Development of RNAi technology for targeted therapy - A track of siRNA based agents to RNAi therapeutics

Journal of Controlled Release

Volumn 193, Issue , 2014, Pages 270-281

  Zhou, Yinjian ^a   Zhang, Chunling ^a   Liang, Wei ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

Author keywords

Barriers; Clinical trials; Off target effect; RNAi therapeutics; siRNA delivery

Indexed keywords

BARRIERS; CLINICAL TRIAL; OFF-TARGET EFFECT; RNAI THERAPEUTICS; SIRNA DELIVERY;

NANOPARTICLE; SMALL INTERFERING RNA; DRUG CARRIER;

ANGIOGENESIS; ARTICLE; CHEMICAL MODIFICATION; CIRCULATION; CLINICAL TRIAL (TOPIC); DRUG DELIVERY SYSTEM; ENCAPSULATION; ENDOSOME; EXTRACELLULAR MATRIX; GENE TARGETING; GENE TECHNOLOGY; HUMAN; KIDNEY CLEARANCE; NONHUMAN; POLYMERIZATION; PROTEIN BINDING; RETICULOENDOTHELIAL SYSTEM; RNA INTERFERENCE; TUMOR CELL; ANIMAL; BLOOD; CHEMISTRY; GENETICS; METABOLISM; NEOPLASMS; PHARMACEUTICS; TISSUE DISTRIBUTION;

ANIMALS; DRUG CARRIERS; EXTRACELLULAR MATRIX; GENE TARGETING; HUMANS; NEOPLASMS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TECHNOLOGY, PHARMACEUTICAL; TISSUE DISTRIBUTION;

EID: 84908266291     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.04.044     Document Type: Article

References (148)

1. A. Fire, S. Xu, M.K. Montgomery, S.A. Kostas, S.E. Driver, and C.C. Mello Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 391 1998 806 811
2. C.A. Sledz, and B.R. Williams RNA interference in biology and disease Blood 106 2005 787 794
3. L.P. Ford, and M.M. Toloue Delivery of RNAi mediators, Wiley interdisciplinary reviews RNA 1 2010 341 350
4. N. Manjunath, and D.M. Dykxhoorn Advances in synthetic siRNA delivery Discov. Med. 9 2010 418 430
5. S.L. Ameres, J. Martinez, and R. Schroeder Molecular basis for target RNA recognition and cleavage by human RISC Cell 130 2007 101 112
6. M. DiFiglia, M. Sena-Esteves, K. Chase, E. Sapp, E. Pfister, M. Sass, J. Yoder, P. Reeves, R.K. Pandey, K.G. Rajeev, M. Manoharan, D.W. Sah, P.D. Zamore, and N. Aronin Therapeutic silencing of mutant huntingtin with siRNA attenuates striatal and cortical neuropathology and behavioral deficits Proc. Natl. Acad. Sci. U. S. A. 104 2007 17204 17209
7. J. DeVincenzo, R. Lambkin-Williams, T. Wilkinson, J. Cehelsky, S. Nochur, E. Walsh, R. Meyers, J. Gollob, and A. Vaishnaw A randomized, double-blind, placebo-controlled study of an RNAi-based therapy directed against respiratory syncytial virus Proc. Natl. Acad. Sci. U. S. A. 107 2010 8800 8805
8. S.I. Pai, Y.Y. Lin, B. Macaes, A. Meneshian, C.F. Hung, and T.C. Wu Prospects of RNA interference therapy for cancer Gene Ther. 13 2006 464 477
9. F.T. Vicentini, L.N. Borgheti-Cardoso, L.V. Depieri, D. de Macedo Mano, T.F. Abelha, R. Petrilli, and M.V. Bentley Delivery systems and local administration routes for therapeutic siRNA Pharm. Res. 30 2013 915 931
10. J. Whelan First clinical data on RNAi Drug Discov. Today 10 2005 1014 1015
11. K. Bruno Using drug-excipient interactions for siRNA delivery Adv. Drug Deliv. Rev. 63 2011 1210 1226
12. K.A. Whitehead, R. Langer, and D.G. Anderson Knocking down barriers: advances in siRNA delivery Nat. Rev. Drug Discov. 8 2009 129 138
13. J. Soutschek, A. Akinc, B. Bramlage, K. Charisse, R. Constien, M. Donoghue, S. Elbashir, A. Geick, P. Hadwiger, J. Harborth, M. John, V. Kesavan, G. Lavine, R.K. Pandey, T. Racie, K.G. Rajeev, I. Rohl, I. Toudjarska, G. Wang, S. Wuschko, D. Bumcrot, V. Koteliansky, S. Limmer, M. Manoharan, and H.P. Vornlocher Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs Nature 432 2004 173 178
14. D.M. Dykxhoorn, D. Palliser, and J. Lieberman The silent treatment: siRNAs as small molecule drugs Gene Ther. 13 2006 541 552
15. D.W. Bartlett, and M.E. Davis Effect of siRNA nuclease stability on the in vitro and in vivo kinetics of siRNA-mediated gene silencing Biotechnol. Bioeng. 97 2007 909 921
16. M. Longmire, P.L. Choyke, and H. Kobayashi Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats Nanomedicine 3 2008 703 717
17. A. Sato, S.W. Choi, M. Hirai, A. Yamayoshi, R. Moriyama, T. Yamano, M. Takagi, A. Kano, A. Shimamoto, and A. Maruyama Polymer brush-stabilized polyplex for a siRNA carrier with long circulatory half-life J. Control. Release 122 2007 209 216
18. D.E. Owens, and N.A. Peppas Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles Int. J. Pharm. 307 2006 93 102
19. S. Dokka, D. Toledo, X.G. Shi, V. Castranova, and Y. Rojanasakul Oxygen radical-mediated pulmonary toxicity induced by some cationic liposomes Pharm. Res. 17 2000 521 525
20. D.T. Auguste, K. Furman, A. Wong, J. Fuller, S.P. Armes, T.J. Deming, and R. Langer Triggered release of siRNA from poly(ethylene glycol)-protected, pH-dependent liposomes J. Control. Release 130 2008 266 274
21. S. Salmaso, and P. Caliceti Stealth properties to improve therapeutic efficacy of drug nanocarriers J. Drug Deliv. 2013 2013 (article ID: 374252)
22. D. Peer, and J. Lieberman Special delivery: targeted therapy with small RNAs Gene Ther. 18 2011 1127 1133
23. J. Heyes, L. Palmer, K. Bremner, and I. MacLachlan Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids J. Control. Release 107 2005 276 287
24. R. Juliano, M.R. Alam, V. Dixit, and H. Kang Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides Nucleic Acids Res. 36 2008 4158 4171
25. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs Cancer Res. 46 1986 6387 6392
26. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284
27. G.J. Villares, M. Zigler, H. Wang, V.O. Melnikova, H. Wu, R. Friedman, M.C. Leslie, P.E. Vivas-Mejia, G. Lopez-Berestein, A.K. Sood, and M. Bar-Eli Targeting melanoma growth and metastasis with systemic delivery of liposome-incorporated protease-activated receptor-1 small interfering RNA Cancer Res. 68 2008 9078 9086
28. J.S. Desgrosellier, and D.A. Cheresh Integrins in cancer: biological implications and therapeutic opportunities, nature reviews Cancer 10 2010 9 22
29. Y. Sakurai, H. Hatakeyama, Y. Sato, M. Hyodo, H. Akita, N. Ohga, K. Hida, and H. Harashima RNAi-mediated gene knockdown and anti-angiogenic therapy of RCCs using a cyclic RGD-modified liposomal-siRNA system J. Control. Release 173 2014 110 118
30. H. Hillaireau, and P. Couvreur Nanocarriers' entry into the cell: relevance to drug delivery Cell. Mol. Life Sci. 66 2009 2873 2896
31. J. Nguyen, and F.C. Szoka Nucleic acid delivery: the missing pieces of the puzzle? Acc. Chem. Res. 45 2012 1153 1162
32. D. Vercauteren, J. Rejman, T.F. Martens, J. Demeester, S.C. De Smedt, and K. Braeckmans On the cellular processing of non-viral nanomedicines for nucleic acid delivery: mechanisms and methods J. Control. Release 161 2012 566 581
33. S. Kumari, M.G. Swetha, and S. Mayor Endocytosis unplugged: multiple ways to enter the cell Cell Res. 20 2010 256 275
34. L.M. Bareford, and P.W. Swaan Endocytic mechanisms for targeted drug delivery Adv. Drug Deliv. Rev. 59 2007 748 758
35. J. Rejman, V. Oberle, I.S. Zuhorn, and D. Hoekstra Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis Biochem. J. 377 2004 159 169
36. S. Mao, O. Germershaus, D. Fischer, T. Linn, R. Schnepf, and T. Kissel Uptake and transport of PEG-graft-trimethyl-chitosan copolymer-insulin nanocomplexes by epithelial cells Pharm. Res. 22 2005 2058 2068
37. O. Harush-Frenkel, N. Debotton, S. Benita, and Y. Altschuler Targeting of nanoparticles to the clathrin-mediated endocytic pathway Biochem. Biophys. Res. Commun. 353 2007 26 32
38. H.R. Kim, K. Andrieux, S. Gil, M. Taverna, H. Chacun, D. Desmaele, F. Taran, D. Georgin, and P. Couvreur Translocation of poly(ethylene glycol-co-hexadecyl)cyanoacrylate nanoparticles into rat brain endothelial cells: role of apolipoproteins in receptor-mediated endocytosis Biomacromolecules 8 2007 793 799
39. M. Ogris, P. Steinlein, S. Carotta, S. Brunner, and E. Wagner DNA/polyethylenimine transfection particles: influence of ligands, polymer size, and PEGylation on internalization and gene expression AAPS PharmSci 3 2001 E21
40. C. Foerg, U. Ziegler, J. Fernandez-Carneado, E. Giralt, R. Rennert, A.G. Beck-Sickinger, and H.P. Merkle Decoding the entry of two novel cell-penetrating peptides in HeLa cells: lipid raft-mediated endocytosis and endosomal escape Biochemistry 44 2005 72 81
41. C. Moreira, H. Oliveira, L.R. Pires, S. Simoes, M.A. Barbosa, and A.P. Pego Improving chitosan-mediated gene transfer by the introduction of intracellular buffering moieties into the chitosan backbone Acta Biomater. 5 2009 2995 3006
42. H. Yu, Y. Zou, Y. Wang, X. Huang, G. Huang, B.D. Sumer, D.A. Boothman, and J. Gao Overcoming endosomal barrier by amphotericin B-loaded dual pH-responsive PDMA-b-PDPA micelleplexes for siRNA delivery ACS Nano 5 2011 9246 9255
43. S. Kakimoto, T. Hamada, Y. Komatsu, M. Takagi, T. Tanabe, H. Azuma, S. Shinkai, and T. Nagasaki The conjugation of diphtheria toxin T domain to poly(ethylenimine) based vectors for enhanced endosomal escape during gene transfection Biomaterials 30 2009 402 408
44. H. Jenssen, P. Hamill, and R.E. Hancock Peptide antimicrobial agents Clin. Microbiol. Rev. 19 2006 491 511
45. T. Endoh, and T. Ohtsuki Cellular siRNA delivery using cell-penetrating peptides modified for endosomal escape Adv. Drug Deliv. Rev. 61 2009 704 709
46. S.C. Semple, A. Akinc, J. Chen, A.P. Sandhu, B.L. Mui, C.K. Cho, D.W. Sah, D. Stebbing, E.J. Crosley, E. Yaworski, I.M. Hafez, J.R. Dorkin, J. Qin, K. Lam, K.G. Rajeev, K.F. Wong, L.B. Jeffs, L. Nechev, M.L. Eisenhardt, M. Jayaraman, M. Kazem, M.A. Maier, M. Srinivasulu, M.J. Weinstein, Q. Chen, R. Alvarez, S.A. Barros, S. De, S.K. Klimuk, T. Borland, V. Kosovrasti, W.L. Cantley, Y.K. Tam, M. Manoharan, M.A. Ciufolini, M.A. Tracy, A. de Fougerolles, I. MacLachlan, P.R. Cullis, T.D. Madden, and M.J. Hope Rational design of cationic lipids for siRNA delivery Nat. Biotechnol. 28 2010 172 176
47. N.D. Sonawane, F.C. Szoka, and A.S. Verkman Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes J. Biol. Chem. 278 2003 44826 44831
48. A. Kichler, A.J. Mason, A. Marquette, and B. Bechinger Histidine-rich cationic amphipathic peptides for plasmid DNA and siRNA delivery Methods Mol. Biol. 948 2013 85 103
49. A.K. Varkouhi, M. Scholte, G. Storm, and H.J. Haisma Endosomal escape pathways for delivery of biologicals J. Control. Release 151 2011 220 228
50. A.L. Jackson, S.R. Bartz, J. Schelter, S.V. Kobayashi, J. Burchard, M. Mao, B. Li, G. Cavet, and P.S. Linsley Expression profiling reveals off-target gene regulation by RNAi Nat. Biotechnol. 21 2003 635 637
51. A.L. Jackson, J. Burchard, D. Leake, A. Reynolds, J. Schelter, J. Guo, J.M. Johnson, L. Lim, J. Karpilow, K. Nichols, W. Marshall, A. Khvorova, and P.S. Linsley Position-specific chemical modification of siRNAs reduces "off-target" transcript silencing RNA 12 2006 1197 1205
52. E. Iorns, C.J. Lord, N. Turner, and A. Ashworth Utilizing RNA interference to enhance cancer drug discovery Nat. Rev. Drug Discov. 6 2007 556 568
53. R. Kittler, V. Surendranath, A.K. Heninger, M. Slabicki, M. Theis, G. Putz, K. Franke, A. Caldarelli, H. Grabner, K. Kozak, J. Wagner, E. Rees, B. Korn, C. Frenzel, C. Sachse, B. Sonnichsen, J. Guo, J. Schelter, J. Burchard, P.S. Linsley, A.L. Jackson, B. Habermann, and F. Buchholz Genome-wide resources of endoribonuclease-prepared short interfering RNAs for specific loss-of-function studies Nat. Methods 4 2007 337 344
54. M. Schlee, V. Hornung, and G. Hartmann siRNA and isRNA: two edges of one sword Mol. Ther. 14 2006 463 470
55. A.L. Jackson, and P.S. Linsley Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application Nat. Rev. Drug Discov. 9 2010 57 67
56. V. Hornung, M. Guenthner-Biller, C. Bourquin, A. Ablasser, M. Schlee, S. Uematsu, A. Noronha, M. Manoharan, S. Akira, A. de Fougerolles, S. Endres, and G. Hartmann Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7 Nat. Med. 11 2005 263 270
57. A. Judge, and I. MacLachlan Overcoming the innate immune response to small interfering RNA Hum. Gene Ther. 19 2008 111 124
58. A.A. Khan, D. Betel, M.L. Miller, C. Sander, C.S. Leslie, and D.S. Marks Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs Nat. Biotechnol. 27 2009 549 555
59. S. Shukla, C.S. Sumaria, and P.I. Pradeepkumar Exploring chemical modifications for siRNA therapeutics: a structural and functional outlook ChemMedChem 5 2010 328 349
60. J.B. Bramsen, and J. Kjems Chemical modification of small interfering RNA Methods Mol. Biol. 721 2011 77 103
61. S. Choung, Y.J. Kim, S. Kim, H.O. Park, and Y.C. Choi Chemical modification of siRNAs to improve serum stability without loss of efficacy Biochem. Biophys. Res. Commun. 342 2006 919 927
62. J.B. Bramsen, M.B. Laursen, A.F. Nielsen, T.B. Hansen, C. Bus, N. Langkjaer, B.R. Babu, T. Hojland, M. Abramov, A. Van Aerschot, D. Odadzic, R. Smicius, J. Haas, C. Andree, J. Barman, M. Wenska, P. Srivastava, C. Zhou, D. Honcharenko, S. Hess, E. Muller, G.V. Bobkov, S.N. Mikhailov, E. Fava, T.F. Meyer, J. Chattopadhyaya, M. Zerial, J.W. Engels, P. Herdewijn, J. Wengel, and J. Kjems A large-scale chemical modification screen identifies design rules to generate siRNAs with high activity, high stability and low toxicity Nucleic Acids Res. 37 2009 2867 2881
63. M. Amarzguioui, and J.J. Rossi Principles of Dicer substrate (D-siRNA) design and function Methods Mol. Biol. 442 2008 3 10
64. F. Iversen, C.X. Yang, F. Dagnaes-Hansen, D.H. Schaffert, J. Kjems, and S. Gao Optimized siRNA-PEG conjugates for extended blood circulation and reduced urine excretion in mice Theranostics 3 2013 201 209
65. B.R. Meade, and S.F. Dowdy Exogenous siRNA delivery using peptide transduction domains/cell penetrating peptides Adv. Drug Deliv. Rev. 59 2007 134 140
66. A.L. Bolcato-Bellemin, M.E. Bonnet, G. Creusat, P. Erbacher, and J.P. Behr Sticky overhangs enhance siRNA-mediated gene silencing Proc. Natl. Acad. Sci. U. S. A. 104 2007 16050 16055
67. A. Schroeder, C.G. Levins, C. Cortez, R. Langer, and D.G. Anderson Lipid-based nanotherapeutics for siRNA delivery J. Intern. Med. 267 2010 9 21
68. S. Hobel, and A. Aigner Polyethylenimine (PEI)/siRNA-mediated gene knockdown in vitro and in vivo Methods Mol. Biol. 623 2010 283 297
69. A. Kano, K. Moriyama, T. Yamano, I. Nakamura, N. Shimada, and A. Maruyama Grafting of poly(ethylene glycol) to poly-lysine augments its lifetime in blood circulation and accumulation in tumors without loss of the ability to associate with siRNA J. Control. Release 149 2011 2 7
70. E. Kawakami, N. Kinouchi, T. Adachi, Y. Ohsawa, N. Ishimaru, H. Ohuchi, Y. Sunada, Y. Hayashi, E. Tanaka, and S. Noji Atelocollagen-mediated systemic administration of myostatin-targeting siRNA improves muscular atrophy in caveolin-3-deficient mice Dev. Growth Differ. 53 2011 48 54
71. M. Chen, S. Gao, M. Dong, J. Song, C. Yang, K.A. Howard, J. Kjems, and F. Besenbacher Chitosan/siRNA nanoparticles encapsulated in PLGA nanofibers for siRNA delivery ACS Nano 6 2012 4835 4844
72. U.l. Langel Cell-penetrating Peptides: Methods and Protocols 2011 Humana Press New York, NY
73. X.X. Liu, P. Rocchi, and L. Peng Dendrimers as non-viral vectors for siRNA delivery N. J. Chem. 36 2012 256 263
74. J.D. Heidel, and T. Schluep Cyclodextrin-containing polymers: versatile platforms of drug delivery materials J. Drug Deliv. 2012 2012 (Article ID 262731)
75. A.W. Tong, C.M. Jay, N. Senzer, P.B. Maples, and J. Nemunaitis Systemic therapeutic gene delivery for cancer: crafting Paris' arrow Curr. Gene Ther. 9 2009 45 60
76. Y. Wang, Z.G. Li, Y. Han, L.H. Liang, and A.M. Ji Nanoparticle-based delivery system for application of siRNA in vivo Curr. Drug Metab. 11 2010 182 196
77. S. Hobel, I. Koburger, M. John, F. Czubayko, P. Hadwiger, H.P. Vornlocher, and A. Aigner Polyethylenimine/small interfering RNA-mediated knockdown of vascular endothelial growth factor in vivo exerts anti-tumor effects synergistically with Bevacizumab J. Gene Med. 12 2010 287 300
78. S. Gao, F. Dagnaes-Hansen, E.J.B. Nielsen, J. Wengel, F. Besenbacher, K.A. Howard, and J. Kjems The effect of chemical modification and nanoparticle formulation on stability and biodistribution of siRNA in mice Mol. Ther. 17 2009 1225 1233
79. J. Zhou, K.T. Shum, J.C. Burnett, and J.J. Rossi Nanoparticle-based delivery of RNAi therapeutics: progress and challenges Pharmaceuticals (Basel) 6 2013 85 107
80. X. Liu, J. Wu, M. Yammine, J. Zhou, P. Posocco, S. Viel, C. Liu, F. Ziarelli, M. Fermeglia, S. Pricl, G. Victorero, C. Nguyen, P. Erbacher, J.P. Behr, and L. Peng Structurally flexible triethanolamine core PAMAM dendrimers are effective nanovectors for DNA transfection in vitro and in vivo to the mouse thymus Bioconjug. Chem. 22 2011 2461 2473
81. J.H. Zhou, J.Y. Wu, N. Hafdi, J.P. Behr, P. Erbacher, and L. Peng PAMAM dendrimers for efficient siRNA delivery and potent gene silencing Chem. Commun. 2006 2362 2364
82. W.E. Rudzinski, and T.M. Aminabhavi Chitosan as a carrier for targeted delivery of small interfering RNA Int. J. Pharm. 399 2010 1 11
83. H. Katas, and H.O. Alpar Development and characterisation of chitosan nanoparticles for siRNA delivery J. Control. Release 115 2006 216 225
84. K.A. Howard, S.R. Paludan, M.A. Behlke, F. Besenbacher, B. Deleuran, and J. Kjems Chitosan/siRNA nanoparticle-mediated TNF-alpha knockdown in peritoneal macrophages for anti-inflammatory treatment in a murine arthritis model Mol. Ther. 17 2009 162 168
85. F. Heitz, M.C. Morris, and G. Divita Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics Br. J. Pharmacol. 157 2009 195 206
86. L. Crombez, G. Aldrian-Herrada, K. Konate, Q.N. Nguyen, G.K. McMaster, R. Brasseur, F. Heitz, and G. Divita A new potent secondary amphipathic cell-penetrating peptide for siRNA delivery into mammalian cells Mol. Ther. 17 2009 95 103
87. A. Akinc, A. Zumbuehl, M. Goldberg, E.S. Leshchiner, V. Busini, N. Hossain, S.A. Bacallado, D.N. Nguyen, J. Fuller, R. Alvarez, A. Borodovsky, T. Borland, R. Constien, A. de Fougerolles, J.R. Dorkin, K.N. Jayaprakash, M. Jayaraman, M. John, V. Koteliansky, M. Manoharan, L. Nechev, J. Qin, T. Racie, D. Raitcheva, K.G. Rajeev, D.W.Y. Sah, J. Soutschek, I. Toudjarska, H.P. Vornlocher, T.S. Zimmermann, R. Langer, and D.G. Anderson A combinatorial library of lipid-like materials for delivery of RNAi therapeutics Nat. Biotechnol. 26 2008 561 569
88. K.T. Love, K.P. Mahon, C.G. Levins, K.A. Whitehead, W. Querbes, J.R. Dorkin, J. Qin, W. Cantley, L.L. Qin, T. Racie, M. Frank-Kamenetsky, K.N. Yip, R. Alvarez, D.W.Y. Sah, A. de Fougerolles, K. Fitzgerald, V. Koteliansky, A. Akinc, R. Langer, and D.G. Anderson Lipid-like materials for low-dose, in vivo gene silencing Proc. Natl. Acad. Sci. U. S. A. 107 2010 1864 1869
89. R. Gref, M. Luck, P. Quellec, M. Marchand, E. Dellacherie, S. Harnisch, T. Blunk, and R.H. Muller 'Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption Colloids Surf. B Biointerfaces 18 2000 301 313
90. X. Yan, G.L. Scherphof, and J.A. Kamps Liposome opsonization J. Liposome Res. 15 2005 109 139
91. J.G. Li, D. Cheng, T.H. Yin, W.C. Chen, Y.J. Lin, J.F. Chen, R.T. Li, and X.T. Shuai Copolymer of poly(ethylene glycol) and poly((l)-lysine) grafting polyethylenimine through a reducible disulfide linkage for siRNA delivery Nanoscale 6 2014 1732 1740
92. S. Stolnik, S.E. Dunn, M.C. Garnett, M.C. Davies, A.G. Coombes, D.C. Taylor, M.P. Irving, S.C. Purkiss, T.F. Tadros, and S.S. Davis Surface modification of poly(lactide-co-glycolide) nanospheres by biodegradable poly(lactide)-poly(ethylene glycol) copolymers Pharm. Res. 11 1994 1800 1808
93. K. Kostarelos, T.F. Tadros, and P.F. Luckham Physical conjugation of (tri-) block copolymers to liposomes toward the construction of sterically stabilized vesicle systems Langmuir 15 1999 369 376
94. K. Kostarelos, and A.D. Miller Synthetic, self-assembly ABCD nanoparticles; a structural paradigm for viable synthetic non-viral vectors Chem. Soc. Rev. 34 2005 970 994
95. J. Wang, Y. Wang, and W. Liang Delivery of drugs to cell membranes by encapsulation in PEG-PE micelles J. Control. Release 160 2012 637 651
96. T. Musacchio, O. Vaze, G. D'Souza, and V.P. Torchilin Effective stabilization and delivery of siRNA: reversible siRNA-phospholipid conjugate in nanosized mixed polymeric micelles Bioconjug. Chem. 21 2010 1530 1536
97. N. Tang, G. Du, N. Wang, C. Liu, H. Hang, and W. Liang Improving penetration in tumors with nanoassemblies of phospholipids and doxorubicin J. Natl. Cancer Inst. 99 2007 1004 1015
98. L. Qin, F. Zhang, X. Lu, X. Wei, J. Wang, X. Fang, D. Si, Y. Wang, C. Zhang, R. Yang, C. Liu, and W. Liang Polymeric micelles for enhanced lymphatic drug delivery to treat metastatic tumors J. Control. Release 171 2013 133 142
99. C. Zhang, N. Tang, X. Liu, W. Liang, W. Xu, and V.P. Torchilin siRNA-containing liposomes modified with polyarginine effectively silence the targeted gene J. Control. Release 112 2006 229 239
100. A. Aigner Nonviral in vivo delivery of therapeutic small interfering RNAs Curr. Opin. Mol. Ther. 9 2007 345 352
101. J.J. Rossi RNAi therapeutics: SNALPing siRNAs in vivo Gene Ther. 13 2006 583 584
102. O.M. Merkel, A. Beyerle, D. Librizzi, A. Pfestroff, T.M. Behr, B. Sproat, P.J. Barth, and T. Kissel Nonviral siRNA delivery to the lung: investigation of PEG-PEI polyplexes and their in vivo performance Mol. Pharm. 6 2009 1246 1260
103. L.R. Tsai, M.H. Chen, C.T. Chien, M.K. Chen, F.S. Lin, K.M. Lin, Y.K. Hwu, C.S. Yang, and S.Y. Lin A single-monomer derived linear-like PEI-co-PEG for siRNA delivery and silencing Biomaterials 32 2011 3647 3653
104. S.R. Mao, W. Sun, and T. Kissel Chitosan-based formulations for delivery of DNA and siRNA Adv. Drug Deliv. Rev. 62 2010 12 27
105. M. Ravina, E. Cubillo, D. Olmeda, R. Novoa-Carballal, E. Fernandez-Megia, R. Riguera, A. Sanchez, A. Cano, and M.J. Alonso Hyaluronic acid/chitosan-g-poly(ethylene glycol) nanoparticles for gene therapy: an application for pDNA and siRNA delivery Pharm. Res. 27 2010 2544 2555
106. A. Daka, and D. Peer RNAi-based nanomedicines for targeted personalized therapy Adv. Drug Deliv. Rev. 64 2012 1508 1521
107. J. Shen, R. Samul, R.L. Silva, H. Akiyama, H. Liu, Y. Saishin, S.F. Hackett, S. Zinnen, K. Kossen, K. Fosnaugh, C. Vargeese, A. Gomez, K. Bouhana, R. Aitchison, P. Pavco, and P.A. Campochiaro Suppression of ocular neovascularization with siRNA targeting VEGF receptor 1 Gene Ther. 13 2006 225 234
108. X.Y. Niu, Z.L. Peng, W.Q. Duan, H. Wang, and P. Wang Inhibition of HPV 16 E6 oncogene expression by RNA interference in vitro and in vivo Int. J. Gynecol. Cancer 16 2006 743 751
109. S.M. Tompkins, C.Y. Lo, T.M. Tumpey, and S.L. Epstein Protection against lethal influenza virus challenge by RNA interference in vivo Proc. Natl. Acad. Sci. U. S. A. 101 2004 8682 8686
110. P.H. Tan, L.C. Yang, H.C. Shih, K.C. Lan, and J.T. Cheng Gene knockdown with intrathecal siRNA of NMDA receptor NR2B subunit reduces formalin-induced nociception in the rat Gene Ther. 12 2005 59 66
111. M.A. Tran, R. Gowda, A. Sharma, E.J. Park, J. Adair, M. Kester, N.B. Smith, and G.P. Robertson Targeting B-V600E-Raf and AW using nanoliposomal-small interfering RNA inhibits cutaneous melanocytic lesion development Cancer Res. 68 2008 7638 7649
112. S. David, B. Pitard, J.P. Benoit, and C. Passirani Non-viral nanosystems for systemic siRNA delivery Pharmacol. Res. 62 2010 100 114
113. A.K. Iyer, G. Khaled, J. Fang, and H. Maeda Exploiting the enhanced permeability and retention effect for tumor targeting Drug Discov. Today 11 2006 812 818
114. T. Ishimoto, Y. Takei, Y. Yuzawa, K. Hanai, S. Nagahara, Y. Tarumi, S. Matsuo, and K. Kadomatsu Downregulation of monocyte chemoattractant protein-1 involving short interfering RNA attenuates hapten-induced contact hypersensitivity Mol. Ther. 16 2008 387 395
115. E. Kawata, E. Ashihara, S. Kimura, K. Takenaka, K. Sato, R. Tanaka, A. Yokota, Y. Kamitsuji, M. Takeuchi, J. Kuroda, F. Tanaka, T. Yoshikawa, and T. Maekawa Administration of PLK-1 small interfering RNA with atelocollagen prevents the growth of liver metastases of lung cancer Mol. Cancer Ther. 7 2008 2904 2912
116. T.M. Allen, and P.R. Cullis Liposomal drug delivery systems: from concept to clinical applications Adv. Drug Deliv. Rev. 65 2013 36 48
117. T.S. Zimmermann, A.C. Lee, A. Akinc, B. Bramlage, D. Bumcrot, M.N. Fedoruk, J. Harborth, J.A. Heyes, L.B. Jeffs, M. John, A.D. Judge, K. Lam, K. McClintock, L.V. Nechev, L.R. Palmer, T. Racie, I. Rohl, S. Seiffert, S. Shanmugam, V. Sood, J. Soutschek, I. Toudjarska, A.J. Wheat, E. Yaworski, W. Zedalis, V. Koteliansky, M. Manoharan, H.P. Vornlocher, and I. MacLachlan RNAi-mediated gene silencing in non-human primates Nature 441 2006 111 114
118. R.O. Hynes A reevaluation of integrins as regulators of angiogenesis Nat. Med. 8 2002 918 921
119. R.M. Schiffelers, A. Ansari, J. Xu, Q. Zhou, Q. Tang, G. Storm, G. Molema, P.Y. Lu, P.V. Scaria, and M.C. Woodle Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle Nucleic Acids Res. 32 2004 e149
120. X.F. Zheng, C. Vladau, X.S. Zhang, M. Suzuki, T.E. Ichim, Z.X. Zhang, M. Li, E. Carrier, B. Garcia, A.M. Jevnikar, and W.P. Min A novel in vivo siRNA delivery system specifically targeting dendritic cells and silencing CD40 genes for immunomodulation Blood 113 2009 2646 2654
121. E.W. Song, P.C. Zhu, S.K. Lee, D. Chowdhury, S. Kussman, D.M. Dykxhoorn, Y. Feng, D. Palliser, D.B. Weiner, P. Shankar, W.A. Marasco, and J. Lieberman Antibody mediated in vivo delivery of small interfering RNAs via cell-surface receptors Nat. Biotechnol. 23 2005 709 717
122. P. Kumar, H.S. Ban, S.S. Kim, H.Q. Wu, T. Pearson, D.L. Greiner, A. Laouar, J.H. Yao, V. Haridas, K. Habiro, Y.G. Yang, J.H. Jeong, K.Y. Lee, Y.H. Kim, S.W. Kim, M. Peipp, G.H. Fey, N. Manjunath, L.D. Shultz, S.K. Lee, and P. Shankar T cell-specific siRNA delivery suppresses HIV-1 infection in humanized mice Cell 134 2008 577 586
123. P. Kumar, H.Q. Wu, J.L. McBride, K.E. Jung, M.H. Kim, B.L. Davidson, S.K. Lee, P. Shankar, and N. Manjunath Transvascular delivery of small interfering RNA to the central nervous system Nature 448 2007 39 43
124. J.Y. Yhee, S.J. Lee, S. Lee, S. Song, H.S. Min, S.W. Kang, S. Son, S.Y. Jeong, I.C. Kwon, S.H. Kim, and K. Kim Tumor-targeting transferrin nanoparticles for systemic polymerized siRNA delivery in tumor-bearing mice Bioconjug. Chem. 24 2013 1850 1860
125. G.Y. Xiang, J. Wu, Y.H. Lu, Z.L. Liu, and R.J. Lee Synthesis and evaluation of a novel ligand for folate-mediated targeting liposomes Int. J. Pharm. 356 2008 29 36
126. D. Peer, J.M. Karp, S. Hong, O.C. FaroKHzad, R. Margalit, and R. Langer Nanocarriers as an emerging platform for cancer therapy Nat. Nanotechnol. 2 2007 751 760
127. X. Li, Q.H. Zhao, and L.Y. Qiu Smart ligand: aptamer-mediated targeted delivery of chemotherapeutic drugs and siRNA for cancer therapy J. Control. Release 171 2013 152 162
128. Y.D. Yao, T.M. Sun, S.Y. Huang, S. Dou, L. Lin, J.N. Chen, J.B. Ruan, C.Q. Mao, F.Y. Yu, M.S. Zeng, J.Y. Zang, Q. Liu, F.X. Su, P. Zhang, J. Lieberman, J. Wang, and E. Song Targeted delivery of PLK1-siRNA by ScFv suppresses Her2 + breast cancer growth and metastasis Sci. Transl. Med. 4 2012 130ra148
129. S.S. Kim, S. Subramanya, D. Peer, M. Shimaoka, and P. Shankar Antibody-mediated delivery of siRNAs for anti-HIV therapy Methods Mol. Biol. 721 2011 339 353
130. M.E. Davis, J.E. Zuckerman, C.H. Choi, D. Seligson, A. Tolcher, C.A. Alabi, Y. Yen, J.D. Heidel, and A. Ribas Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles Nature 464 2010 1067 1070
131. J.D. Heidel, Z. Yu, J.Y. Liu, S.M. Rele, Y. Liang, R.K. Zeidan, D.J. Kornbrust, and M.E. Davis Administration in non-human primates of escalating intravenous doses of targeted nanoparticles containing ribonucleotide reductase subunit M2 siRNA Proc. Natl. Acad. Sci. U. S. A. 104 2007 5715 5721
132. A.C. Yan, and M. Levy Aptamers and aptamer targeted delivery RNA Biol. 6 2009 316 320
133. A. Daka, and D. Peer RNAi-based nanomedicines for targeted personalized therapy Adv. Drug Deliv. Rev. 64 2012 1508 1521
134. J.P. Dassie, X.Y. Liu, G.S. Thomas, R.M. Whitaker, K.W. Thiel, K.R. Stockdale, D.K. Meyerholz, A.P. McCaffrey, J.O. McNamara II, and P.H. Giangrande Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors Nat. Biotechnol. 27 2009 839 849
135. D. Hymel, and B.R. Peterson Synthetic cell surface receptors for delivery of therapeutics and probes Adv. Drug Deliv. Rev. 64 2012 797 810
136. H. Arima, A. Yoshimatsu, H. Ikeda, A. Ohyama, K. Motoyama, T. Higashi, A. Tsuchiya, T. Niidome, Y. Katayama, K. Hattori, and T. Takeuchi Folate-PEG-appended dendrimer conjugate with alpha-cyclodextrin as a novel cancer cell-selective siRNA delivery carrier Mol. Pharm. 9 2012 2591 2604
137. M. Oishi, Y. Nagasaki, N. Nishiyama, K. Itaka, M. Takagi, A. Shimamoto, Y. Furuichi, and K. Kataoka Enhanced growth inhibition of hepatic multicellular tumor spheroids by lactosylated poly(ethylene glycol)-siRNA conjugate formulated in PEGylated polyplexes ChemMedChem 2 2007 1290 1297
138. W. Zhou, X. Yuan, A. Wilson, L. Yang, M. Mokotoff, B. Pitt, and S. Li Efficient intracellular delivery of oligonucleotides formulated in folate receptor-targeted lipid vesicles Bioconjug. Chem. 13 2002 1220 1225
139. A.T. Jones, and E.J. Sayers Cell entry of cell penetrating peptides: tales of tails wagging dogs J. Control. Release 161 2012 582 591
140. B. Gupta, and V.P. Torchilin Transactivating transcriptional activator-mediated drug delivery Expert Opin. Drug Deliv. 3 2006 177 190
141. C. Lin, and J.F. Engbersen Effect of chemical functionalities in poly(amido amine)s for non-viral gene transfection J. Control. Release 132 2008 267 272
142. N. Nishiyama, Arnida, W.D. Jang, K. Date, K. Miyata, and K. Kataoka Photochemical enhancement of transgene expression by polymeric micelles incorporating plasmid DNA and dendrimer-based photosensitizer J. Drug Target. 14 2006 413 424
143. P.J. Lou, P.S. Lai, M.J. Shieh, A.J. Macrobert, K. Berg, and S.G. Bown Reversal of doxorubicin resistance in breast cancer cells by photochemical internalization Int. J. Cancer 119 2006 2692 2698
144. K. Sasaki, K. Kogure, S. Chaki, Y. Nakamura, R. Moriguchi, H. Hamada, R. Danev, K. Nagayama, S. Futaki, and H. Harashima An artificial virus-like nano carrier system: enhanced endosomal escape of nanoparticles via synergistic action of pH-sensitive fusogenic peptide derivatives Anal. Bioanal. Chem. 391 2008 2717 2727
145. H. Hatakeyama, E. Ito, H. Akita, M. Oishi, Y. Nagasaki, S. Futaki, and H. Harashima A pH-sensitive fusogenic peptide facilitates endosomal escape and greatly enhances the gene silencing of siRNA-containing nanoparticles in vitro and in vivo J. Control. Release 139 2009 127 132
146. J.C. Burnett, J.J. Rossi, and K. Tiemann Current progress of siRNA/shRNA therapeutics in clinical trials Biotechnol. J. 6 2011 1130 1146
147. D.L. Stirland, J.W. Nichols, S. Miura, and Y.H. Bae Mind the gap: a survey of how cancer drug carriers are susceptible to the gap between research and practice J. Control. Release 172 2013 1045 1064
148. T. Coelho, D. Adams, A. Silva, P. Lozeron, P.N. Hawkins, T. Mant, J. Perez, J. Chiesa, S. Warrington, E. Tranter, M. Munisamy, R. Falzone, J. Harrop, J. Cehelsky, B.R. Bettencourt, M. Geissler, J.S. Butler, A. Sehgal, R.E. Meyers, Q.M. Chen, T. Borland, R.M. Hutabarat, V.A. Clausen, R. Alvarez, K. Fitzgerald, C. Gamba-Vitalo, S.V. Nochur, A.K. Vaishnaw, D.W.Y. Sah, J.A. Gollob, and O.B. Suhr Safety and efficacy of RNAi therapy for transthyretin amyloidosis N. Engl. J. Med. 369 2013 819 829.