Therapeutic targeting in the silent era: Advances in non-viral siRNA delivery

Molecular BioSystems

Volumn 6, Issue 7, 2010, Pages 1143-1161

  Guo, Jianfeng ^a   Fisher, Karen A ^a   Darcy, Raphael ^b   Cryan, John F ^a,c   O'Driscoll, Caitriona ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA;

ANIMAL; CLINICAL TRIAL; DRUG DELIVERY SYSTEM; GENETICS; HUMAN; METHODOLOGY; NEOPLASM; PHARMACEUTICS; RETINA MACULA DEGENERATION; REVIEW; RNA INTERFERENCE; CLINICAL TRIAL (TOPIC); MACULAR DEGENERATION; NEOPLASMS; PROCEDURES;

ANIMALS; CLINICAL TRIALS AS TOPIC; DRUG DELIVERY SYSTEMS; HUMANS; MACULAR DEGENERATION; NEOPLASMS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TECHNOLOGY, PHARMACEUTICAL;

MAMMALIA;

EID: 77953553846     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c001050m     Document Type: Review

References (169)

1. T. F. Kresina and A. D. Branch, Molecular Medicine and Gene Therapy, in An Introduction to Molecular Medicine and Gene Therapy, ed., T. F. Kresina,, Wiley-Liss, New York, 2001, pp. 1-24
2. C. Smith Drug target validation: Hitting the target Nature 2003 422 6929 341 347
3. T. Chapman Drug discovery: the leading edge Nature 2004 430 6995 109 115
4. A. Fire S. Xu M. K. Montgomery S. A. Kostas S. E. Driver C. C. Mello Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 1998 391 806 811
5. R. A. Van der Vlugt R. K. Ruiter R. Goldbach Evidence for sense RNA-mediated protection to PVYN in tabacco plants transformed with the viral coat protein cistron Plant Mol. Biol. 1992 20 631 639
6. S. Elbashir J. Harborth W. Lendeckel A. Yalcin K. Weber T. Tuschl Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells Nature 2001 411 494 498
7. Y. Dorsett T. Tuschl siRNAs: applications in functional genomics and potential as therapeutics Nat. Rev. Drug Discovery 2004 3 318 329
8. T. Karagiannisand A. El-Osta RNA interference and potential therapeutic applications of short interfering RNAs Cancer Gene Ther. 2005 12 787 795
9. A. de Fougerolles H.-P. Vornlocher J. Maraganore J. Lieberman Interfering with disease: a progress report on siRNA-based therapeutics Nat. Rev. Drug Discovery 2007 6 443 453
10. S. Katiyar-Agarwal D. Dahlbeck O. Borsani A. Villegas, Jr. J. K. Zhu B. J. Staskawicz H. Jin A pathogen-inducible endogenous siRNA in plant immunity Proc. Natl. Acad. Sci. U. S. A. 2006 103 18002 18007
11. L. Navarro P. Dunover F. Jay B. Arnold N. Dharmasiri M. Estelle O. Voinnet J. D. Jones A plant miRNA contributes to antibacterial resistance by repressing auxin signalling Science 2006 312 436 439
12. C. E. Thomas A. Ehrhardt M. A. Kay Progress and problems with the use of viral vectors for gene therapy Nat. Rev. Genet. 2003 4 5 346 58
13. P. B. Hajeri S. K. Singh siRNA: their potential as therapeutic agents - Part I. Designing of siRNAs Drug Discovery Today 2009 14 851 858
14. A. L. Jackson P. S. Linsley Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application Nat. Rev. Drug Discovery 2010 9 1 57 67
15. F. Jiang H. Wu Y. Da F. Sang J. Wei X. Sun Z. Lu RFRCDB-siRNA: improved design of siRNAs by random forest regression model coupled with database searching Comput. Methods Programs Biomed. 2007 87 230 238
16. D. Huesken J. Lange C. Mickanin J. Weiler F. Asselbergs J. Warner B. Meloon S. Engel A. Rosenberg D. Cohen M. Labow M. Reinhardt F. Natt J. Hall Design of a genome-wide siRNA library using an artificial neural network Nat. Biotechnol. 2005 23 995 1001
17. Y. Naito T. Yamada K. Ui-Tei S. Morishita K. Saigo siDirect: highly effective, target-specific siRNA design software for mammalian RNA interference Nucleic Acids Res. 2004 32 web server W124 W129
18. J. K. Shah H. R. Garner M. A. White D. S. Shames J. D. Minna sIR: siRNA Information Resource, a web-based tool for siRNA sequence design and analysis and an open access siRNA database BMC Bioinformatics 2007 8 178
19. R. Goraczniak M. A. Behlke S. I. Gunderson Gene silencing by synthetic U1 adaptors Nat. Biotechnol. 2009 27 257 263
20. A. L. Jackson S. R. Bartz J. Schelter S. V. Kobayashi J. Burchard M. Mao B. Li G. Cavet P. S. Linsley Expression profiling reveals off-target gene regulation by RNAi Nat. Biotechnol. 2003 21 635 637
21. A. Birmingham E. M. Anderson A. Reynolds D. Ilsley-Tyree D. Leake Y. Fedorov S. Baskerville E. Maksimova K. Robinsion J. Karpilow W. S. Marshall A. Khvornova 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets Nat. Methods 2006 3 199 204
22. Y. Fedorov E. M. Anderson A. Birmingham A. Reynolds J. Karpliow K. Robinson D. Leake W. S. Marshall A. Khvorova Off-target effects by siRNA can induce toxic phenotype RNA 2006 12 1188 1196
23. P. Y. Chen L. Weinmann D. Gaidatzis Y. Pei M. Zavolan T. Tuschl G. Meister Strand-specific 5′-O-methylation of siRNA duplexes controls guide strand selection and targeting specificity RNA 2008 14 263 274
24. 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 P. S. Linsley Position-specific chemical modification of siRNAs reduces "off-target" transcript silencing RNA 2006 12 1197 1205
25. M. Schlee V. Hornung G. Hartmann siRNA and isRNA: two edges of one sword Mol. Ther. 2006 14 463 470
26. C. A. Sledz M. Holko M. J. de Veer R. H. Silverman B. R. Williams Activation of the interferon system by short-interfering RNAs Nat. Cell Biol. 2003 5 834 839
27. K. Kariko P. Bhuyan J. Capodici D. Weissman Small interfering RNAs mediate sequence-independent gene suppression and induce immune activation by signalling through toll-like receptor 3 J. Immunol. 2004 172 6545 6549
28. M. E. Kleinman K. Yamada A. Takeda V. Chandrasekaran M. Nozaki J. Z. Baffi R. J. Albuquerque S. Yamasaki M. Itaya Y. Pan B. Appukuttan D. Gibbs Z. Yang K. Kariko B. K. Ambati et al. Sequence- and target-independent angiogenesis suppression by siRNA via TLR3 Nature 2008 452 591 598
29. V. Hornung M. Guenthner-Biller C. Bourquin A. Ablasser M. Schlee S. Uematsu A. Noronha M. Manoharan S. Akira A. de Fougerolles S. Endres G. Hartmann Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7 Nat. Med. 2005 11 3 263 270
30. M. Sioud Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization J. Mol. Biol. 2005 348 1079 1090
31. A. D. Judge V. Sood J. R. Shaw D. Fang K. McClintock I. MacLachlan Sequence-dependentstimulation of the mammalian innate immune response by synthetic siRNA Nat. Biotechnol. 2005 23 457 462
32. M. Sioud Single-stranded small interfering RNA are more immunostimulatory than their double-stranded counterparts: A central role for 2′-hydroxyl uridines in immune responses Eur. J. Immunol. 2006 36 1222 1230
33. A. D. Judge G. Bola A. C. Lee I. MacLachlan Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo Mol. Ther. 2006 13 494 505
34. J. T. Margues T. Devosse D. Wang M. Zamanian-Daryoush P. Serbinowski R. Hartmann T. Fujita M. A. Behlke B. R. Willians A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells Nat. Biotechnol. 2006 24 559 565
35. D. Grimm K. L. Streetz C. L. Jopling T. A. Storm K. Pandey C. R. Davis P. Marion F. Salazar M. A. Kay Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways Nature 2006 441 537 541
36. D. S. Corey Chemical modification: the key to clinical application of RNA interference? J. Clin. Invest. 2007 117 3615 3622
37. 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. Pandev T. Racie et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs Nature 2004 432 173 178
38. J. M. Layzer A. P. McCaffrey A. K. Tanner Z. Huang M. A. Kay B. A. Sullenger In vivo activity of nuclease-resistant siRNA RNA 2004 10 766 771
39. S. Choung Y. J. Kim S. Kim H. O. Park Y. C. Choi Chemical modification of siRNAs to improve serum stability without loss of efficacy Biochem. Biophys. Res. Commun. 2006 342 919 927
40. C. R. Allerson N. Sioufi R. Jarres T. P. Prakash N. Naik A. Berdeja L. Wanders R. H. Griffey E. E. Swayze B. Bhat Fully 2′-modified oligonucleotide duplexes with improved in vitro potency and stability compared to unmodified small interfering RNA J. Med. Chem. 2005 48 901 904
41. J. Harborth S. M. Elbashir K. Vandenburgh H. Manninga S. A. Scaringe K. Weber T. Tuschl Sequence, chemical, and structural variation of small interfering RNAs and short hairpin RNAs and the effect on mammalian gene silencing Antisense Nucleic Acid Drug Dev. 2003 13 83 105
42. B. A. Kraynack B. F. Baker Small interfering RNAs containing full 2′-O-methylribonucleotide-modified sense strands display Argonaute2/eIF2C2-dependent activity RNA 2006 12 163 176
43. A. M. Krieg C. A. Stein Phosphorothioate oligodeoxynucleotides: antisense or anti-protein? Antisense Res. Dev. 1995 5 241
44. A. H. Hall J. Wan E. E. Shaughnessy B. Ramsay Shaw K. A. Alexander RNA interference using boranophosphate siRNAs: structure-activity relationships Nucleic Acids Res. 2004 32 5991 6000
45. T. P. Prakash C. R. Allerson P. Dande T. A. Vickers N. Sioufi R. Jarres B. F. Baker E. E. Swayze R. H. Griffey B. Bhat Positional effect of chemical modifications on short interference RNA activity in mammalian cells J. Med. Chem. 2005 48 4247 4253
46. J. Kurreck Antisense technologies. Improvement through novel chemicalmodifications Eur. J. Biochem. 2003 270 1628 1644
47. R. Juliano J. Bauman H. Kang X. Ming Biological barriers to therapy with antisense and siRNA oligonucleotides Mol. Pharmaceutics 2009 6 3 686 695
48. D. W. Pack A. S. Hoffman S. Pun P. S. Stayton Design and development of polymers for gene delivery Nat. Rev. Drug Discovery 2005 4 7 581 593
49. M. L. Edelstein M. R. Abedi J. Wixon R. M. Edelstein Gene therapy clinical trails worldwide 1989-2004-an overview J. Gene Med. 2004 6 6 597 602
50. M. L. Edelstein M. R. Abedi J. Wixon Gene therapy clinical trials worldwide to 2007-anupdate J. Gene Med. 2007 9 10 833 842
51. D. Bumcrot M. Manoharan V. Koteliansky D. W. Sah RNAi therapeutics: a potential new class of pharmaceutical drugs Nat. Chem. Biol. 2006 2 12 711 719
52. E. Lai J. H. van Zanten Monitoring DNA/poly-l-lysine polyplex formation with time-resolved multiangle laser light scattering Biophys. J. 2001 80 864 873
53. P. R. Dash M. L. Read L. B. Barrett M. A. Wolfert L. W. Seymour Factors affecting blood clearance and in vivo distribution of polyelectrolyte complexes for gene delivery Gene Ther. 1999 6 643 650
54. W. Li F. C. Szoka, Jr. Lipid-based nanoparticles for nucleic acid delivery Pharm. Res. 2007 24 3 438 449
55. A. Abuchowski J. R. McCoy N. C. Palczuk T. van Es F. F. Davis Effect of Covalent Attachment of Polyethylene-Glycol on Immunogenicity and Circulating Life of Bovine Liver Catalase J. Biol Chem 1977 252 11 3582 3586
56. A. Abuchowski T. van Es N. C. Palczuk F. F. Davis Alteration of Immunological Properties of Bovine Serum-Albumin by Covalent Attachment of Polyethylene-Glycol J. Biol. Chem. 1977 252 11 3578 3581
57. F. M. Veronses G. Pasut PEGylation, successful approach to drug delivery Drug Discovery Today 2005 10 1451 1458
58. M. Lee S. W. Kim Polyethylene glycol-conjugated copolymers for plasmid DNA delivery Pharm. Res. 2005 22 1 10
59. P. Bailon C. Y. Won PEG-modified biopharmaceuticals Expert Opin. Drug Delivery 2009 6 1 16
60. S. M. Ryan G. Mantovani X. Wang D. M. Haddleton D. J. Brayden Advances in PEGylation of important biotech molecules: delivery aspects Expert Opin. Drug Delivery 2008 5 371 383
61. S. Mishra P. Webster M. E. Davis PEGylation significantly affects cellular uptake and intracellular trafficking of non-viral gene delivery particles Eur. J. Cell Biol. 2004 83 97 111
62. T. Ishida H. Kiwada Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes Int. J. Pharm. 2008 354 1-2 56 62
63. K. F. Pirollo G. Zon A. Rait Q. Zhou W. Yu R. Hogrefe Chang E.H. Tumor-targeting nanoimmunoliposome complex for short interfering RNA delivery, Hum. Gene Ther. 2006 17 1 117 124
64. K. F. Pirollo A. Rait Q. Zhou S. H. Hwang J. A. Dagata G. Zon R. I. Hogrefe G. Palchik E. H. Chang Materializing the potential of small interfering RNA via a tumor-targeting nanodelivery system Cancer Res. 2007 67 7 2938 2943
65. D. M. Dykxhoorn J. Lieberman Running interference: prospects and obstacles to using small interfering RNAs as small molecule drugs Annu. Rev. Biomed. Eng. 2006 8 377 402
66. P. Oh P. Borgstrom H. Witkiewicz Y. Li B. J. Borgstrom A. Chrastina K. Iwata K. R. Zinn R. Baldwin J. E. Testa J. E. Schnitzer Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung Nat. Biotechnol. 2007 25 3 327 337
67. P. Kumar H. S. Ban S. S. Kim H. Wu T. Pearson D. L. Greiner A. Laouar J. Yao V. Haridas K. Habiro Y. G. Yang J. H. Jeong K. Y. Lee Y. H. Kim S. W. Kim, et al. T cell-specific siRNA delivery suppresses HIV-1 infection in humanized mice Cell 2008 134 4 577 586
68. D. Peer P. Zhu C. V. Carman J. Lieberman M. Shimaoka Selective gene silencing in activated leukocytes by targeting siRNAs to the integrin lymphocyte function-associated antigen-1 Proc. Natl. Acad. Sci. U. S. A. 2007 104 10 4095 4100
69. D. Peer E. J. Park Y. Morishita C. V. Carman M. Shimaoka Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target Science 2008 319 627 630
70. R. M. Schiffelers A. Ansari J. Xu Q. Zhou Q. Tang G. Storm G. Molema P. Y. Lu P. V. Scaria M. C. Woodle Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticles Nucleic Acids Res. 2004 32 19 e149
71. D. Hogemann-Savellano E. Bos C. Blondet F. Sato T. Abe L. Josephson R. Weissleder J. Gaudet D. Sgroi P. J. Peters J. P. Basilion The transferrin receptor: A potential molecular Imaging marker for human cancer Neoplasia 2003 5 6 495 506
72. D. Bartlett M. Davis Impact of tumor-specific targeting and dosing schedule on tumour growth inhibition after intravenous administration of siRNA-containing nanoparticles Biotechnol. Bioeng. 2008 99 4 975 985
73. Y. Zhang Y. F. Zhang J. Bryant A. Charles R. J. Boado W. M. Pardridge Intravenous RNA interference gene therapy targeting the human epidermal growth factor receptor prolongs survival in intracranial brain cancer Clin. Cancer Res. 2004 10 3667 3677
74. P. S. Low A. C. Antony Folate-receptor-targeted drugs for cancer and inflammatory diseases Adv. Drug Del. Rev. 2004 56 8 1055 1058
75. K. Zhang Q. Wang Y. Xie G. Mor E. Sega P. S. Low Y. Huang Receptor-mediated delivery of siRNAs by tethered nucleic acid base-paired interactions RNA 2008 14 3 577 583
76. P. S. Low S. A. Kularatne Folate-targeted therapeutic and imaging agents for cancer. Curr. Opin. Chem. Biol. 2009 13 3 256 262
77. R. Banerief P. Tyagi S. Li L. Huang Anisamide-targeted stealth liposomes: a potent carrier for targeting doxorubicin to human prostate cancer cells Int. J. Cancer 2004 112 693 700
78. S.-D. Li S. Chono L. Huang Efficient oncogene silencing and metastasis inhibition via systemic delivery of siRNA Mol. Ther. 2008 16 5 942 946
79. S.-D. Li S. Chono L. Huang Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles J. Controlled Release 2008 126 77 84
80. Y. Chen J. Sen S. R. Bathula Q. Yang R. Fittipaldi L. Huang Novel cationic lipid that delivers siRNA and enhances therapeutic effect in lung cancer cells Mol. Pharmaceutics 2009 6 3 696 705
81. A. Sato M. Takagi A. Shimamoto S. Kawakami M. Hashida Small interfering RNA delivery to the liver by intravenous administration of galactosylated cationic liposomes in mice Biomaterials 2007 28 7 1434 1442
82. T. Watanabe T. Umehara F. Yasui S. Nakagawa J. Yano T. Ohgi S. Sonoke K. Satoh K. Inoue M. Yoshiba M. Kohara Liver target delivery of small interfering RNA to the HCV gene by lactosylated cationic liposome J. Hepatol. 2007 47 744 750
83. K. A. Mislick J. D. Baldeschwieler Evidence for the role of proteoglycans in cation-mediated gene transfer Proc. Natl. Acad. Sci. U. S. A. 1996 93 22 12349 12354
84. P. Midoux G. Breuzard J. P. Gomez C. P. Pichon Polymer-based gene delivery: a current review on the uptake and intracellular trafficking of polyplexes Curr. Gene Ther. 2008 8 5 335 352
85. P. Erbacher A. C. Roche M. Monsigny P. Midoux Putative role of chloroquine in gene transfer into a human hepatoma cell line by DNA/lactosylated polylysine complexes Exp. Cell Res. 1996 225 186 194
86. X. Zhang G. J. Sawyer X. Dong Y. Qiu L. Collins J. W. Fabre The in vivo use of chloroquine to promote non-viral gene delivery to the liver via the portal vein and bile duct J. Gene Med. 2003 5 3 209 218
87. D. T. Curiel S. Agarwal E. Wagner M. Cotton Adenovirus enhancement of transferrin-polylysine-mediated gene delivery Proc. Natl. Acad. Sci. U. S. A. 1991 88 8850 8854
88. C. Plank B. Oberhauser K. Mechtler C. Koch E. Wagner The influence of endosome-disruptive peptides on gene transfer using synthetic virus-like gene transfer systems J. Biol. Chem. 1994 269 12918 12924
89. H. Lee J. H. Jeong T. G. Park A new gene delivery formulation of polyethylenimine/DNA complexes coated with PEG conjugated fusogenic peptide 2001 76 183 192
90. N. D. Sonawane F. C. Szoka, Jr. A. S. Verkman Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes J. Biol. Chem. 2003 278 45 44826 44831
91. P. Erbacher A. C. Roche M. Monsigny P. Midoux The reduction of the positive charges of polylysine by partial gluconoylation increases the transfection efficiency of polylysine/DNA complexes Biochim. Biophys. Acta, Biomembr. 1997 1324 27 36
92. M. G. Banaszczyk C. P. LollO D. Y. Kowh A. T. Phillips A. Amini D. P. Wu P. M. Mullen C. C. Coffin S. W. Brostoff D. J. Carlo Poly-l-lysine-graft-PEG- comb-type polycation copolymers for delivery J. Macromol. Sci., Part A: Pure Appl. Chem. 1999 36 1061 1084
93. D. V. Schaffer N. A. Fidelman N. Dan D. A. Lauffenburger Vector unpacking as a potential barrier for receptor-mediated polyplex gene delivery Biotechnol. Bioeng. 2000 67 598 606
94. S. Spagnou A. Miller M. Keller Lipidic carriers of siRNA: differences in the formulation, cellular uptake, and delivery with plasmid DNA Biochemistry 2004 43 13348 13356
95. K. Kostarelos A. D. Miller Synthetic, self-assembly ABCD nanoparticles; a structural paradigm for viable synthetic non-viral vectors Chem. Soc. Rev. 2005 34 11 970 994
96. M. J. Tolentino A. J. Brucker J. Fosnot G. S. Ying I. H. Wu G. Malik S. Wan S. J. Reich Intravitreal injection of vascular endothelial growth factor small interfering RNA inhibits growth and leakage in a nonhuman primate, laser-induced model of choroidal neovascularisation Retina 2004 24 132-138 & 660-661
97. 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 P. A. Campochiaro Suppression of ocular neovascularization with siRNA targeting VEGF receptor 1 Gene Ther. 2006 13 3 225 234
98. B. J. Li Q. Tang D. Cheng C. Qin F. Y. Xie Q. Wei J. Xu Y. Liu B. J. Zheng M. C. Woodle N. Zhong P. Y. Lu Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque Nature Med. 2005 11 944 951
99. Y. Sato T. Ajiki S. Inoue J. Fujishiro H. Yoshino Y. Igarashi Y. Hakamata T. Kaneko T. Murakamid E. Kobayashi Gene silencing in rat-liver and limb grafts by rapid injection of small interference RNA Transplantation 2005 79 2 240 243
100. H. Makimura T. M. Mizuno J. W. Mastaitis R. Agami C. V. Mobbs Reducing hypothalamic AGRP by RNA interference increases metabolic rate and decrease body weight without influencing food intake BMC Neurosci. 2002 3 18
101. D. R. Thakker F. Natt D. Husken R. Maier M. Muller H. van der Putten D. Hoyer J. F. Cryan Neurochemical and behavioral consequences of widespread gene knockdown in the adult mouse brain by using nonviral RNA interference Proc. Natl. Acad. Sci. U. S. A. 2004 101 49 17270 17275
102. S. E. Khorsandi P. Bachellier J. C. Weber M. Greget D. Jaeck D. Zacharoulis C. Rountas S. Helmy A. Helmy M. Al-Waracky H. Salama L. Jiao J. Nicholls A. J. Davies N. Leyicar, et al. Minimally invasive and selective hydrodynamic gene therapy of liver segments in the pig and human Cancer Gene Ther. 2008 15 4 225 230
103. D. R. Thakker F. Natt D. Husken H. van der Putten R. Maier D. Hoyer J. F. Cryan siRNA-mediated knockdown of the serotonin transporter in the adult mouse brain Mol. Psychiatry 2005 10 8 782 789
104. G. Dorn S. Patel G. Wotherspoon M. Hemmings-Mieszczak J. Barclay F. J. Natt P. Martin S. Bevan A. Fox P. Ganju W. Wishart J. Hall siRNA relieves chronic neuropathic pain Nucleic Acids Res. 2004 32 e49
105. V. Bitko A. Musiyenko O. Shulyayeva S. Barik Inhibition of respiratory viruses by nasally administered siRNA Nat. Med. 2005 11 50 55
106. S. Oliveira I. van Rooy O. Kranenburg G. Storm R. M. Schiffelers Fusogenic peptides enhance endosomal escape improving siRNA-induced silencing of oncogenes Int. J. Pharm. 2007 331 211 214
107. F. Simeoni M. C. Morris F. Heitz G. Divita Insight into the mechanism of the peptide-based gene delivery system MPG: implications for delivery of siRNA into mammalian cells Nucleic Acids Res. 2003 31 11 2717 2724
108. G. Cesarone O. P. Edupuganti C. P. Chen E. Wickstrom Insulin receptor substrate 1 knockdown in human MCF7 ER+ breast cancer cells by nuclease-resistant IRS1 siRNA conjugated to a disulfide-bridged D-peptide analogue of insulin-like growth factor 1 Bioconjugate Chem. 2007 18 1831 1840
109. T. C. Chu K. Y. Twu A. D. Ellington M. Levy Aptamer mediated siRNA delivery Nucleic Acids Res. 2006 34 10 e73
110. J. O. McNamara, 2nd E. R. Andrechek Y. Wang K. D. Viles R. E. Rempel E. Gilboa B. A. Sullenger P. H. Giangrande Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras Nat. Biotechnol. 2006 24 8 1005 1015
111. C. Wolfrum S. Shi K. N. Jayaprakash M. Jayaraman G. Wang R. K. Pandey K. G. Rajeev T. Nakayama K. Charrise E. M. Ndungo T. Zimmermann V. Kotelianshy M. Manoharan M. Stoffel Mechanisms and optimization of in vivo delivery of lipophilic siRNAs Nat. Biotechnol. 2007 25 10 1149 1157
112. P. Kumar H. Wu J. L. McBride K. F. Jung M. H. Kim B. L. Davidson S. K. Lee P. Shankar N. Manjunath Transvascular delivery of small interfering RNA to the central nervous system Nature 2007 448 39 45
113. M. Kortylewski P. Swiderski A. Herrmann L. Wang C. Kowolik M. Kujawski H. Lee A. Scuto Y. Liu C. Yang J. Deng H. S. Soifer A. Raubitschek S. Forman J. J. Rossi et al. In vivo delivery of siRNA to immune cells by conjugation to a TLR9 agonist enhances antitumor immune responses Nat. Biotechnol. 2009 27 10 925 932
114. S. H. Kim J. H. Jeong S. H. Lee S. W. Kim T. G. Park Local and systemic delivery of VEGF siRNA using polyelectrolyte complex micelles for effective treatment of cancer J. Controlled Release 2008 129 107 115
115. A. Akinc M. Goldberg J. Qin J. R. Dorkin C. Gamba-Vitalo M. Maier K. N. Jayaprakash M. Jayaraman K. G. Rajeev M. Manoharan V. Koteliansky I. Rohl E. S. Leshchiner R. Langer D. G. Anderson Development of lipidoid-siRNA formulations for systemic delivery to the liver Mol. Ther. 2009 17 5 872 879
116. J. Gu W. P. Cheng J. Liu S. Y. Lo D. Smith X. Qu Z. Yang pH-triggered reversible "stealth" polycationic micelles Biomacromolecules 2008 9 1 255 262
117. C. Ding J. Gu X. Qu Z. Yang Preparation of multifunctional drug carrier for tumor-specific uptake and enhanced intracellular delivery through the conjugation of weak acid labile linker Bioconjugate Chem. 2009 20 1163 1170
118. Y. Sato K. Murase J. Kato M. Kobune T. Sato Y. Kawano R. Takimoto K. Takada K. Miyanishi Matsunaga T. Takayama Y. Niitsu Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone Nat. Biotechnol. 2008 26 4 431 442
119. C. F. Xia Y. Zhang Y. Zhang R. J. Boado W. M. Pardridge Intravenous siRNA of brain cancer with receptor targeting and avidin-biotin technology Pharm. Res. 2007 24 12 2309 2316
120. M. Aouadi G. J. Tesz S. M. Nicoloro M. Wang M. Chouinard E. Soto G. R. Ostroff M. P. Czech Orally delivered siRNA targeting macrophage Map4k4 suppresses systemic inflammation Nature 2009 458 7242 1180 1184
121. 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 P. H. Giangrande Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors Nat. Biotechnol. 2009 27 9 839 849
122. S.-D. Li Y. C. Chen M. J. Hackett L. Huang Tumor-targeted Delivery of siRNA by Self-assembled Nanoparticles Mol. Ther. 2008 16 1 163 169
123. M. E. Davis M. E. Brewster Cyclodextrin-based pharmaceutics: past, present and future Nat. Rev. Drug Discovery 2004 3 12 1023 1035
124. S. Hu-Lieskovan J. D. Heidel D. W. Bartlett M. E. Davis T. J. Triche Sequence-specific knockdown of EWS-FLI1 by targeted, nonviral delivery of small interfering RNA inhibits tumor growth in a murine model of metastatic Ewing's sarcoma Cancer Res. 2005 65 19 8984 8992
125. M. E. Davis The first targeted delivery of siRNA in humans via a self-assembling, cyclodextrin polymer-based nanoparticle: from concept to clinic Mol. Pharmaceutics 2009 6 3 659 668
126. F. Sallas R. Darcy Amphiphilic cyclodextrins - advances in synthesis and supramolecular chemistry Eur. J. Org. Chem. 2008 957 969
127. S. A. Cryan R. Donohue B. J. Ravoo R. Darcy C. M. O'Driscoll Cationic cyclodextrin amphiphiles as gene delivery vectors J. Drug Del. Sci. Tech. 2004 14 1 57 62
128. S. A. Cryan A. Holohan R. Donohue R. Darcy C. M. O'Driscoll Cell transfection with polycationic cyclodextrin vectors Eur. J. Pharm. Sci. 2004 21 625 633
129. A. McMahon E. Gomez R. Donohue D. Forde R. Darcy C. M. O'Driscoll Cyclodextrin gene vectors: cell trafficking and the influence of lipophilic chain length J. Drug Deliv. Sci. Technol. 2008 18 303 307
130. C. M. O'Driscoll Delivery of siRNA: challenges and opportunities J. Pharm. Pharmacol. 2008 60 Supplement 1 A74
131. R. Donohue A. Mazzaglia B. J. Ravoo R. Darcy Cationic β-cyclodextrin bilayer vesicles Chem. Commun. 2002 2864 2865
132. A. R. de Fougerolles Delivery vehicles for small interfering RNA in vivo Hum. Gene Ther. 2008 19 2 125 132
133. S. A. Leachman R. P. Hickerson P. R. Hull F. J. Smith L. M. Milstone E. B. Lane S. J. Bale D. R. Roop W. H. McLean R. L. Kaspar Therapeutic siRNAs for dominant genetic skin disorders including pachyonychia congenita J. Dermatol. Sci. 2008 51 151 157
134. K. L. Talks H. Turley K. C. Gatter P. H. Maxwell C. W. Pugh P. J. Ratcliffe A. L. Harris The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages Am. J. Pathol. 2000 157 411 421
135. J. Zhou H. Li S. Li J. Zaia J. J. Rossi Novel dual inhibitory function aptamer-siRNA delivery system for HIV-1 therapy Mol. Ther. 2008 16 8 1481 1489
136. M. L. Read S. Singh Z. Ahmed M. Stevenson S. S. Briggs D. Oupicky L. B. Barrett R. Spice M. Kendall M. Berry J. A. Preece A. Logan L. W. Seymour A versatile reducible polycation-based system for efficient delivery of a broad range of nucleic acids Nucleic Acids Res. 2005 33 9 e86
137. C. Zhang N. Tang X. Liu W. Liang W. Xu V. P. Torchilin siRNA-containing liposomes modified with polyarginine effectively silence the targeted gene J. Controlled Release 2006 112 229 239
138. K. Yamato J. Fen H. Kobuchi Y. Nasu T. Yamada T. Nishihara Y. Ikeda M. Kizaki M. Yoshinouchi Induction of cell death in human papillomavirus 18-positive cervical cancer cells by E6 siRNA Cancer Gene Ther. 2006 13 234 241
139. W. M. Merritt Y. G. Lin W. A. Spannuth M. S. Fletcher A. A. Kamat L. Y. Han C. N. Landen N. Jennings K. De Geest R. R. Langley G. Villares A. Sanguino S. K. Lutgendorf G. Lopez-Berestein M. M. Bar-Eli A. K. Sood Effect of interleukin-8 gene silencing with liposome-encapsulated small interfering RNA on ovarian cancer cell growth J. Natl. Cancer Inst. 2008 100 5 359 372
140. S. Garcia A. Bodano J. L. Pablos J. J. Gomez-Reino C. Conde Poly(ADP-ribose) polymerase inhibition reduces tumor necrosis factor-induced inflammatory response in rheumatoid synovial fibroblasts Ann. Rheum. Dis. 2007 67 631 637
141. J. Hoelters M. Ciccarella M. Drechsel C. Geissler H. Gulkan W. Bocher M. Schieker M. Jochum P. Neth Nonviral genetic modification mediates effective transgene expression and functional RNA interference in human mesenchymal stem cells J. Gene Med. 2005 7 718 728
142. K. Habig M. Walter S. Poths O. Riess M. Bonin RNA interference of LRRK2-microarray expression analysis of a Parkinson's disease key player Neurogenetics 2008 9 83 94
143. L. J. Min M. Mogi J. M. Li J. Iwanami M. Iwai M. Horiuchi Aldosterone and angiotensin II synergistically induce mitogenic response in vascular smooth muscle cells Circ. Res. 2005 97 434 442
144. V. Dolcini J. Dunys J. Sevalle F. Chen M. V. Guillot-Sestier P. St George-Hyslop P. E. Fraser F. Checler TMP21 regulates Abeta production but does not affect caspase-3, p53, and neprilysin Biochem. Biophys. Res. Commun. 2008 371 69 74
145. L. Gitlin S. Karelsky R. Andino Short interfering RNA confers intracellular antiviral immunity in human cells Nature 2002 418 430 434
146. A. M. Derfus A. A. Chen D. H. Min E. Ruoslahti S. N. Bhatia Targeted quantum dot conjugates for siRNA delivery Bioconjugate Chem. 2007 18 1391 1396
147. K. A. Howard U. L. Rahbek X. Liu C. K. Damgaard S. Z. Glud M. Ø. Andersen M. B. Hovgaard A. Schmitz J. R. Nyengaard F. Besenbacher J. Kjems RNA interference in vitro and in vivo using a novel chitosan/siRNA nanoparticle system Mol. Ther. 2006 14 4 476 484
148. R. Krajcik A. Jung A. Hirsch W. Neuhuber O. Zolk Functionalization of carbon nanotubes enables non-covalent binding and intracellular delivery of small interfering RNA for efficient knock-down of genes Biochem. Biophys. Res. Commun. 2008 369 595 602
149. S. H. Lee S. H. Choi S. H. Kim T. G. Park Thermally sensitive cationic polymer nanocapsules for specific cytosolic delivery and efficient gene silencing of siRNA: swelling induced physical disruption of endosome by cold shock J. Controlled Release 2008 125 25 32
150. A. Khaled S. Guo F. Li P. Guo Controllable self-assembly of nanoparticles for specific delivery of multiple therapeutic molecules to cancer cells using RNA nanotechnology Nano Lett. 2005 5 9 1797 1808
151. D. Bartlett M. E. Davis Physicochemical and biological characterization of targeted nucleic, acid-containing nanoparticles Bioconjugate Chem. 2007 18 456 468
152. D. Sutton S. Kim X. Shuai K. Leskoy J. T. Marques B. R. Williams D. A. Boothman J. Gao Efficient suppression of secretory clusterin levels by polymer-siRNA nanocomplexes enhances ionizing radiation lethality in human MCF-7 breast cancer cells in vitro Int. J. Nanomed. 2006 1 2 155 162
153. Y. Y. Wang X. Deng L. Xu F. Gao T. Flagg W. S. May Bcl2 enhances induced hematopoietic differentiation of murine embryonic stem cells Exp. Hematol. 2008 36 2 128 139
154. D. Massaro G. D. Massaro L. B. Clerch Noninvasive delivery of small inhibitory RNA and other reagents to pulmonary alveoli in mice Am. J. Physiol.: Lung Cell. Mol. Phys. 2004 287 L1066 1070
155. J. E. Hagstrom J. Hegge G. Zhang M. Noble V. Budker D. L. Lewis H. Herweijer J. A. Wolff A facile nonviral method for delivering genes and siRNAs to skeletal muscle of mammalian limbs Mol. Ther. 2004 10 2 386 398
156. F. Takeshita Y. Minakuchi S. Nagahara K. Honma H. Sasaki K. Hirai T. Teratani N. Namatame Y. Yamamoto K. Hanai T. Kato A. Sano T. Ochiya Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo Proc. Natl. Acad. Sci. U. S. A. 2005 102 34 12177 12182
157. L. N. Johnson S. M. Cashman R. Kumar-Singh Cell-penetrating peptide for enhanced delivery of nucleic acids and drugs to ocular tissues including retina and cornea Mol. Ther. 2008 16 1 107 114
158. J. Halder A. A. Kamat C. N. Lander, Jr. L. Y. Han S. K. Lutgendorf Y. G. Lin W. M. Merritt N. B. Jennings A. Chavez-Reyes R. L. Coleman D. M. Gershenson R. Schmandt S. W. Cole G. Lopez-Berestein A. K. Sood Focal adhesion kinase targeting using in vivo short interfering RNA delivery in neutral liposomes for ovarian carcinoma therapy Clin. Cancer Res. 2006 12 16 4916 4924
159. T. Yokota S. Iijima T. Kubodera K. Ishii Y. Katakai N. Ageyama Y. Chen Y. J. Lee T. Unno K. Nishina Y. Iwasaki N. Maki H. Mizusawa H. Akari Efficient regulation of viral replication by siRNA in a non-human primate surrogate model for hepatitis C Biochem. Biophys. Res. Commun. 2007 361 294 300
160. M. Nogawa T. Yuasa S. Kimura M. Tanaka J. Kuroda K. Sato A. Yokota H. Segawa Y. Toda S. Kageyama T. Yoshiki Y. Okada T. Maekawa Intravesical
161. M. Khoury P. Louis-Plence V. Escriou D. Noel C. Largeau C. Cantos D. Scherman C. Jorgensen F. Apparailly Efficient new cationic liposome formulation for systemic delivery of small interfering RNA silencing tumor necrosis factor alpha in experimental arthritis Arthritis Rheum. 2006 54 6 1867 1877
162. K. Futami E. Kumagai H. Makino A. Sato M. Takagi A. Shimamoto Y. Furuichi Anticancer activity of RecQL1 helicase siRNA in mouse xenograft models Cancer Sci. 2008 99 6 1227 1236
163. Y. Zhang P. Cristofaro R. Silbermann O. Pusch D. Boden T. Konkin V. Hovanesian P. R. Monfils M. Resnick S. F. Moss B. Ramratnam Engineering mucosal RNA interference in vivo Mol. Ther. 2006 14 3 336 343
164. A. Khan M. Benboubetra P. Z. Syyed K. W. Ng S. Fox G. Beck I. F. Benter S. Akhtar Sustained polymeric delivery of gene silencing antisense ONDs, siRNA, DNAzymes and ribozymes: in vitro and in vivo studies J. Drug Targeting 2004 12 6 393 404
165. N. Murata Y. Takashima K. Toyoshima M. Yamamoto H. Okada Antitumor effects of anti-VEGF siRNA encapsulated with PLGA microspheres in mice J. Controlled Release 2008 126 246 254
166. J. Elmén H. Thonberg K. Ljungberg M. Frieden M. Westergaard Y. Xu B. Wahren Z. Liang H. Ørum T. Koch C. Wahlestedt Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality 2005 33 1 439 47
167. R. N. Veedu J. Wengel Locked nucleic acid nucleoside triphosphates and polymerases: on the way towards evolution of LNA aptamers Mol. BioSyst. 2009 5 8 787 92
168. D. R. Thakker D. Hoyer J. F. Cryan Interfering with the brain: use of RNA interference for understanding the pathophysiology of psychiatric and neurological disorders Pharmacol. Ther. 2006 109 413 38
169. 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, et al. Rational design of cationic lipids for siRNA delivery Nat. Biotechnol. 2010 28 2 172 178