Vehicles for Small Interfering RNA transfection:
Exosomes versus Synthetic Nanocarriers

• Authors: Markus Duechler
• Languages of publication: EN

Abstracts

EN

Therapies based on RNA interference (RNAi) hold a great potential for
targeted interference of the expression of specific genes. Small-interfering
RNAs (siRNA) and micro-RNAs interrupt protein synthesis by inducing the
degradation of messenger RNAs or by blocking their translation. RNAibased
therapies can modulate the expression of otherwise undruggable
target proteins. Full exploitation of RNAi for medical purposes depends
on efficient and safe methods for delivery of small RNAs to the target
cells. Tremendous effort has gone into the development of synthetic
carriers to meet all requirements for efficient delivery of nucleic acids into
particular tissues. Recently, exosomes unveiled their function as a natural
communication system which can be utilized for the transport of small
RNAs into target cells. In this review, the capabilities of exosomes as
delivery vehicles for small RNAs are compared to synthetic carrier systems.
The step by step requirements for efficient transfection are considered:
production of the vehicle, RNA loading, protection against degradation,
lack of immunogenicity, targeting possibilities, cellular uptake, cytotoxicity,
RNA release into the cytoplasm and gene silencing efficiency. An exosomebased
siRNA delivery system shows many advantages over conventional
transfection agents, however, some crucial issues need further optimization
before broad clinical application can be realized.

Keywords

EN

siRNA; exosomes; liposomes; polycations; transfection

• Publisher: De Gruyter Open
• Journal: DNA and RNA Nanotechnology
• Year: 2013
• Volume: 1
• Issue: 1

Dates

received

1 - 3 - 2013

accepted

19 - 4 - 2013

online

31 - 5 - 2013

Contributors

author

Markus Duechler

• Department of Bioorganic Chemistry,
  Centre of Molecular and Macromolecular
  Studies, Polish Academy of Sciences, 112
  Sienkiewicza Street, 90-363 Lodz, Poland

References

• Ramachandran P.V., Ignacimuthu S. RNA Interference-A Silent but an Efficient Therapeutic Tool, Appl Biochem Biotechnol., 2013; 169, 1774-1789.
• Nykanen A., Haley B., Zamore, P. D. ATP requirements and small interfering RNA structure in the RNA interference pathway, Cell, 2001; 107, 309–321.[Crossref][PubMed]
• Kota J., Chivukula R.R., O’Donnell K.A., Wentzel E.A., Montgomery C.L., Hwang H.W., Chang T.C., Vivekanandan P., Torbenson M., Clark K.R., Mendell J.R., Mendell J.T. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model, Cell, 2009; 137, 1005-1017.
• Tavazoie S.F., Alarcón C., Oskarsson T., Padua D., Wang Q., Bos P.D., Gerald W.L., Massagué J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature, 2008; 451, 147-152.
• Ryther, R.C., Flynt, A.S., Phillips, J.A. 3rd, and Patton, J.G. siRNA therapeutics: big potential from small RNAs, Gene Ther. 2005; 12, 5–11.[Crossref]
• Chen X., Liang H., Zhang J., Zen K., Zhang C.Y. Horizontal transfer of microRNAs: molecular mechanisms and clinical applications, Protein Cell, 2012; 3, 28-37.[PubMed]
• Burnett J.C., Rossi J.J., Tiemann K. Current progress of siRNA/shRNA therapeutics in clinical trials, Biotechnol. J., 2011; 6, 1130-1146.
• van den Boorn J.G., Schlee M., Coch C., Hartmann G. SiRNA delivery with exosome nanoparticles, Nat. Biotechnol., 2011; 29, 325-326.[Crossref]
• El Andaloussi S., Lakhal S., Mäger I., Wood M.J. Exosomes for targeted siRNA delivery across biological barriers, Adv. Drug Deliv. Rev., 2013; 65, 391-397.[Crossref][PubMed]
• Hood J.L., Pan H., Lanza G.M., Wickline S.A., Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN). Paracrine induction of endothelium by tumor exosomes. Lab. Invest., 2009; 89, 1317–1328.[Crossref][PubMed]
• Record M., Subra C., Silvente-Poirot S., Poirot M. Exosomes as intercellular signalosomes and pharmacological effectors, Biochem, Pharmacol., 2011; 81, 1171-1182.[PubMed][Crossref]
• Xiao D., Ohlendorf J., Chen Y., Taylor D.D., Rai S.N., Waigel S., Zacharias W., Hao H., McMasters K.M. Identifying mRNA, microRNA and protein profiles of melanoma exosomes, PLoS One, 2012; 7, e46874.
• Ohshima K., Inoue K., Fujiwara A., Hatakeyama K., Kanto K., Watanabe Y., Muramatsu K., Fukuda Y., Ogura S., Yamaguchi K., Mochizuki T. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line, PLoS One, 2010; 5, e13247.
• Kogure T., Lin W.L., Yan I.K., Braconi C. Patel T. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth, Hepatology, 2011; 54, 1237-1248.[Crossref][PubMed]
• Bianchi F., Nicassio F., Marzi M., Belloni E., Dall’Olio V., Bernard L., Pelosi G., Maisonneuve P., Veronesi G., Di Fiore P.P. A serum circulating miRNA diagnostic test to identify asymptomatic high-risk individuals with early stage lung cancer. EMBO Mol. Med., 2011; 3, 495–503.[Crossref][PubMed]
• Keller S., Ridinger J., Rupp A.K., Janssen J.W., Altevogt P. Body fluid derived exosomes as a novel template for clinical diagnostics. J. Transl. Med., 2011; 9, 86. [Crossref]
• Mitchell P.S., Parkin R.K., Kroh E.M., Fritz B.R., Wyman S.K., Pogosova-Agadjanyan E.L., Peterson A., Noteboom J., O’Briant K.C., Allen A., Lin D.W., Urban N., Drescher C.W., Knudsen B.S., Stirewalt D.L., Gentleman R., Vessella R.L., Nelson P.S., Martin D.B., Tewari M. Circulating microRNAs as stable blood-based markers for cancer detection, Proc. Natl. Acad. Sci. U S A., 2008; 105, 10513-10518.[Crossref]
• Pegtel D.M., Cosmopoulos K., Thorley-Lawson D.A., van Eijndhoven M.A., Hopmans E.S., Lindenberg J.L., de Gruijl T.D., Würdinger T., Middeldorp J.M. Functional delivery of viral miRNAs via exosomes, Proc. Natl. Acad. Sci. U S A., 2010; 107, 6328-6333.[Crossref]
• Liu C., Yu S., Zinn K., Wang J., Zhang L., Jia Y., Kappes J.C., Barnes S., Kimberly R.P., Grizzle W.E., Zhang H.G. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function, J. Immunol., 2006; 176, 1375-1385.
• Kosaka N., Ochiya T. Unraveling the Mystery of Cancer by Secretory microRNA: Horizontal microRNA Transfer between Living Cells, Front. Genet., 2011; 2, 97.[PubMed]
• Singha K., Namgung R., Kim W.J. Polymers in small-interfering RNA delivery, Nucleic Acid Ther., 2011; 21, 133-147.[PubMed]
• Lai R.C., Yeo R.W., Tan K.H., Lim S.K. Exosomes for drug delivery - a novel application for the mesenchymal stem cell, Biotechnol. Adv., 2012, [Epub ahead of print].
• Lamparski H.G., Metha-Damani A., Yao J-Y., Patel S., Hsu D-H., Ruegg C., et al. Production and characterization of clinical grade exosomes derived from dendritic cells. J. Immunol. Methods, 2002; 270, 211–226.
• Mathivanan S., Lim J.W.E., Tauro B.J., Ji H., Moritz R.L., Simpson R.J. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature, Mol. Cell. Proteomics, 2010; 9, 197–208.[PubMed][Crossref]
• Taylor D.D., Zacharias W., Gercel-Taylor C. Exosome isolation for proteomic analyses and RNA profiling, Methods Mol. Biol., 2011; 728, 235-246.
• Alvarez-Erviti L., Seow Y., Yin H., Betts C., Lakhal S., Wood M.J. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes, Nat. Biotechnol., 2011; 29, 341–345.[Crossref]
• Wahlgren J., De Karlson T., Brisslert M., Vaziri Sani F., Telemo E., Sunnerhagen P., Valadi H. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes, Nucleic Acids Res., 2012; 40, e130.[Crossref]
• Simoes S., Filipe A., Faneca H., Mano M., Penacho N., Duzgunes N., de Lima M. P. Cationic liposomes for gene delivery. Expert Opin. Drug Delivery, 2005; 2, 237–254.
• Taratula O., Savla R., He H., Minko T. Poly(propyleneimine) dendrimers as potential siRNA delivery nanocarrier: from structure to function, Int. J. Nanotechnol., 2011; 8, 36–52.[Crossref]
• Pisitkun T., Shen R.F., Knepper M.A. Identification and proteomic profiling of exosomes in human urine, Proc. Natl. Acad. Sci. U S A., 2004; 101, 13368–13373.[Crossref]
• Gu Y., Li M., Wang T., Liang Y., Zhong Z., Wang X., Zhou Q., Chen L., Lang Q., He Z., Chen X., Gong J., Gao X., Li X., Lv X. Lactation-related microRNA expression profiles of porcine breast milk exosomes, PLoS One., 2012; 7, e43691.
• Admyre C., Grunewald J., Thyberg J., Gripenbäck S., Tornling G., Eklund A., et al. Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid, Eur. Respir. J., 2003; 22, 578–583.[PubMed][Crossref]
• Takahashi Y., Nishikawa M., Shinotsuka H., Matsui Y., Ohara S., Imai T., Takakura Y. Visualization and in vivo tracking of the exosomes of murine melanoma B16-BL6 cells in mice after intravenous injection, J. Biotechnol., 2013; 165, 77-84.
• Gomes-da-Silva L.C., Fonseca N.A., Moura V., Pedroso de Lima M.C., Simões S., Moreira J.N. Lipid-based nanoparticles for siRNA delivery in cancer therapy: paradigms and challenges, Acc. Chem. Res., 2012; 45, 1163-1171.[Crossref]
• Ishida T., Kiwada H. Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes, Int. J. Pharm., 2008; 354, 56-62.
• Iero M., Valenti R., Huber V., Filipazzi P., Parmiani G., Fais S., Rivoltini L. Tumour-released exosomes and their implications in cancer immunity, Cell Death. Differ., 2008; 15: 80–88.[PubMed][Crossref]
• Wolfers J., Lozier A., Raposo G., Regnault A., Théry C., Masurier C., Flament C., Pouzieux S., Faure F., Tursz T., Angevin E., Amigorena S., Zitvogel L. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming, Nat. Med., 2001; 7, 297-303.[PubMed][Crossref]
• Subra C., Laulagnier K., Perret B., Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies, Biochimie, 2007; 89, 205–212.[Crossref][PubMed]
• Andre F., Chaput N., Schartz NE., Flament C., Aubert N., Bernard J., et al. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells, J. Immunol., 2004; 172, 2126–2136.
• Hood J.L., San R.S., Wickline S.A. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis, Cancer Res., 2011; 71, 3792–3801.[PubMed][Crossref]
• Ruiss R., Jochum S., Mocikat R., Hammerschmidt W., Zeidler R. EBV-gp350 confers B-cell tropism to tailored exosomes and is a neo-antigen in normal and malignant B cells-a new option for the treatment of B-CLL, PLoS One, 2011; 6, e25294.
• Biswal B.K., Debata N.B., Verma R.S. Development of a targeted siRNA delivery system using FOL-PEG-PEI conjugate, Mol. Biol. Rep., 2010; 37, 2919-2926.[PubMed][Crossref]
• Kang J.H., Tachibana Y., Kamata W., Mahara A., Harada-Shiba M., Yamaoka T. Liver-targeted siRNA delivery by polyethylenimine (PEI)-pullulan carrier, Bioorg. Med. Chem., 2010; 18, 3946-3950.[Crossref][PubMed]
• Han H.D., Mangala L.S., Lee J.W., Shahzad M.M., Kim H.S., Shen D., Nam E.J., Mora E.M., Stone R.L., Lu C., Lee S.J., Roh J.W., Nick A.M., Lopez-Berestein G., Sood A.K. Targeted gene silencing using RGD-labeled chitosan nanoparticles, Clin. Cancer Res., 2010; 16, 3910-3922.[PubMed][Crossref]
• Patil M.L., Zhang M., Taratula O., Garbuzenko O.B., He H., Minko T. Internally cationic polyamidoamine PAMAM-OH dendrimers for siRNA delivery: effect of the degree of quaternization and cancer targeting, Biomacromolecules, 2009; 10, 258-266.[PubMed][Crossref]
• Luo Y., Zhai X., Ma C., Sun P., Fu Z., Liu W., Xu J. An inhalable β2-adrenoceptor ligand-directed guanidinylated chitosan carrier for targeted delivery of siRNA to lung, J. Control. Release., 2012; 162, 28-36.
• Noh S.M., Han S.E., Shim G., Lee K.E., Kim C.W., Han S.S., Choi Y., Kim Y.K., Kim W.K., Oh Y.K. Tocopheryl oligochitosan-based self assembling oligomersomes for siRNA delivery, Biomaterials, 2011; 32, 849-857.[Crossref][PubMed]
• Kim H.J., Ishii A., Miyata K., Lee Y., Wu S., Oba M., Nishiyama N., Kataoka K. Introduction of stearoyl moieties into a biocompatible cationic polyaspartamide derivative, PAsp(DET), with endosomal escaping function for enhanced siRNA-mediated gene knockdown, J. Control. Release, 2010; 145, 141-148.[Crossref]
• Dey D., Inayathullah M., Lee A.S., LeMieux M.C., Zhang X., Wu Y., et al. Efficient gene delivery of primary human cells using peptide linked polyethylenimine polymer hybrid, Biomaterials, 2011; 32, 4647–4658.[Crossref][PubMed]
• Parolini I., Federici C., Raggi C., Lugini L., Palleschi S., De Milito A., Coscia C., Iessi E., Logozzi M., Molinari A., Colone M., Tatti M., Sargiacomo M., Fais S. Microenvironmental pH is a key factor for exosome traffic in tumor cells, J. Biol. Chem., 2009; 284, 34211–34222.
• Akinc A., Thomas M., Klibanov A.M., Langer R. Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis, J. Gene Med., 2005; 7, 657-663.[Crossref]
• Kulkarni R.P., Mishra S., Fraser S.E., Davis M.E. Single cell kinetics of intracellular, nonviral, nucleic acid delivery vehicle acidification and trafficking, Bioconjug. Chem., 2005; 16, 986-994.[PubMed][Crossref]
• Midoux P., LeCam E., Coulaud D., Delain E., Pichon C. Histidine containing peptides and polypeptides as nucleic acid vectors, Somat. Cell. Mol. Genet., 2002; 27, 27-47.[Crossref][PubMed]
• Tamura A., Oishi M., Nagasaki Y. Enhanced cytoplasmic delivery of siRNA using a stabilized polyion complex based on PEGylated nanogels with a cross-linked polyamine structure, Biomacromolecules, 2009; 10, 1818-1827.[Crossref][PubMed]
• Nguyen J., Szoka FC. Nucleic acid delivery: the missing pieces of the puzzle? Acc. Chem. Res., 2012; 45, 1153-1162.[Crossref]
• Ohno S., Takanashi M., Sudo K., Ueda S., Ishikawa A., Matsuyama N., Fujita K., Mizutani T., Ohgi T., Ochiya T., Gotoh N., Kuroda M. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells, Mol. Ther., 2013; 21, 185-191.[PubMed][Crossref]
• Dai S., Wei D., Wu Z., Zhou X., Wei X., Huang H., et al. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer, Mol. Ther., 2008; 16, 782–790.[PubMed][Crossref]
• Escudier B., Dorval T., Chaput N., Andre F., Caby M.P., Novault S., et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derivedexosomes: results of the first phase I clinical trial, J. Transl. Med., 2005; 3, 10.[Crossref]
• Morse M.A., Garst J., Osada T., Khan S., Hobeika A., Clay T.M., et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer, J. Transl. Med., 2005; 3, 9.[PubMed][Crossref]
• Xia W., Li Y., Lou B., Wang P., Gao X., Lin C. Bioreducible PEI-siRNA Nanocomplex for Liver Cancer Therapy: Transfection, Biodistribution, and Tumor Growth Inhibition In Vivo, J. Nanomaterials, 2013; 2013, 11 pages.
• Kawakami S., Ito Y., Charoensit P., Yamashita F., Hashida M. Evaluation of proinflammatory cytokine production induced by linear and branched polyethylenimine/plasmid DNA complexes in mice, J. Pharmacol. Exp. Ther., 2006; 317, 1382-1390.
• Hoon Jeong J., Christensen L.V., Yockman J.W., Zhong Z., Engbersen J.F., Jong Kim W., Feijen J., Wan Kim S. Reducible poly(amido ethylenimine) directed to enhance RNA interference, Biomaterials, 2007; 28, 1912-1917.[PubMed][Crossref]
• Foged C. siRNA delivery with lipid-based systems: promises and pitfalls, Curr. Top. Med. Chem., 2012; 12, 97-107.[PubMed][Crossref]
• Ho E.A., Osooly M., Strutt D., Masin D., Yang Y., Yan H., Bally M. Characterization of long-circulating cationic nanoparticle formulations consisting of a two-stage PEGylation step for the delivery of siRNA in a breast cancer tumor model, J. Pharm. Sci., 2013; 102, 227-236.[Crossref]
• Heyes J., Palmer L., Bremner K., MacLachlan I. Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids, J. Control. Release, 2005; 107, 276–287.[Crossref]
• Kim S.I., Shin D., Lee H., Ahn B.Y., Yoon Y., Kim M. Targeted delivery of siRNA against hepatitis C virus by apolipoprotein A-I-bound cationic liposomes, J. Hepatol., 2009; 50, 479-488. [Crossref]
• Pirollo K.F., Rait A., Zhou Q., Hwang S.H., Dagata J.A., Zon G., Hogrefe R.I., Palchik G., Chang E.H. Materializing the potential of small interfering RNA via a tumor-targeting nanodelivery system, Cancer Res., 2007; 67, 2938-2943.[Crossref]
• Zabel M.D. Lipopeptide delivery of siRNA to the central nervous system. Methods Mol. Biol., 2013; 948, 251-262.
• Zhou C., Mao Y., Sugimoto Y., Zhang Y., Kanthamneni N., Yu B., Brueggemeier R.W., Lee L.J., Lee R.J. SPANosomes as delivery vehicles for small interfering RNA (siRNA), Mol. Pharm., 2012; 9, 201-210.[PubMed][Crossref]
• Zhou C., Zhang Y., Yu B., Phelps M.A., Lee L.J., Lee R.J. Comparative cellular pharmacokinetics and pharmacodynamics of siRNA delivery by SPANosomes and by cationic liposomes, Nanomedicine, 2013; 9, 504-513.[Crossref][PubMed]
• Kim W.J., Chang C.W., Lee M., Kim S.W. Efficient siRNA delivery using water soluble lipopolymer for anti-angiogenic gene therapy, J. Control. Release, 2007; 118, 357-363.[Crossref]
• Kim S.K., Park K.M., Singha K., Kim J., Ahn Y., Kim K., Kim W.J. Galactosylated cucurbituril-inclusion polyplex for hepatocyte-targeted gene delivery, Chem. Commun. (Camb.), 2010; 46, 692-694.[Crossref]
• Tsai L.R, Chen M.H, Chien C.T, Chen M.K, Lin F.S, Lin K.M, Hwu Y.K, Yang C.S, Lin S.Y. A single-monomer derived linear-like PEI-co-PEG for siRNA delivery and silencing, Biomaterials, 2011; 32, 3647-3653.[Crossref][PubMed]
• Son S., Kim W.J. Biodegradable nanoparticles modified by branched polyethylenimine for plasmid DNA delivery, Biomaterials, 2010; 31, 133-143.[PubMed][Crossref]
• Wu Z.W., Chien C.T., Liu C.Y., Yan J.Y., Lin S.Y. Recent progress in copolymer-mediated siRNA delivery, J. Drug Target., 2012; 20, 551-560. [Crossref]
• Yang X.Z., Dou S., Sun T.M., Mao C.Q., Wang H.X., Wang J. Systemic delivery of siRNA with cationic lipid assisted PEG-PLA nanoparticles for cancer therapy, J. Control. Release, 2011; 156, 203-211.
• Kong F., Liu G., Sun B., Zhou S., Zuo A., Zhao R., Liang D. Phosphorylatable short peptide conjugated low molecular weight chitosan for efficient siRNA delivery and target gene silencing, Int. J. Pharm., 2012; 422, 445-453.
• Yuan Y., Tan J., Wang Y., Qian C., Zhang M. Chitosan nanoparticles as non-viral gene delivery vehicles based on atomic force microscopy study. Acta Biochim. Biophys. Sin. (Shanghai), 2009; 41, 515-526.[Crossref]
• Opanasopit P., Techaarpornkul S., Rojanarata T., Ngawhirunpat T., Ruktanonchai U. Nucleic acid delivery with chitosan hydroxybenzotriazole, Oligonucleotides, 2010; 20, 127-136.[PubMed][Crossref]
• Rojanarata T., Opanasopit P., Techaarpornkul S., Ngawhirunpat T., Ruktanonchai U. Chitosan-thiamine pyrophosphate as a novel carrier for siRNA delivery, Pharm. Res., 2008; 25, 2807-2814. [PubMed][Crossref]
• Duan Y., Guan X., Ge J., Quan D., Zhuo Y., Ye H., Shao T. Cationic nano-copolymers mediated IKKbeta targeting siRNA inhibit the proliferation of human Tenon’s capsule fibroblasts in vitro, Mol. Vis., 2008; 14, 2616-2628.
• Bartlett D.W., Davis M.E. Physicochemical and biological characterization of targeted, nucleic acid-containing nanoparticles, Bioconjug. Chem., 2007; 18, 456-468.[PubMed][Crossref]
• Byrne C., Sallas F., Rai D.K., Ogier J., Darcy R. Poly-6-cationic amphiphilic cyclodextrins designed for gene delivery, Org. Biomol. Chem., 2009; 7, 3763-3771.[Crossref]
• Miyata K., Oba M., Nakanishi M., Fukushima S., Yamasaki Y., Koyama H., Nishiyama N., Kataoka K. Polyplexes from poly(aspartamide) bearing 1,2-diaminoethane side chains induce pH-selective, endosomal membrane destabilization with amplified transfection and negligible cytotoxicity, J. Am. Chem. Soc., 2008; 130, 16287-16294.
• Rennert R., Neundorf I., Beck-Sickinger A.G. Synthesis and application of peptides as drug carriers, Methods Mol. Biol., 2009; 535, 389-403.
• Kim W.J., Christensen L.V., Jo S., Yockman J.W., Jeong J.H., Kim Y.H., Kim S.W. Cholesteryl oligoarginine delivering vascular endothelial growth factor siRNA effectively inhibits tumor growth in colon adenocarcinoma, Mol. Ther., 2006; 14, 343-350.[PubMed][Crossref]
• Leng Q., Scaria P., Zhu J., Ambulos N., Campbell P., Mixson A.J. Highly branched HK peptides are effective carriers of siRNA, J. Gene Med., 2005; 7, 977-986.[Crossref]
• Pavan G.M., Monteagudo S., Guerra J., Carrion B., Ocana V., Rodriguez-Lopez J., Danani A., Perez-Martinez F.C., Cena V. Role of Generation, Architecture, pH and Ionic Strength on Successful siRNA Delivery and Transfection by Hybrid PPV-PAMAM Dendrimers, Curr. Med. Chem., 2012; 19, 4929-4941.[Crossref]
• Zhou J., Wu J., Hafdi N., Behr J.P., Erbacher P., Peng L. PAMAM dendrimers for efficient siRNA delivery and potent gene silencing, Chem. Commun. (Camb.), 2006; 22, 2362-2364.[Crossref]
• Smith M.H., Lyon L.A. Multifunctional nanogels for siRNA delivery, Acc. Chem. Res., 2012; 45, 985-993.[PubMed][Crossref]
• Vinogradov S.V., Batrakova E.V., Kabanov A.V. Nanogels for oligonucleotide delivery to the brain, Bioconjug. Chem., 2004; 15, 50-60.[Crossref][PubMed]
• Tamura A., Oishi M., Nagasaki Y. Enhanced cytoplasmic delivery of siRNA using a stabilized polyion complex based on PEGylated nanogels with a cross-linked polyamine structure, Biomacromolecules, 2009; 10, 1818-1827.[Crossref][PubMed]
• Lee J.S., Green J.J., Love K.T., Sunshine J., Langer R., Anderson D.G. Gold, poly(beta-amino ester) nanoparticles for small interfering RNA delivery, Nano Lett., 2009; 9, 2402-2406.[PubMed][Crossref]
• Ghosh P., Han G., De M., Kim C.K., Rotello V.M. Gold nanoparticles in delivery applications, Adv. Drug Deliv. Rev., 2008; 60, 1307-1315.[PubMed][Crossref]
• Tzeng S.Y., Hung B.P., Grayson W.L., Green J.J. Cystamine-terminated poly(beta-amino ester)s for siRNA delivery to human mesenchymal stem cells and enhancement of osteogenic differentiation, Biomaterials, 2012; 33, 8142-51.[Crossref][PubMed]
• Muroski M.E., Kogot JM., Strouse G.F. Bimodal gold nanoparticle therapeutics for manipulating exogenous and endogenous protein levels in mammalian cells, J. Am. Chem. Soc., 2012; 134, 19722-19730. [Crossref]
• Song W.J., Du J.Z., Sun T.M., Zhang P.Z., Wang J. Gold nanoparticles capped with polyethyleneimine for enhanced siRNA delivery, Small, 2010; 6, 239-246.[PubMed][Crossref]
• Han L., Zhao J., Zhang X., Cao W., Hu X., Zou G., Duan X., Liang X.J. Enhanced siRNA delivery and silencing gold-chitosan nanosystem with surface charge-reversal polymer assembly and good biocompatibility, ACS Nano, 2012; 6: 7340-7351.[PubMed][Crossref]
• Lacerda L., Bianco A., Prato M., Kostarelos K. Carbon nanotubes as nanomedicines: from toxicology to pharmacology, Advm Drug Delivm Rev., 2006; 58, 1460-1470.
• Cheung W., Pontoriero F., Taratula O., Chen A.M., He H. DNA and carbon nanotubes as medicine, Adv. Drug Deliv. Rev., 2010; 62, 633-649.[Crossref][PubMed]
• Kam N.W., Liu Z., Dai H. Functionalization of carbon nanotubes via cleavable disulfide bonds for efficient intracellular delivery of siRNA and potent gene silencing, J. Am. Chem. Soc., 2005; 127, 12492-12493.[Crossref]
• Li J.M., Zhao M.X., Su H., Wang Y.Y., Tan C.P., Ji L.N., Mao Z.W. Multifunctional quantum-dot-based siRNA delivery for HPV18 E6 gene silence and intracellular imaging, Biomaterials, 2011; 32, 7978-7987.[Crossref]

Identifiers

DOI

10.2478/rnan-2013-0002