1016/j.biomaterials.2014.05.009.
Dohmen, C., Fröhlich, T., Lächelt, U., Röhl, I., Vornlocher, H.-P., Hadwiger, P., Wagner, E., Defined folate-PEG-siRNA conjugates for receptor-specific gene silencing. Mol. Ther. – Nucleic Acids, 1, 2012, e7, 10.1038/MTNA.2011.10.
Dominska, M., Dykxhoorn, D.M., Breaking down the barriers: siRNA delivery and endosome escape. J Cell Sci 123 (2010), 1183–1189, 10.1242/jcs.066399.
Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., Tuschl, T., Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 (2001), 494–498, 10.1038/35078107.
Fan, C., Wang, S., Hong, J.W., Bazan, G.C., Plaxco, K.W., Heeger, A.J., Beyond superquenching: Hyper-efficient energy transfer from conjugated polymers to gold nanoparticles. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 6297–6301, 10.1073/pnas.1132025100.
Ferrari, M., Sun, T., Shen, H., Gilmore, J.H., Nanovector delivery of siRNA for cancer therapy. Cancer Gene Ther. 19 (2012), 1883–1889, 10.1038/cgt.2012.22.
Fischer, D., Bieber, T., Li, Y., Elsässer, H.P., Kissel, T., 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 (1999), 1273–1279, 10.1023/A:1014861900478.
Foillard, S., Zuber, G., Doris, E., Polyethylenimine–carbon nanotube nanohybrids for siRNA-mediated gene silencing at cellular level. Nanoscale, 3, 2011, 1461, 10.1039/c0nr01005g.
Forster, J.C., Harriss-Phillips, W.M., Douglass, M.J., Bezak, E., A review of the development of tumor vasculature and its effects on the tumor microenvironment. Hypoxia (Auckland, N.Z.) 5 (2017), 21–32, 10.2147/HP.S133231.
Fröhlich, T., Edinger, D., Kläger, R., Troiber, C., Salcher, E., Badgujar, N., Martin, I., Schaffert, D., Cengizeroglu, A., Hadwiger, P., Vornlocher, H.-P., Wagner, E., Structure–activity relationships of siRNA carriers based on sequence-defined oligo (ethane amino) amides. J. Control. Release 160 (2012), 532–541, 10.1016/J.JCONREL.2012.03.018.
Galdiero, S., Falanga, A., Morelli, G., Galdiero, M., gH625: A milestone in understanding the many roles of membranotropic peptides. Biochim. Biophys. Acta – Biomembr. 1848 (2015), 16–25, 10.1016/j.bbamem.2014.10.006.
Gary, D.J., Puri, N., Won, Y.-Y., Polymer-based siRNA delivery: perspectives on the fundamental and phenomenological distinctions from polymer-based DNA delivery. J. Control. Release 121 (2007), 64–73, 10.1016/J.JCONREL.2007.05.021.
Gavrilov, K., Saltzman, W.M., Therapeutic siRNA: principles, challenges, and strategies. Yale J. Biol. Med. 85 (2012), 187–200.
Gillies, R.J., Schornack, P.A., Secomb, T.W., Raghunand, N., Causes and effects of heterogeneous perfusion in tumors. Neoplasia 1 (1999), 197–207.
Goren, D., Horowitz, A.T., Zalipsky, S., Woodle, M.C., Yarden, Y., Gabizon, A., Targeting of stealth liposomes to erbB-2 (Her/2) receptor: in vitro and in vivo studies. Br. J. Cancer 74 (1996), 1749–1756.
Guruprasath, P., Kim, J., Gunassekaran, G.R., Chi, L., Kim, S., Park, R.-W., Kim, S.-H., Baek, M.-C., Bae, S.M., Kim, S.Y., Kim, D.-K., Park, I.-K., Kim, W.-J., Lee, B., Interleukin-4 receptor-targeted delivery of Bcl-xL siRNA sensitizes tumors to chemotherapy and inhibits tumor growth. Biomaterials 142 (2017), 101–111, 10.1016/j.biomaterials.2017.07.024.
Haussecker, D., Current issues of RNAi therapeutics delivery and development. J. Control. Release 195 (2014), 49–54, 10.1016/j.jconrel.2014.07.056.
Heldin, C.-H., Rubin, K., Pietras, K., Östman, A., High interstitial fluid pressure – an obstacle in cancer therapy. Nat. Rev. Cancer 4 (2004), 806–813, 10.1038/nrc1456.
Huang, Y., Wang, X., Huang, W., Cheng, Q., Zheng, S., Guo, S., Cao, H., Liang, X.J., Du, Q., Liang, Z., Systemic administration of siRNA via cRGD-containing Peptide. Sci. Rep., 5, 2015, 12458, 10.1038/srep12458.
Huh, M.S., Lee, S.Y., Park, S., Lee, Seulki, Chung, H., Lee, Sojin, Choi, Y., Oh, Y.K., Park, J.H., Jeong, S.Y., Choi, K., Kim, K., Kwon, I.C., Tumor-homing glycol chitosan/polyethylenimine nanoparticles for the systemic delivery of siRNA in tumor-bearing mice. J. Control. Release 144 (2010), 134–143, 10.1016/j.jconrel.2010.02.023.
Jabir, N.R., Tabrez, S., Ashraf, G.M., Shakil, S., Damanhouri, G.A., Kamal, M.A., Nanotechnology-based approaches in anticancer research. Int. J. Nanomed. 7 (2012), 4391–4408, 10.2147/IJN.S33838.
Jaganathan, H., Mitra, S., Srinivasan, S., Dave, B., Godin, B., Design and in vitro evaluation of layer by layer siRNA nanovectors targeting breast tumor initiating cells. PLoS One, 9, 2014, e91986, 10.1371/journal.pone.0091986.
Jain, R.K., Stylianopoulos, T., Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7 (2010), 653–664, 10.1038/nrclinonc.2010.139.
Jiang, T., Zhang, Z., Zhang, Y., Lv, H., Zhou, J., Li, C., Hou, L., Zhang, Q., Dual-functional liposomes based on pH-responsive cell-penetrating peptide and hyaluronic acid for tumor-targeted anticancer drug delivery. Biomaterials 33 (2012), 9246–9258, 10.1016/j.biomaterials.2012.09.027.
Jonker, C., de Heus, C., Faber, L., ten Brink, C., Potze, L., Fermie, J., Liv, N., Klumperman, J., An adapted protocol to overcome endosomal damage caused by polyethylenimine (PEI) mediated transfections. Matters, 3, 2017, e201711000012 https://doi.org/10.19185/matters.201711000012.
Kaczmarek, J.C., Kowalski, P.S., Anderson, D.G., Advances in the delivery of RNA therapeutics: from concept to clinical reality. Genome Med., 9, 2017, 60, 10.1186/s13073-017-0450-0.
Kang, L., Fan, B., Sun, P., Huang, W., Jin, M., Wang, Q., Gao, Z., An effective tumor-targeting strategy utilizing hypoxia-sensitive siRNA delivery system for improved anti-tumor outcome. Acta Biomater. 44 (2016), 341–354, 10.1016/J.ACTBIO.2016.08.029.
Kievit, F.M., Veiseh, O., Fang, C., Bhattarai, N., Lee, D., Ellenbogen, R.G., Zhang, M., Chlorotoxin labeled magnetic nanovectors for targeted gene delivery to glioma. ACS Nano 4 (2010), 4587–4594, 10.1021/nn1008512.
Kim, E.J., Shim, G., Kim, K., Kwon, I.C., Oh, Y.K., Shim, C.K., Hyaluronic acid complexed to biodegradable poly L-arginine for targeted delivery of siRNAs. J. Gene Med. 11 (2009), 791–803, 10.1002/jgm.1352.
Krivitsky, A., Polyak, D., Scomparin, A., Eliyahu, S., Ofek, P., Tiram, G., Kalinski, H., Avkin-Nachum, S., Feiner Gracia, N., Albertazzi, L., Satchi-Fainaro, R., Amphiphilic poly(α)glutamate polymeric micelles for systemic administration of siRNA to tumors. Nanomedicine Nanotechnology. Biol. Med. 14 (2018), 303–315, 10.1016/j.nano.2017.10.012.
Landry, B., Aliabadi, H.M., Samuel, A., Gül-Uludağ, H., Jiang, X., Kutsch, O., Uludağ, H., Effective non-viral delivery of siRNA to acute myeloid leukemia cells with lipid-substituted polyethylenimines. PLoS One, 7, 2012, e44197, 10.1371/journal.pone.0044197.
Lee, D.-J., He, D., Kessel, E., Padari, K., Kempter, S., Lächelt, U., Rädler, J.O., Pooga, M., Wagner, E., Tumoral gene silencing by receptor-targeted combinatorial siRNA polyplexes. J. Control. Release 244 (2016), 280–291, 10.1016/J.JCONREL.2016.06.011.
Lee, D.-J., Kessel, E., Edinger, D., He, D., Klein, P.M., Voith von Voithenberg, L., Lamb, D.C., Lächelt, U., Lehto, T., Wagner, E., Dual antitumoral potency of EG5 siRNA nanoplexes armed with cytotoxic bifunctional glutamyl-methotrexate targeting ligand. Biomaterials 77 (2016), 98–110, 10.1016/J.BIOMATERIALS.2015.11.004.
Lee, J.E., Lee, K., Nam, J.A., Kim, A., Lee, S.Y., Lee, M.S., Kim, N.W., Yin, Y., Park, J.W., Park, S.Y., Jeong, J.H., Cellular delivery of siRNA using Poly(2-dimethylaminoethyl methacrylate)- functionalized graphene oxide nano-wrap. Macromol. Res. 26 (2018), 1115–1122, 10.1007/s13233-019-7017-4.
Liu, C., Liu, X., Rocchi, P., Qu, F., Iovanna, J.L., Peng, L., Arginine-terminated generation 4 PAMAM dendrimer as an effective nanovector for functional siRNA delivery in vitro and in vivo. Bioconjug. Chem. 25 (2014), 521–532, 10.1021/bc4005156.
Liu, G., Xie, J., Zhang, F., Wang, Z.-Y., Luo, K., Zhu, L., Quan, Q.-M., Niu, G., Lee, S., Ai, H., Chen, X., N-Alkyl-PEI functional iron oxide nanocluster for efficient siRNA delivery**. Small 7 (2011), 2742–2749, 10.1002/smll.201100825.
Liu, X., Peng, L., Dendrimer nanovectors for siRNA delivery. Methods Mol. Biol. 1364 (2016), 127–142, 10.1007/978-1-4939-3112-5_11.
Lodish, H., Berk, A., Zipursky, S.L., Matsudaira, P., Baltimore, D., Darnell, J., Receptor-Mediated Endocytosis and the Sorting of. 2000, Internalized Proteins.
Lu, A.-H., Salabas, E.L., Schüth, F., Magnetic nanoparticles: synthesis, protection, functionalization, and application. Angew. Chem. Int. Ed. Engl. 46 (2007), 1222–1244, 10.1002/anie.200602866.
Lv, H., Zhang, S., Wang, B., Cui, S., Yan, J., Toxicity of cationic lipids and cationic polymers in gene delivery. J. Control. Release Off. J. Control. Release Soc. 114 (2006), 100–109, 10.1016/j.jconrel.2006.04.014.
Malhotra, M., Tomaro-Duchesneau, C., Saha, S., Prakash, S., Intranasal, siRNA delivery to the Brain by TAT/MGF tagged PEGylated chitosan nanoparticles. J. Pharm. 2013 (2013), 1–10, 10.1155/2013/812387.
Marsh, M., McMahon, H.T., The structural era of endocytosis. Science 285 (1999), 215–220.
de Menezes, D.E.L., Pilarski, L.M., Allen, T.M., In vitro and in vivo targeting of immunoliposomal doxorubicin to human B-Cell Lymphoma. Cancer Res. 58 (1998), 3320–3330.
Mi, R.P., Ki, O.H., In, K.H., Myung, H.C., Jae, W.N., Yun, J.C., Chong, S.C., Degradable polyethylenimine-alt-poly(ethylene glycol) copolymers as novel gene carriers. J. Control. Release 105 (2005), 367–380, 10.1016/j.jconrel.2005.04.008.
Minakuchi, Y., Takeshita, F., Kosaka, N., Sasaki, H., Yamamoto, Y., Kouno, M., Honma, K., Nagahara, S., Hanai, K., Sano, A., Kato, T., Terada, M., Ochiya, T., Atelocollagen-mediated synthetic small interfering RNA delivery for effective gene silencing in vitro and in vivo. Nucleic Acids Res., 32, 2004, e109, 10.1093/nar/gnh093.
Miteva, M., Kirkbride, K.C., Kilchrist, K.V., Werfel, T.A., Li, H., Nelson, C.E., Gupta, M.K., Giorgio, T.D., Duvall, C.L., Tuning PEGylation of mixed micelles to overcome intracellular and systemic siRNA delivery barriers. Biomaterials 38 (2015), 97–107, 10.1016/j.biomaterials.2014.10.036.
Mok, H., Veiseh, O., Fang, C., Kievit, F.M., Wang, F.Y., Park, J.O., Zhang, M., PH-sensitive siRNA nanovector for targeted gene silencing and cytotoxic effect in cancer cells. Mol. Pharm. 7 (2010), 1930–1939, 10.1021/mp100221h.
Mokhtarieh, A.A., Lee, J., Kim, S., Lee, M.K., Preparation of siRNA encapsulated nanoliposomes suitable for siRNA delivery by simply discontinuous mixing. Biochim. Biophys. Acta – Biomembr. 1860 (2018), 1318–1325, 10.1016/J.BBAMEM.2018.02.027.
Mu, P., Nagahara, S., Makita, N., Tarumi, Y., Kadomatsu, K., Takei, Y., Systemic delivery of siRNA specific to tumor mediated by atelocollagen: combined therapy using siRNA targeting Bcl-xL and cisplatin against prostate cancer. Int. J. Cancer 125 (2009), 2978–2990, 10.1002/ijc.24382.
Muratovska, A., Eccles, M.R., Conjugate for efficient delivery of short interfering RNA (siRNA) into mammalian cells. FEBS Lett. 558 (2004), 63–68, 10.1016/S0014-5793(03)01505-9.
Nguyen, J., Szoka, F.C., Nucleic acid delivery: the missing pieces of the puzzle?. Acc. Chem. Res. 45 (2012), 1153–1162, 10.1021/ar3000162.
Nikam, R.R., Gore, K.R., Journey of siRNA: clinical developments and targeted delivery. Nucleic Acid Ther. 28 (2018), 209–224, 10.1089/nat.2017.0715.
Oh, B., Lee, M., Combined delivery of HMGB-1 box A peptide and S1PLyase siRNA in animal models of acute lung injury. J. Control. Release 175 (2014), 25–35, 10.1016/j.jconrel.2013.12.008.
Ohsaki, M., Okuda, T., Wada, A., Hirayama, T., Niidome, T., Aoyagi, H., In vitro gene transfection using dendritic poly(L-lysine). Bioconjug. Chem. 13 (2002), 510–517, 10.1021/bc015525a.
Owens, D.E. III, Peppas, N.A., Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307 (2006), 93–102, 10.1016/j.ijpharm.2005.10.010.
Ozcan, G., Ozpolat, B., Coleman, R.L., Sood, A.K., Lopez-Berestein, G., Medicine, R., Preclinical and clinical development of siRNA-based therapeutics. Adv. Drug Deliv. Rev. 87 (2015), 108–119, 10.1016/j.addr.2015.01.007.
Pan, J., Ruan, W., Qin, M., Long, Y., Wan, T., Yu, K., Zhai, Y., Wu, C., Xu, Y., Intradermal delivery of STAT3 siRNA to treat melanoma via dissolving microneedles. Sci. Rep., 8, 2018, 1117, 10.1038/s41598-018-19463-2.
Pan, X., Thompson, R., Meng, X., Wu, D., Xu, L., Tumor-targeted RNA-interference: functional non-viral nanovectors. Am. J. Cancer Res. 1 (2010), 25–42.
Parmar, M.B., Bahadur, R., Lö, R., Uludağ, H., Additive polyplexes to undertake siRNA therapy against CDC20 and survivin in breast cancer cells. Biomacromolecules 19:11 (2018), 4193–4206, 10.1021/acs.biomac.8b00918.
Pärnaste, L., Arukuusk, P., Langel, K., Tenson, T., Langel, Ü., The formation of nanoparticles between small interfering RNA and amphipathic cell-penetrating peptides. Mol. Ther. Nucleic Acids 7 (2017), 1–10, 10.1016/j.omtn.2017.02.003.
Perche, F., Biswas, S., Patel, N.R., Torchilin, V.P., Hypoxia-responsive copolymer for siRNA delivery. Methods Mole. Biol., 2016, 139–162, 10.1007/978-1-4939-3148-4_12.
Perche, F., Biswas, S., Wang, T., Zhu, L., Torchilin, V.P., Hypoxia-targeted siRNA delivery. Angew. Chemie – Int. Ed. 53 (2014), 3362–3366, 10.1002/anie.201308368.
Pittella, F., Zhang, M., Lee, Y., Kim, H.J., Tockary, T., Osada, K., Ishii, T., Miyata, K., Nishiyama, N., Kataoka, K., Enhanced endosomal escape of siRNA-incorporating hybrid nanoparticles from calcium phosphate and PEG-block charge-conversional polymer for efficient gene knockdown with negligible cytotoxicity. Biomaterials 32 (2011), 3106–3114, 10.1016/j.biomaterials.2010.12.057.
Prokop, A., Davidson, J.M.J., Nanovehicular intracellular delivery systems. J. Pharm. Sci. 97 (2008), 3518–3590, 10.1002/jps.21270.
Ragelle, H., Colombo, S., Pourcelle, V., Vanvarenberg, K., Vandermeulen, G., Bouzin, C., Marchand-Brynaert, J., Feron, O., Foged, C., Préat, V., Intracellular siRNA delivery dynamics of integrin-targeted, PEGylated chitosan-poly(ethylene imine) hybrid nanoparticles: a mechanistic insight. J. Control. Release 211 (2015), 1–9, 10.1016/j.jconrel.2015.05.274.
Ratcliff, F., Harrison, B.D., Baulcombe, D.C., A similarity between viral defense and gene silencing in plants. Science (80) 276 (1997), 1558–1560, 10.1126/science.276.5318.1558.
Rehman, Z., ur Hoekstra, D., Zuhorn, I.S., Mechanism of polyplex- and lipoplex-mediated delivery of nucleic acids: Real-time visualization of transient membrane destabilization without endosomal lysis. ACS Nano 7 (2013), 3767–3777, 10.1021/nn3049494.
Reischl, D., Zimmer, A., Drug delivery of siRNA therapeutics: potentials and limits of nanosystems. Nanomedicine Nanotechnology. Biol. Med. 5 (2009), 8–20, 10.1016/J.NANO.2008.06.001.
Resnier, P., Montier, T., Mathieu, V., Benoit, J.-P.P., Passirani, C., A review of the current status of siRNA nanomedicines in the treatment of cancer. Biomaterials 34 (2013), 6429–6443, 10.1016/j.biomaterials.2013.04.060.
Reynolds, A., Anderson, E.M., Vermeulen, A., Fedorov, Y., Robinson, K., Leake, D., Karpilow, J., Marshall, W.S., Khvorova, A., Induction of the interferon response by siRNA is cell type- and duplex length-dependent. RNA 12 (2006), 988–993, 10.1261/rna.2340906.
Richards Grayson, A.C., Doody, A.M., Putnam, D., Biophysical and structural characterization of polyethylenimine-mediated siRNA delivery in vitro. Pharm. Res. 23 (2006), 1868–1876, 10.1007/s11095-006-9009-2.
Rizk, M., Tüzmen, Ş., Update on the clinical utility of an RNA interference-based treatment: focus on Patisiran. Pharmgenomics. Pers. Med. 10 (2017), 267–278, 10.2147/PGPM.S87945.
Rosi, N.L., Giljohann, D.A., Thaxton, C.S., Lytton-Jean, A.K.R., Han, M.S., Mirkin, C.A., Oligonucleotide-modified gold nanoparticles for intracellular gene regulation. Science 312 (2006), 1027–1030, 10.1126/science.1125559.
Rothbard, J.B., Jessop, T.C., Lewis, R.S., Murray, B.A., Wender, P.A., Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J. Am. Chem. Soc. 126 (2004), 9506–9507, 10.1021/ja0482536.
Scherer, F., Anton, M., Schillinger, U., Henke, J., Bergemann, C., Krüger, A., Gänsbacher, B., Plank, C., Magnetofection: enhancing and targeting gene delivery by magnetic force in vitro and in vivo. Gene Ther. 9 (2002), 102–109, 10.1038/sj.gt.3301624.
Schmohl, K.A., Gupta, A., Grünwald, G.K., Trajkovic-Arsic, M., Klutz, K., Braren, R., Schwaiger, M., Nelson, P.J., Ogris, M., Wagner, E., Siveke, J.T., Spitzweg, C., Imaging and targeted therapy of pancreatic ductal adenocarcinoma using the theranostic sodium iodide symporter (NIS) gene. Oncotarget 8 (2017), 33393–33404 https://doi.org/10.18632/oncotarget.16499.
Schubert, U.S., Traeger, A., Bus, T., The great escape: how cationic polyplexes overcome the endosomal barrier. J. Mater. Chem. B 6 (2018), 6904–6918, 10.1039/C8TB00967H.
Shakiba, A., Zenasni, O., Marquez, M.D., Lee, T.R., Advanced drug delivery via self-assembled monolayer-coated nanoparticles. AIMS Bioeng. 4 (2017), 275–299, 10.3934/bioeng.2017.2.275.
Shim, M.S., Kwon, Y.J., Efficient and targeted delivery of siRNA in vivo. FEBS J. 277 (2010), 4814–4827, 10.1111/j.1742-4658.2010.07904.x.
Song, E., Lee, S.-K., Wang, J., Ince, N., Ouyang, N., Min, J., Chen, J., Shankar, P., Lieberman, J., RNA interference targeting Fas protects mice from fulminant hepatitis. Nat. Med. 9 (2003), 347–351, 10.1038/nm828.
Song, W.-J., Du, J.-Z., Sun, T.-M., Zhang, P.-Z., Wang, J., Gold nanoparticles capped with polyethyleneimine for enhanced sirna delivery. Small 6 (2010), 239–246, 10.1002/smll.200901513.
Sosnovik, D.E., Nahrendorf, M., Weissleder, R., Magnetic nanoparticles for MR imaging: agents, techniques and cardiovascular applications. Basic Res. Cardiol. 103 (2008), 122–130, 10.1007/s00395-008-0710-7.
Sun, C.-Y.Y., Shen, S., Xu, C.-F.F., Li, H.-J.J., Liu, Y., Cao, Z.-T.T., Yang, X.-Z.Z., Xia, J.-X.X., Wang, J., Tumor acidity-sensitive polymeric vector for active targeted siRNA delivery. J. Am. Chem. Soc. 137 (2015), 15217–15224, 10.1021/jacs.5b09602.
Sun, C., Lee, J.S.H., Zhang, M., Magnetic nanoparticles in mr imaging and drug delivery. Adv. Drug Deliv. Rev. 60 (2008), 1252–1265, 10.1016/j.addr.2008.03.018.
Sun, P., Huang, W., Jin, M., Wang, Q., Fan, B., Kang, L., Gao, Z., Chitosan-based nanoparticles for survivin targeted siRNA delivery in breast tumor therapy and preventing its metastasis. Int. J. Nanomed. 11 (2016), 4931–4945, 10.2147/IJN.S105427.
Tabernero, J., Shapiro, G.I., LoRusso, P.M., Cervantes, A., Schwartz, G.K., Weiss, G.J., Paz-Ares, L., Cho, D.C., Infante, J.R., Alsina, M., Gounder, M.M., Falzone, R., Harrop, J., White, A.C.S., Toudjarska, I., Bumcrot, D., Meyers, R.E., Hinkle, G., Svrzikapa, N., Hutabarat, R.M., Clausen, V.A., Cehelsky, J., Nochur, S.V., Gamba-Vitalo, C., Vaishnaw, A.K., Sah, D.W.Y., Gollob, J.A., Burris, H.A., First-in-humans trial of an RNA interference therapeutic targeting VEGF and KSP in cancer patients with liver involvement. Cancer Discov. 3 (2013), 406–417, 10.1158/2159-8290.CD-12-0429.
Takeshita, F., Minakuchi, Y., Nagahara, S., Honma, K., Sasaki, H., Hirai, K., Teratani, T., Namatame, N., Yamamoto, Y., Hanai, K., Kato, T., Sano, A., Ochiya, T., Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo. Proc. Natl. Acad. Sci. USA 102 (2005), 12177–12182, 10.1073/pnas.0501753102.
Tan, S.J., Kiatwuthinon, P., Roh, Y.H., Kahn, J.S., Luo, D., Engineering nanocarriers for siRNA delivery. Small 7 (2011), 841–856, 10.1002/smll.201001389.
Tatiparti, K., Sau, S., Kashaw, S.K., Iyer, A.K., siRNA delivery strategies: a comprehensive review of recent developments. Nanomater. (Basel, Switzerland), 7, 2017, 10.3390/nano7040077.
Tian, H., Xiong, W., Wei, J., Wang, Y., Chen, X., Jing, X., Zhu, Q., Gene transfection of hyperbranched PEI grafted by hydrophobic amino acid segment PBLG. Biomaterials 28 (2007), 2899–2907, 10.1016/j.biomaterials.2007.02.027.
Trützschler, A.K., Bus, T., Reifarth, M., Brendel, J.C., Hoeppener, S., Traeger, A., Schubert, U.S., Beyond gene transfection with methacrylate-based polyplexes – the influence of the amino substitution pattern. Bioconjug. Chem. 29 (2018), 2181–2194, 10.1021/acs.bioconjchem.8b00074.
Tuma, P.L., Hubbard, A.L., Transcytosis: crossing cellular barriers. Physiol. Rev. 83 (2003), 871–932, 10.1152/physrev.00001.2003.
Veiseh, O., Kievit, F.M., Ellenbogen, R.G., Zhang, M., Cancer cell invasion: treatment and monitoring opportunities in nanomedicine. Adv. Drug Deliv. Rev Target Cell Movement Tumor Cardiovascular Diseases 63 (2011), 582–596, 10.1016/j.addr.2011.01.010.
Veiseh, O., Kievit, F.M., Fang, C., Mu, N., Jana, S., Leung, M.C., Mok, H., Ellenbogen, R.G., Park, J.O., Zhang, M., Chlorotoxin bound magnetic nanovector tailored for cancer cell targeting, imaging, and siRNA delivery. Biomaterials 31 (2010), 8032–8042, 10.1016/j.biomaterials.2010.07.016.
Veiseh, O., Kievit, F.M., Mok, H., Ayesh, J., Clark, C., Fang, C., Leung, M., Arami, H., Park, J.O., Zhang, M., Cell transcytosing poly-arginine coated magnetic nanovector for safe and effective siRNA delivery. Biomaterials 32 (2011), 5717–5725, 10.1016/j.biomaterials.2011.04.039.
Veiseh, O., Sun, C., Fang, C., Bhattarai, N., Gunn, J., Kievit, F., Du, K., Pullar, B., Lee, D., Ellenbogen, R.G., Olson, J., Zhang, M., Specific targeting of brain tumors with an optical/magnetic resonance imaging nanoprobe across the blood-brain barrier. Cancer Res. 69 (2009), 6200–6207, 10.1158/0008-5472.CAN-09-1157.
Venditti, I., Morphologies and functionalities of polymeric nanocarriers as chemical tools for drug delivery: a review. J. King Saud Univ. – Sci., 2017, 10.1016/j.jksus.2017.10.004.
Videira, M., Arranja, A., Rafael, D., Gaspar, R., Preclinical development of siRNA therapeutics: towards the match between fundamental science and engineered systems. Nanomedicine Nanotechnology. Biol. Med. 10 (2014), 689–702, 10.1016/j.nano.2013.11.018.
Wang, F., Wang, Y., Zhang, X., Zhang, W., Guo, S., Jin, F., Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery. J. Control. Release 174 (2014), 126–136, 10.1016/j.jconrel.2013.11.020.
Wang, J., Lu, Z., Wientjes, M.G., Au, J.L.-S., Delivery of siRNA therapeutics: barriers and carriers. AAPS J. 12 (2010), 492–503, 10.1208/s12248-010-9210-4.
Wang, T., Shigdar, S., Shamaileh, H. Al, Gantier, M.P., Yin, W., Xiang, D., Wang, L., Zhou, S.-F., Hou, Y., Wang, P., Zhang, W., Pu, C., Duan, W., Challenges and opportunities for siRNA-based cancer treatment. Cancer Lett. 387 (2017), 77–83, 10.1016/J.CANLET.2016.03.045.
Wang, X.-L., Xu, R., Wu, X., Gillespie, D., Jensen, R., Lu, Z.-R., Targeted systemic delivery of a therapeutic siRNA with a multifunctional carrier controls tumor proliferation in mice. Mol. Pharm. 6 (2009), 738–746, 10.1021/mp800192d.
Werfel, T.A., Jackson, M.A., Kavanaugh, T.E., Kirkbride, K.C., Miteva, M., Giorgio, T.D., Duvall, C., Combinatorial optimization of PEG architecture and hydrophobic content improves ternary siRNA polyplex stability, pharmacokinetics, and potency in vivo. J. Control. Release 255 (2017), 12–26, 10.1016/j.jconrel.2017.03.389.
Xie, Y., Qiao, H., Su, Z., Chen, M., Ping, Q., Sun, M., PEGylated carboxymethyl chitosan/calcium phosphate hybrid anionic nanoparticles mediated hTERT siRNA delivery for anticancer therapy. Biomaterials 35 (2014), 7978–7991, 10.1016/j.biomaterials.2014.05.068.
Yin, T., Liu, J., Zhao, Z., Dong, L., Cai, H., Yin, L., Zhou, J., Huo, M., Smart nanoparticles with a detachable outer shell for maximized synergistic antitumor efficacy of therapeutics with varying physicochemical properties. J. Control. Release 243 (2016), 54–68, 10.1016/j.jconrel.2016.09.036.
Zhang, W., Müller, K., Kessel, E., Reinhard, S., He, D., Klein, P.M., Höhn, M., Rödl, W., Kempter, S., Wagner, E., Targeted siRNA delivery using a lipo-oligoaminoamide nanocore with an influenza peptide and transferrin shell. Adv. Healthc. Mater. 5 (2016), 1493–1504, 10.1002/adhm.201600057.
Zhu, H., Zhang, S., Ling, Y., Meng, G., Yang, Y., Zhang, W., PH-responsive hybrid quantum dots for targeting hypoxic tumor siRNA delivery. J. Control. Release 220 (2015), 529–544, 10.1016/j.jconrel.2015.11.017.

Similar publications