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Nanomedicine Volume 5, 2010 - Issue 7
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Review

Smart siRNA Delivery Systems Based on Polymeric Nanoassemblies and Nanoparticles

Atsushi Tamura1 Graduate School of Pure & Applied Sciences, University of Tsukuba. 1–1-1 Ten-noudai, Tsukuba, Ibaraki 305–8573, JapanView further author information
&
Yukio Nagasaki1 Graduate School of Pure & Applied Sciences, University of Tsukuba. 1–1-1 Ten-noudai, Tsukuba, Ibaraki 305–8573, Japan;2 Tsukuba Research Center for Interdisciplinary Materials Science (TIMS), University of Tsukuba;3 Center for Tsukuba Advanced Research Alliance (TARA), University of Tsukuba;4 Master‘s School of Medical Sciences, Graduate School of Comprehensive Human Science, University of Tsukuba;5 International Center for Materials Nanoarchitectonics Satellite (MANA), National Institute for Materials Science (NIMS) & University of Tsukuba.Correspondence[email protected]
View further author information
Pages 1089-1102 | Published online: 27 Sep 2010

Bibliography

  • Paterson BM , RobertsBE, KuffEL: Structural gene identification and mapping by DNA-mRNA hybrid-arrested cell-free translation.Proc. Natl Acad. Sci. USA74(10), 4370–4374 (1977).
  • Zamecnik PC , StephensonML: Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide.Proc. Natl Acad. Sci. USA75(1), 280–284 (1978).
  • Stephenson ML , ZamecnikPC: Inhibition of Rous sarcoma viral RNA translation by a specific oligodeoxyribonucleotide.Proc. Natl Acad. Sci. USA75(1), 285–288 (1978).
  • Breaker RR : Natural and engineered nucleic acids as tools to explore biology.Nature432(7019), 838–845 (2004).
  • Gewirtz AM , SokolDL, RatajczakMZ: Nucleic acid therapeutics: state of the art and future prospects.Blood92(3), 712–736 (1988).
  • Stull RA , SzokaFC Jr: Antigene, ribozyme and aptamer nucleic acid drugs: progress and prospects. Pharm. Res.12(4), 465–483 (1995).
  • Opalinska JB , GewirtzAM: Nucleic-acid therapeutics: basic principles and recent applications.Nat. Rev. Drug Discov.1(7), 503–514 (2002).
  • Gleave ME , MoniaBP: Antisense therapy for cancer.Nat. Rev. Drug Discov.5(6), 468–479 (2005).
  • Grillone LR , LanzR: Formivirsen.Drugs Today37(4), 245–255 (2001).
  • Ng EWM , ShimaDT, CaliasP, CunninghamET Jr, Guyer DR, Adamis AP: Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat. Rev. Drug Discov.5(2), 123–132 (2006).
  • Dorsett Y , TuschlT: siRNAs: Applications in functional genomics and potential as therapeutics.Nat. Rev. Drug Discov.3(4), 318–329 (2004).
  • Iorns E , LordCJ, TurnerN, AshworthA: Utilizing RNA interference to enhance cancer drug discovery.Nat. Rev. Drug Discov.6(7), 556–568 (2007).
  • Bumcrot D , ManoharanM, KotelianskyV, SahDWY: RNAi therapeutics: a potential new class of pharmaceutical drugs.Nat. Chem. Biol.2(12), 711–719 (2006).
  • Behlke MA : Progress towards in vivo use of siRNAs.Mol. Ther.13(4), 644–670 (2006).
  • Kim DH , RossiJJ: Strategies for silencing human disease using RNA interference.Nat. Rev. Genetics8(3), 173–184 (2007).
  • Fire A , XuS, MontgomeryMK, KostasSA, DriverSE, MelloCC: Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.Nature391(6669), 806–811 (1998).
  • Zamore PD , TuschlT, SharpPA, BartelDP: RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals.Cell101(1), 25–33 (2000).
  • Elbashir SM , LendeckelW, TuschlT: RNA interference is mediated by 21- and 22-nucleotide RNAs.Genes Dev.15(2), 188–200 (2001).
  • Stark GR , KerrIM, WilliamsBRG, SilvermanRH, SchreiberRD: How cells respond to interferons.Annu. Rev. Biochem.67, 227–264 (1998).
  • Elbashir SM , HarborthJ, LendeckelW, YalcinA, WeberK, TuschlT: Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.Nature411(6836), 494–498 (2001).
  • Martinez J , PatkaniowskaA, UrlaubH, LührmannR, TuschlT: Single-stranded antisense siRNAs guide target RNA cleavage in RNAi.Cell110(5), 563–574 (2002).
  • Whitehead KA , LangerR, AndersonDG: Knocking down barriers: advances in siRNA delivery.Nat. Rev. Drug Discov.8(2), 129–138 (2009).
  • Manoharan M : RNA interference and chemically modified small interfering RNAs.Curr. Opin. Chem. Biol.8(6), 570–579 (2004).
  • Zhang HY , DuQ, WahlestedtC, LiangZ: RNA interference with chemically modified siRNA.Curr. Top. Med. Chem.6(9), 893–900 (2006).
  • Jeong JH , MokH, OhYK, ParkTG: siRNA conjugate delivery systems.Bioconjugate Chem.20, 5–14 (2009).
  • Gao S , Dagnaes-HansenF, NielsenEJBet al.: The effect of chemical modification and nanoparticle formulation on stability and biodistribution of siRNA in mice.Mol. Ther.17(7), 1225–1233 (2009).
  • Braasch DA , ParooZ, ConstantinescuAet al.: Biodistribution of phosphodiester and phosphorothioate siRNA.Bioorg. Med. Chem. Lett.14(5), 1139–1143 (2004).
  • Kim WJ , KimSW: Efficient siRNA delivery with nonviral polymeric vehicles.Pharm. Res.26(3), 657–666 (2008).
  • Zhang S , ZhaoB, JiangH, WangB, MaB: Cationic lipids and polymers mediated vectors for delivery of siRNA.J. Controlled Release123(1), 1–10 (2007).
  • Pack DW , HoffmanAS, PunS, StaytonPS: Design and development of polymers for gene delivery.Nat. Rev. Drug Discov.4(7), 581–593 (2005).
  • Bloomfield VA : DNA condensation by multivalent cations.Biopolymers44(3), 269–282 (1997).
  • Boussif O , Lezoualc‘hF, ZantaMAet al.: A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine.Proc. Natl Acad. Sci. USA92(16), 7297–7301 (1995).
  • Behr JP : The proton sponge: A trick to enter cells the viruses did not exploit.Chimia51(1–2), 34–36 (1997).
  • Sonawane ND , Szoka Jr. FC, Verkman AS: Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine–DNA polyplexes. J. Biol. Chem.278(45), 44826–44831 (2003).
  • Urban-Klein B , WerthS, AbuharbeidS, CzubaykoF, AignerA: RNAi-mediated gene-targeting through systemic application of polyethylenimine (PEI)-complexed siRNA in vivo.Gene Ther.12(5), 461–466 (2005).
  • Esfand R , TomaliaDA: Poly(amidoamine) (PAMAM) dendrimers: from biomimicry to drug delivery and biomedical applications.Drug Discov. Today6(8), 427–436 (2001).
  • Dufès C , UchegbuIF, SchätzleinAG: Dendrimers in gene delivery.Adv. Drug Deliv. Rev.57(15), 2177–2202 (2005).
  • Zhou J , WuJ, HafdiN, BehrJP, ErbacherP, PengL: PAMAM dendrimers for efficient siRNA delivery and potent gene silencing.Chem. Commun.2362–2364 (2006).
  • Watanabe K , Harada-ShibaM, SuzukiAet al.: in vivo siRNA delivery with dendritic poly(L-lysine) for the treatment of hypercholesterolemia.Mol. BioSyst.5(11), 1306–1310 (2009).
  • Taratula O , GarbuzenkoOB, KirkpatrickPet al.: Surface-engineered targeted PPI dendrimer for efficient intracellular and intratumoral siRNA delivery.J. Controlled Release140(3), 284–293 (2009).
  • Mao S , SunW, KisselT: Chitosan-based formulations for delivery of DNA and siRNA.Adv. Drug Deliv. Rev.62, 12–27 (2010).
  • Liu X , HowardKA, DongMet al.: The influence of polymeric properties on chitosan–siRNA nanoparticle formulation and gene silencing.Biomaterials28, 1280–1288 (2007).
  • Katas H , AlparHO: Development and characterisation of chitosan nanoparticles for siRNA delivery.J. Controlled Release115(2), 216–225 (2006).
  • Howard KA , RahbekUL, LiuXet al.: RNA interference in vitro and in vivo using a chitosan–siRNA nanoparticle system.Mol. Ther.14, 476–484 (2006).
  • Moghimi SM , SzebeniJ: Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization and protein-binding properties.Prog. Lipid Res.42(6), 463–478 (2003).
  • Harris JM , ChessRB: Effect of PEGylation on pharmaceuticals.Nat. Rev. Drug Discov.2(3), 214–221 (2003).
  • van Vlerken LE , VyasTK, AmijiMM: Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery.Pharm. Res.24(8), 1405–1414 (2007).
  • Sato A , ChoiSW, HiraiMet al.: Polymer brush-stabilized polyplex for a siRNA carrier with long circulatory half-life.J. Controlled Release122(3), 209–216 (2007).
  • Scales CW , HuangF, LiNet al.: Corona-stabilized interpolyelectrolyte complexes of siRNA with nonimmunogenic, hydrophilic/cationic block copolymers prepared by aqueous RAFT polymerization.Macromolecules39(20), 6871–6881 (2006).
  • Greenwald RB , ChoeYH, McGuireJ, ConoverCD: Effective drug delivery by PEGylated drug conjugates.Adv. Drug Deliv. Rev.55(2), 217–250 (2003).
  • Veronese FM , PasutG: PEGylation, successful approach to drug delivery.Drug Discov. Today10(21), 1451–1458 (2005).
  • Roberts MJ , BentleyMD, HarrisJM: Chemistry for peptide and protein PEGylation.Adv. Drug Deliv. Rev.54(4), 459–476 (2002).
  • Otsuka H , NagasakiY, KataokaK: PEGylated nanoparticles for biological and pharmaceutical applications.Adv. Drug. Deliv. Rev.55(3), 403–419 (2003).
  • Kataoka K , HaradaA, NagasakiY: Block copolymer micelles for drug delivery: design, characterization and biological significance.Adv. Drug. Deliv. Rev.47(1), 113–131 (2001).
  • Kakizawa Y , KataokaK: Block copolymer micelles for delivery of gene and related compounds.Adv. Drug. Deliv. Rev.54(2), 203–222 (2002).
  • Matsumura Y , MaedaH: A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent Smancs.Cancer Res.46(12), 6387–6392 (1986).
  • Maeda H , WuJ, SawaT, MatsumuraY, HoriK: Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review.J. Control. Release65(1–2), 271–284 (2000).
  • Mao S , NeuM, GermershausOet al.: Influence of polyethylene glycol chain length on the physicochemical and biological properties of poly(ethylene imine)-graft-poly(ethylene glycol) block copolymer/siRNA polyplexes.Bioconjugate Chem.17(5), 1209–1218 (2006).
  • Malek A , MerkelO, FinkL, CzubaykoF, KisselT, AignerA: in vivo pharmacokinetics, tissue distribution and underlying mechanisms of various PEI(-PEG)/siRNA complexes.Toxicol. Appl. Pharm.236(1), 97–108 (2009).
  • Torchilin VP : Multifunctional nanocarriers.Adv. Drug Deliv. Rev.58(14), 1532–1555 (2006).
  • Forssen E , WillisM: Ligand-targeted liposomes.Adv. Drug Deliv. Rev.29(3), 249–271 (1998).
  • Davis ME , ChenZ, ShinDM: Nanoparticle therapeutics: an emerging treatment modality for cancer.Nat. Rev. Drug Discov.7(9), 771–782 (2008).
  • Schiffelers RM , AnsariA, XuJet al.: Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle.Nucleic Acids Res.32(19), E149 (2004).
  • Kim SH , MokH, JeongJH, KimSW, ParkTG: Comparative evaluation of target-specific GFP gene silencing efficiencies for antisense ODN, synthetic siRNA, and siRNA plasmid complexed with PEI-PEG-FOL conjugate.Bioconjugate Chem.17(1), 241–244 (2007).
  • Forrest ML , MeisterGE, KoerberJT, PackDW: Partial acetylation of polyethylenimine enhances in vitro gene delivery.Pharm. Res.21(2), 365–371 (2004).
  • Thomas M , KlibanovAM: Enhancing polyethylenimine‘s delivery of plasmid DNA into mammalian cells.Proc. Natl Acad. Sci. USA99(23), 14640–14645 (2002).
  • Zintchenko A , PhilippA, DehshahriA, WagnerE: Simple modifications of branched PEI lead to highly efficient siRNA carriers with low toxicity.Bioconjugate Chem.19(7), 1448–1455 (2008).
  • Han SO , MahatoRI, KimSW: Water-soluble lipopolymer for gene delivery.Bioconjugate Chem.12(3), 337–345 (2001).
  • Lee M , RentzJ, HanSO, BullDA, KimSW: Water-soluble lipopolymer as an efficient carrier for gene delivery to myocardium.Gene Ther.10(7), 585–593 (2003).
  • Kim WJ , ChangCW, LeeM, KimSW: Efficient siRNA delivery using water soluble lipopolymer for anti-angiogenic gene therapy.J. Controlled Release118(3), 357–363 (2007).
  • Philipp A , ZhaoX, TarchaP, WagnerE, ZintchenkoA: Hydrophobically modified oligoethylenimines as highly efficient transfection agents for siRNA delivery.Bioconjugate Chem.20(11), 2055–2061 (2009).
  • Chen J , TianH, GuoZet al.: A highly efficient siRNA carrier of PBLG modified hyperbranched PEI.Macromol. Biosci.9(12), 1247–1253 (2009).
  • Segura T , HubbellJA: Synthesis and in vitro characterization of an ABC triblock copolymer for siRNA delivery.Bioconjugate Chem.18(3), 736–745 (2007).
  • DeRouchey J , SchmidtC, WalkerGFet al.: Monomolecular assembly of siRNA and poly(ethylene glycol)-peptide copolymers.Biomacromolecules9(2), 724–732 (2008).
  • Xiong XB , UludaqH, LavasanifarA: Biodegradable amphiphilic poly(ethylene oxide)-block-polyesters with grafted polyamines as supramolecular nanocarriers for efficient siRNA delivery.Biomaterials30(2), 242–253 (2009).
  • Toita A , SomaY, MorimotoN, AkiyoshiK. Cycloamylose-based biomaterial: nanogel of cholesterol-bearing cationic cycloamylose for siRNA delivery. Chem. Lett.38(11), 1114–1115 (2009).
  • Kim WJ , ChristensenLV, JoSet al.: Cholesteryl oligoarginine delivering vascular endothelial growth factor siRNA effectively inhibits tumor growth in colon adenocarcinoma.Mol. Ther.14(3), 343–350 (2006).
  • Itaka K , KanayamaN, NishiyamaNet al.: Supramolecular nanocarrier of siRNA from PEG-based block catiomer carrying diamine side chain with distinctive pKa directed to enhance intracellular gene silencing.J. Am. Chem. Soc.126(42), 13612–13613 (2004).
  • Bartlett DW , DavisME: Insights into the kinetics of siRNA-mediated gene silencing from live-cell and live-animal bioluminescent imaging.Nucleic Acids Res.34(1), 322–333 (2006).
  • Davis ME : The first targeted delivery of siRNA in humans via a self-assembling, cyclodextrin polymer-based nanoparticle: From concept to clinic.Mol. Pharm.6(3), 659–668 (2009).
  • Bartlett DW , DavisME: Physicochemical and biological characterization of targeted, nucleic acid-containing nanoparticles.Bioconjugate Chem.18(2), 456–468 (2007).
  • Bartlett DW , DavisME: Impact of tumor-specific targeting and dosing schedule on tumor growth inhibition after intravenous administration of siRNA-containing nanoparticles.Biotechnol. Bioeng.99(4), 975–985 (2008).
  • Breunig M , LungwitzU, LieblR, GoepferichA: Breaking up the correlation between efficacy and toxicity for nonviral gene delivery.Proc. Natl Acad. Sci. USA104(36), 14454–14459 (2007).
  • Breunig M , HozsaC, LungwitzUet al.: Mechanistic investigation of poly(ethylene imine)-based siRNA delivery: disulfide bonds boost intracellular release of the cargo.J. Controlled Release130(1), 57–63 (2008).
  • Meister A , AndersonME: Glutathione.Annu. Rev. Biochem.52, 711–760 (1983).
  • Kim SH , JeongJH, KimT, KimSW, BullDA: VEGF siRNA delivery system using arginine-grafted bioreducible poly(disulfide amine).Mol. Pharm.6(3), 718–726 (2009).
  • Tarcha PJ , PelisekJ, MerdanTet al.: Synthesis and characterization of chemically condensed oligoethylenimine containing β-aminopropionamide linkages for siRNA delivery.Biomaterials28(25), 3731–3740 (2007).
  • Tietze N , PelisekJ, PhilippAet al.: Induction of apoptosis in murine neuroblastoma by systemic delivery of transferrin-shielded siRNA polyplexes for downregulation of Ran.Oligonucleotides18(2), 161–174 (2008).
  • Jere D , XuCX, AroteR, YunCH, ChoMH, ChoCS: Poly(amino ester) as a carrier for si/shRNA delivery in lung cancer cells.Biomaterials29(16), 2535–2547 (2008).
  • Shim MS , KwonYJ: Acid-responsive linear polyethylenimine for efficient, specific, and biocompatible siRNA delivery.Bioconjugate Chem.20(3), 488–499 (2009).
  • Matsumoto S , ChristieRJ, NishiyamaNet al.: Environment-responsive block copolymer micelles with a disulfide cross-linked core for enhanced siRNA delivery.Biomacromolecules10(1), 119–127 (2009).
  • Oishi M , NagasakiY, ItakaK, NishiyamaN, KataokaK: Lactosylated poly(ethylene glycol)-siRNA conjugate through acid-labile β-thiopropionate linkage to construct pH-sensitive poly-ion complex micelles achieving enhanced gene silencing in hepatoma cells.J. Am. Chem. Soc.127(6), 1624–1625 (2005).
  • Oishi M , NagasakiY, NishiyamaNet al.: Enhanced growth inhibition of hepatic multicellular tumor spheroids by lactosylated poly(ethylene glycol)-siRNA conjugate formulated in PEGylated polyplexes.ChemBioChem2(9), 1290–1297 (2007).
  • Oishi M , SasakiS, NagasakiY, KataokaK: pH-responsive oligodeoxynucleotide (ODN)-poly(ethylene glycol) conjugate through acid-labile thiopropionate linkage: Preparation and poly-ion complex micelle formation.Biomacromolecules4(5), 1426–1432 (2003).
  • Wu CH , WuGY: Receptor-mediated delivery of foreign genes to hepatocytes.Adv. Drug Deliv. Rev.29(3), 243–248 (1998).
  • Oishi M , NagatsugiF, SasakiS, NagasakiY, KataokaK: Smart poly-ion complex micelles for targeted intracellular delivery of PEGylated antisense oligonucleotides containing acid-labile linkages.ChemBioChem6(4), 718–725 (2005).
  • Kim SH , JeongJH, LeeSH, KimSW, ParkTG: PEG conjugated VEGF siRNA for anti-angiogenic gene therapy.J. Controlled Release116(2), 123–129 (2006).
  • Lee SH , KimSH, ParkTG: Intracellular siRNA delivery system using polyelectrolyte complex micelles prepared from VEGF siRNA-PEG conjugate and cationic fusogenic peptide.Biochem. Biophys. Res. Commun.357(2), 511–516 (2007).
  • Kim SH , JeongJH, LeeSH, KimSW, ParkTG: Local and systemic delivery of VEGF siRNA using polyelectrolyte complex micelles for effective treatment of cancer.J. Controlled Release129(2), 107–116 (2008).
  • Meyer M , PhilippA, OskueeR, SchmidtC, WagnerE: Breathing life into polycations: Functionalization with pH-responsive endosomolytic peptides and polyethylene glycol enables siRNA delivery.J. Am. Chem. Soc.130(11), 3272–3273 (2008).
  • Meyer M , DohmenC, Philipp A et al.: Synthesis and biological evaluation of a bioresponsive and endosomolytic siRNA-polymer conjugate. Mol. Pharm.6(3), 752–762 (2009).
  • Lee H , MokH, LeeS, OhYK, ParkTG: Target-specific intracellular delivery of siRNA using degradable hyaluronic acid nanogels.J. Controlled Release119(2), 245–252 (2007).
  • York AW , HuangF, McCormickCL: Rational design of targeted cancer therapeutics through the multiconjugation of folate and cleavable siRNA to RAFT-synthesized (HPMA-s-APMA) copolymers.Biomacromolecules11(2), 505–514 (2010).
  • Heredia KL , NguyenTH, ChangCW, BulmusV, DavisTP, MaynardHD: Reversible siRNA–polymer conjugates by RAFT polymerization.Chem. Commun.3245–3247 (2008).
  • Xu J , BoyerC, BulmusV, DavisTP: Synthesis of dendritic carbohydrate end-functional polymers via RAFT: Versatile multi-functional precursors for bioconjugations.J. Polym. Sci. A Polym. Chem.47(17), 4302–4313 (2009).
  • Barlett DW , SuH, HildebrandtIJ, WeberWA, DavisME: Impact of tumor-specific targeting on the biodistribution and efficacy of siRNA nanoparticles measured by multimodality in vivo imaging.Proc. Natl Acad. Sci. USA104(39), 15549–15554 (2007).
  • Merkel OM , LibrizziD, PfestroffAet al.: Stability of siRNA polyplexes from poly(ethylenimine) and poly(ethylenimine)-g-poly(ethylene glycol) under in vivo conditions: Effects on pharmacokinetics and biodistribution measured by fluorescence fluctuation spectroscopy and single photon emission computed tomography (SPECT) imaging.J. Controlled Release138(2), 148–159 (2009).
  • Oishi M , NagasakiY: Stimuli-responsive smart nanogels for cancer diagnostics and therapy.Nanomedicine (Lond.)5(3), 451–468 (2010).
  • Tamura A , OishiM, NagasakiY: Enhanced cytoplasmic delivery of sirna using a stabilized poly-ion complexes based on PEGylated nanogels with a cross-linked polyamine structure.Biomacromolecules10(7), 1818–1827 (2009).
  • Hu Y , AtukoralePU, LuJJet al.: Cytosolic delivery mediated via electrostatic surface binding of protein, virus, or siRNA cargos to pH-responsive core-shell gel particles.Biomacromolecules10(4), 756–765 (2009).
  • Raemdonck K , NaeyeB, BuyensKet al.: Biodegradable dextran nanogels for RNA interference: Focusing on endosomal escape and intracellular siRNA delivery.Adv. Func. Mater.19(9), 1406–1415 (2009).
  • Blackburn WH , DickersonEB, SmithMH, McDonaldJF, LyonLA: Peptide-functionalized nanogels for targeted siRNA delivery.Bioconjugate Chem.20(5), 960–968 (2009).

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