Chemical and structural modifications of RNAi therapeutics

Advanced Drug Delivery Reviews

Volumn 104, Issue , 2016, Pages 16-28

  Ku, Sook Hee ^a   Jo, Sung Duk ^a   Lee, Yeon Kyung ^a   Kim, Kwangmeyung ^a   Kim, Sun Hwa ^a  

^a Korea Institute of Science and Technology   (South Korea)

Author keywords

Chemical modification; RNA interference; siRNA; siRNA delivery; Structural modification

Indexed keywords

GENES; GENETIC ENGINEERING; NUCLEIC ACIDS; PLANTS (BOTANY); RNA;

INTRACELLULAR DELIVERY; POST-TRANSCRIPTIONAL GENE SILENCING; RNA INTERFERENCE; SEQUENCE-SPECIFIC MANNER; SIRNA; SIRNA DELIVERY; SMALL INTERFERING RNA (SIRNA); STRUCTURAL MODIFICATIONS;

CHEMICAL MODIFICATION;

APTAMER; HYALURONIC ACID; MACROGOL; NANOPARTICLE; POLYETHYLENEIMINE; POLYMER; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; CHEMICAL MODIFICATION; DRUG CLEARANCE; DRUG DEGRADATION; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG HALF LIFE; DRUG POTENCY; DRUG STRUCTURE; DRUG TARGETING; GENE SILENCING; HUMAN; HYDROGEL; NONHUMAN; POLYMERIZATION; REVIEW; RNA INTERFERENCE; ANIMAL; RNAI THERAPEUTICS;

ANIMALS; HUMANS; NANOPARTICLES; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNAI THERAPEUTICS;

EID: 84957687437     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2015.10.015     Document Type: Review

References (115)

1. [1] Dykxhoorn, D.M., Novina, C.D., Sharp, P.A., Killing the messenger: short RNAs that silence gene expression. Nat. Rev. Mol. Cell Biol. 4 (2003), 457–467.
2. [2] Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., Mello, C.C., Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998), 806–811.
3. [3] Hannon, G.J., RNA interference. Nature 418 (2002), 244–251.
4. [4] de Fougerolles, A., Vornlocher, H.-P., Maraganore, J., Lieberman, J., Interfering with disease: a progress report on siRNA-based therapeutics. Nat. Rev. Drug Discov. 6 (2007), 443–453.
5. [5] Dykxhoorn, D.M., Palliser, D., Lieberman, J., The silent treatment: siRNAs as small molecule drugs. Gene Ther. 13 (2006), 541–552.
6. [6] Pecot, C.V., Calin, G.A., Coleman, R.L., Lopez-Berestein, G., Sood, A.K., RNA interference in the clinic: challenges and future directions. Nat. Rev. Cancer 11 (2011), 59–67.
7. [7] Wang, J., Lu, Z., Wientjes, M.G., Au, J.S., Delivery of siRNA therapeutics: barriers and carriers. AAPS J. 12 (2010), 492–503.
8. [8] Whitehead, K.A., Langer, R., Anderson, D.G., Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 8 (2009), 129–138.
9. [9] Ku, S.H., Kim, K., Choi, K., Kim, S.H., Kwon, I.C., Tumor-targeting multifunctional nanoparticles for siRNA delivery: recent advances in cancer therapy. Adv. Healthcare Mater. 3 (2014), 1182–1193.
10. [10] Kanasty, R., Dorkin, J.R., Vegas, A., Anderson, D., Delivery materials for siRNA therapeutics. Nat. Mater. 12 (2013), 967–977.
11. [11] Turner, J.J., Jones, S.W., Moschos, S.A., Lindsay, M.A., Gait, M.J., MALDI-TOF mass spectral analysis of siRNA degradation in serum confirms an RNAse A-like activity. Mol. BioSyst. 3 (2007), 43–50.
12. [12] Haupenthal, J., Baehr, C., Kiermayer, S., Zeuzem, S., Piiper, A., Inhibition of RNAse A family enzymes prevents degradation and loss of silencing activity of siRNAs in serum. Biochem. Pharmacol. 71 (2006), 702–710.
13. [13] Kennedy, S., Wang, D., Ruvkun, G., A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427 (2004), 645–649.
14. [14] Takabatake, Y., Isaka, Y., Mizui, M., Kawachi, H., Takahara, S., Imai, E., Chemically modified siRNA prolonged RNA interference in renal disease. Biochem. Biophys. Res. Commun. 363 (2007), 432–437.
15. [15] Lai, E.C., Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30 (2002), 363–364.
16. [16] Birmingham, A., Anderson, E.M., Reynolds, A., Ilsley-Tyree, D., Leake, D., Fedorov, Y., Baskerville, S., Maksimova, E., Robinson, K., Karpilow, J., Marshall, W.S., Khvorova, A., 3′-UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Methods 3 (2006), 199–204.
17. [17] Jackson, A.L., Burchard, J., Schelter, J., Chau, B.N., Cleary, M., Lim, L., Linsley, P.S., Widespread siRNA “off-target” transcript silencing mediated by seed region sequence complementarity. RNA 12 (2006), 1179–1187.
18. [18] Wei, J.-X., Yang, J., Sun, J.-F., Jia, L.-T., Zhang, Y., Zhang, H.-Z., Li, X., Meng, Y.-L., Yao, L.-B., Yang, A.-G., Both strands of siRNA have potential to guide posttranscriptional gene silencing in mammalian cells. PLoS One, 4, 2009, e5382.
19. [19] Kleinman, M.E., Yamada, K., Takeda, A., Chandrasekaran, V., Nozaki, M., Baffi, J.Z., Albuquerque, R.J.C., Yamasaki, S., Itaya, M., Pan, Y., Appukuttan, B., Gibbs, D., Yang, Z., Kariko, K., Ambati, B.K., Wilgus, T.A., DiPietro, L.A., Sakurai, E., Zhang, K., Smith, J.R., Taylor, E.W., Ambati, J., Sequence- and target-independent angiogenesis suppression by siRNA via TLR3. Nature 452 (2008), 591–597.
20. [20] Reynolds, A., Anderson, E.M., Vermeulen, A., Fedorov, Y., Robinson, K., Leake, D., Karpilow, J., Marshall, W.S., Khvorova, A., Induction of the interferon response by siRNA is cell type- and duplex length-dependent. RNA 12 (2006), 988–993.
21. [21] Judge, A.D., Sood, V., Shaw, J.R., Fang, D., McClintock, K., MacLachlan, I., Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23 (2005), 457–462.
22. [22] Forsbach, A., Nemorin, J.-G., Montino, C., Müller, C., Samulowitz, U., Vicari, A.P., Jurk, M., Mutwiri, G.K., Krieg, A.M., Lipford, G.B., Vollmer, J., Identification of RNA sequence motifs stimulating sequence-specific TLR8-dependent immune responses. J. Immunol. 180 (2008), 3729–3738.
23. [23] Manche, L., Green, S.R., Schmedt, C., Mathews, M.B., Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol. Cell. Biol. 12 (1992), 5238–5248.
24. [24] Hornung, V., Ellegast, J., Kim, S., Brzózka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K.-K., Schlee, M., Endres, S., Hartmann, G., 5′-Triphosphate RNA is the ligand for RIG-I. Science 314 (2006), 994–997.
25. [25] Marques, J.T., Devosse, T., Wang, D., Zamanian-Daryoush, M., Serbinowski, P., Hartmann, R., Fujita, T., Behlke, M.A., Williams, B.R.G., A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat. Biotechnol. 24 (2006), 559–565.
26. [26] Juliano, R., Bauman, J., Kang, H., Ming, X., Biological barriers to therapy with antisense and siRNA oligonucleotides. Mol. Pharm. 6 (2009), 686–695.
27. [27] Fang, J., Nakamura, H., Maeda, H., The EPR effect: Unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 63 (2011), 136–151.
28. [28] Vivès, E., Schmidt, J., Pèlegrin, A., Cell-penetrating and cell-targeting peptides in drug delivery. Biochim. Biophys. Acta 1786 (2008), 126–138.
29. [29] Gary, D.J., Puri, N., Won, Y.-Y., Polymer-based siRNA delivery: Perspectives on the fundamental and phenomenological distinctions from polymer-based DNA delivery. J. Control. Release 121 (2007), 64–73.
30. [30] Bramsen, J.B., Kjems, J., Development of therapeutic-grade small interfering RNAs by chemical engineering. Front. Genet., 3, 2012, 154.
31. [31] Jeong, J.H., Mok, H., Oh, Y.-K., Park, T.G., siRNA conjugate delivery systems. Bioconjug. Chem. 20 (2009), 5–14.
32. [32] Agrawal, S., Temsamani, J., Tang, J.Y., Pharmacokinetics, biodistribution, and stability of oligodeoxynucleotide phosphorothioates in mice. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 7595–7599.
33. [33] Braasch, D.A., Paroo, Z., Constantinescu, A., Ren, G., Öz, O.K., Mason, R.P., Corey, D.R., Biodistribution of phosphodiester and phosphorothioate siRNA. Bioorg. Med. Chem. Lett. 14 (2004), 1139–1143.
34. [34] Li, Z.-Y., Mao, H., Kallick, D.A., Gorenstein, D.G., The effects of thiophosphate substitutions on native siRNA gene silencing. Biochem. Biophys. Res. Commun. 329 (2005), 1026–1030.
35. [35] Harborth, J., Elbashir, S.M., Vandenburgh, K., Manninga, H., Scaringe, S.A., Weber, K., Tuschl, T., 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. 13 (2003), 83–105.
36. [36] Yang, X., Sierant, M., Janicka, M., Peczek, L., Martinez, C., Hassell, T., Li, N., Li, X., Wang, T., Nawrot, B., Gene silencing activity of siRNA molecules containing phosphorodithioate substitutions. ACS Chem. Biol. 7 (2012), 1214–1220.
37. [37] Li, P., Sergueeva, Z.A., Dobrikov, M., Shaw, B.R., Nucleoside and oligonucleoside boranophosphates: chemistry and properties. Chem. Rev. 107 (2007), 4746–4796.
38. [38] Hall, A.H.S., Wan, J., Shaughnessy, E.E., Ramsay Shaw, B., Alexander, K.A., RNA interference using boranophosphate siRNAs: structure–activity relationships. Nucleic Acids Res. 32 (2004), 5991–6000.
39. [39] Chiu, Y.-L., Rana, T.M., siRNA function in RNAi: A chemical modification analysis. RNA 9 (2003), 1034–1048.
40. [40] Choung, S., Kim, Y.J., Kim, S., Park, H.-O., Choi, Y.-C., Chemical modification of siRNAs to improve serum stability without loss of efficacy. Biochem. Biophys. Res. Commun. 342 (2006), 919–927.
41. [41] Kraynack, B.A., Baker, B.F., Small interfering RNAs containing full 2′-O-methylribonucleotide-modified sense strands display Argonaute2/eIF2C2-dependent activity. RNA 12 (2006), 163–176.
42. [42] Braasch, D.A., Jensen, S., Liu, Y., Kaur, K., Arar, K., White, M.A., Corey, D.R., RNA interference in mammalian cells by chemically-modified RNA. Biochemistry 42 (2003), 7967–7975.
43. [43] Layzer, J.M., McCaffrey, A.P., Tanner, A.K., Huang, Z., Kay, M.A., Sullenger, B.A., In vivo activity of nuclease-resistant siRNAs. RNA 10 (2004), 766–771.
44. [44] Allerson, C.R., Sioufi, N., Jarres, R., Prakash, T.P., Naik, N., Berdeja, A., Wanders, L., Griffey, R.H., Swayze, E.E., Bhat, B., Fully 2′-modified oligonucleotide duplexes with improved in vitro potency and stability compared to unmodified small interfering RNA. J. Med. Chem. 48 (2005), 901–904.
45. [45] Hogrefe, R.I., Lebedev, A.V., Zon, G., Pirollo, K.F., Rait, A., Zhou, Q., Yu, W., Chang, E.H., Chemically Modified Short Interfering Hybrids (siHYBRIDS): Nanoimmunoliposome Delivery In Vitro and In Vivo for RNAi of HER-2, Nucleosides. Nucleosides Nucleotides Nucleic Acids 25 (2006), 889–907.
46. [46] 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. 67 (2007), 2938–2943.
47. [47] Petersen, M., Wengel, J., LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol. 21 (2003), 74–81.
48. [48] Elmén, J., Thonberg, H., Ljungberg, K., Frieden, M., Westergaard, M., Xu, Y., Wahren, B., Liang, Z., Ørum, H., Koch, T., Wahlestedt, C., Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality. Nucleic Acids Res. 33 (2005), 439–447.
49. [49] Volkov, A.A., Kruglova, N.Y.S., Meschaninova, M.I., Venyaminova, A.G., Zenkova, M.A., Vlassov, V.V., Chernolovskaya, E.L., Selective protection of nuclease-sensitive sites in siRNA prolongs silencing effect. Oligonucleotides 19 (2009), 191–202.
50. [50] Morrissey, D.V., Blanchard, K., Shaw, L., Jensen, K., Lockridge, J.A., Dickinson, B., McSwiggen, J.A., Vargeese, C., Bowman, K., Shaffer, C.S., Polisky, B.A., Zinnen, S., Activity of stabilized short interfering RNA in a mouse model of hepatitis B virus replication. Hepatology 41 (2005), 1349–1356.
51. [51] Jackson, A.L., Burchard, J., Leake, D., Reynolds, A., Schelter, J., Guo, J., Johnson, J.M., Lim, L., Karpilow, J., Nichols, K., Marshall, W., Khvorova, A., Linsley, P.S., Position-specific chemical modification of siRNAs reduces “off-target” transcript silencing. RNA 12 (2006), 1197–1205.
52. [52] Ui-Tei, K., Naito, Y., Zenno, S., Nishi, K., Yamato, K., Takahashi, F., Juni, A., Saigo, K., Functional dissection of siRNA sequence by systematic DNA substitution: modified siRNA with a DNA seed arm is a powerful tool for mammalian gene silencing with significantly reduced off-target effect. Nucleic Acids Res. 36 (2008), 2136–2151.
53. [53] Nykänen, A., Haley, B., Zamore, P.D., ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107 (2001), 309–321.
54. [54] Chen, P.Y., Weinmann, L., Gaidatzis, D., Pei, Y., Zavolan, M., Tuschl, T., Meister, G., Strand-specific 5′-O-methylation of siRNA duplexes controls guide strand selection and targeting specificity. RNA 14 (2008), 263–274.
55. [55] Mook, O.R., Baas, F., de Wissel, M.B., Fluiter, K., Evaluation of locked nucleic acid–modified small interfering RNA in vitro and in vivo. Mol. Cancer Ther. 6 (2007), 833–843.
56. [56] Eberle, F., Gießler, K., Deck, C., Heeg, K., Peter, M., Richert, C., Dalpke, A.H., Modifications in small interfering RNA that separate immunostimulation from RNA interference. J. Immunol. 180 (2008), 3229–3237.
57. [57] Hamm, S., Latz, E., Hangel, D., Müller, T., Yu, P., Golenbock, D., Sparwasser, T., Wagner, H., Bauer, S., Alternating 2′-O-ribose methylation is a universal approach for generating non-stimulatory siRNA by acting as TLR7 antagonist. Immunobiology 215 (2010), 559–569.
58. [58] Hornung, V., Guenthner-Biller, M., Bourquin, C., Ablasser, A., Schlee, M., Uematsu, S., Noronha, A., Manoharan, M., Akira, S., de Fougerolles, A., Endres, S., Hartmann, G., Sequence-specific potent induction of IFN-α by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 11 (2005), 263–270.
59. [59] Nallagatla, S.R., Bevilacqua, P.C., Nucleoside modifications modulate activation of the protein kinase PKR in an RNA structure-specific manner. RNA 14 (2008), 1201–1213.
60. [60] Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., Tuschl, T., Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 (2001), 494–498.
61. [61] Elbashir, S.M., Lendeckel, W., Tuschl, T., RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev. 15 (2001), 188–200.
62. [62] Kim, D.H., Behlke, M.A., Rose, S.D., Chang, M.S., Choi, S., Rossi, J.J., Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy. Nat. Biotechnol. 23 (2005), 222–226.
63. [63] Siolas, D., Lerner, C., Burchard, J., Ge, W., Linsley, P.S., Paddison, P.J., Hannon, G.J., Cleary, M.A., Synthetic shRNAs as potent RNAi triggers. Nat. Biotechnol. 23 (2005), 227–231.
64. [64] Lee, Y.S., Nakahara, K., Pham, J.W., Kim, K., He, Z.Y., Sontheimer, E.J., Carthew, R.W., Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117 (2004), 69–81.
65. [65] Sontheimer, E.J., Assembly and function of RNA silencing complexes. Nat. Rev. Mol. Cell Biol. 6 (2005), 127–138.
66. [66] Bitko, V., Musiyenko, A., Shulyayeva, O., Barik, S., Inhibition of respiratory viruses by nasally administered siRNA. Nat. Med. 11 (2005), 50–55.
67. [67] Persengiev, S.P., Zhu, X.C., Green, M.R., Nonspecific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA Biol. 10 (2004), 12–18.
68. [68] Jackson, A.L., Linsley, P.S., Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat. Rev. Drug Discov. 9 (2010), 57–67.
69. [69] Sun, X.G., Rogoff, H.A., Li, C.J., Asymmetric RNA duplexes mediate RNA interference in mammalian cells. Nat. Biotechnol. 26 (2008), 1379–1382.
70. [70] Bramsen, J.B., Laursen, M.B., Damgaard, C.K., Lena, S.W., Babu, B.R., Wengel, J., Kjems, J., Improved silencing properties using small internally segmented interfering RNAs. Nucleic Acids Res. 35 (2007), 5886–5897.
71. [71] Hohjoh, H., Enhancement of RNAi activity by improved siRNA duplexes. FEBS Lett. 557 (2004), 193–198.
72. [72] Khvorova, A., Reynolds, A., Jayasena, S.D., Functional siRNAs and rniRNAs exhibit strand bias. Cell 115 (2003), 209–216.
73. [73] Schwarz, D.S., Hutvagner, G., Du, T., Xu, Z.S., Aronin, N., Zamore, P.D., Asymmetry in the assembly of the RNAi enzyme complex. Cell 115 (2003), 199–208.
74. [74] Jackson, A.L., Burchard, J., Leake, D., Reynolds, A., Schelter, J., Guo, J., Johnson, J.M., Lim, L., Karpilow, J., Nichols, K., Marshall, W., Khvorova, A., Linsley, P.S., Position-specific chemical modification of siRNAs reduces “off-target” transcript silencing. Rna-a Publ. Rna Soc. 12 (2006), 1197–1205.
75. [75] Manoharan, M., RNA interference and chemically modified small interfering RNAs. Curr. Opin. Chem. Biol. 8 (2004), 570–579.
76. [76] Abe, N., Abe, H., Ito, Y., Dumbbell-shaped nanocircular RNAs for RNA interference. J. Am. Chem. Soc. 129 (2007), 15108–15109.
77. [77] Raouane, M., Desmaële, D., Urbinati, G., Massaad-Massade, L., Couvreur, P., Lipid conjugated oligonucleotides: a useful strategy for delivery. Bioconjug. Chem. 23 (2012), 1091–1104.
78. [78] Soutschek, J., Akinc, A., Bramlage, B., Charisse, K., Constien, R., Donoghue, M., Elbashir, S., Geick, A., Hadwiger, P., Harborth, J., John, M., Kesavan, V., Lavine, G., Pandey, R.K., Racie, T., Rajeev, K.G., Rohl, I., Toudjarska, I., Wang, G., Wuschko, S., Bumcrot, D., Koteliansky, V., Limmer, S., Manoharan, M., Vornlocher, H.-P., Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 432 (2004), 173–178.
79. [79] Wolfrum, C., Shi, S., Jayaprakash, K.N., Jayaraman, M., Wang, G., Pandey, R.K., Rajeev, K.G., Nakayama, T., Charrise, K., Ndungo, E.M., Zimmermann, T., Koteliansky, V., Manoharan, M., Stoffel, M., Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat. Biotechnol. 25 (2007), 1149–1157.
80. [80] Nishina, K., Unno, T., Uno, Y., Kubodera, T., Kanouchi, T., Mizusawa, H., Yokota, T., Efficient in vivo delivery of siRNA to the liver by conjugation of a-tocopherol. Mol. Ther. 16 (2008), 734–740.
81. [81] Iversen, F., Yang, C., Dagnæs-Hansen, F., Schaffert, D.H., Kjems, J., Gao, S., Optimized siRNA-PEG conjugates for extended blood circulation and reduced urine excretion in mice. Theranostics 3 (2013), 201–209.
82. [82] Kim, S.H., Jeong, J.H., Lee, S.H., Kim, S.W., Park, T.G., PEG conjugated VEGF siRNA for anti-angiogenic gene therapy. J. Control. Release 116 (2006), 123–129.
83. [83] Kim, S.H., Jeong, J.H., Lee, S.H., Kim, S.W., Park, T.G., Local and systemic delivery of VEGF siRNA using polyelectrolyte complex micelles for effective treatment of cancer. J. Control. Release 129 (2008), 107–116.
84. [84] Oishi, M., Nagasaki, Y., Itaka, K., Nishiyama, N., Kataoka, K., Lactosylated poly(ethylene glycol)-siRNA conjugate through acid-labile β-thiopropionate linkage to construct pH-sensitive polyion complex micelles achieving enhanced gene silencing in hepatoma cells. J. Am. Chem. Soc. 127 (2005), 1624–1625.
85. [85] Dohmen, C., Frohlich, T., Lachelt, U., Rohl, I., Vornlocher, H.-P., Hadwiger, P., Wagner, E., Defined folate-PEG-siRNA conjugates for receptor-specific gene silencing. Mol. Ther.–Nucleic Acids, 1, 2012, e7.
86. [86] Jang, Y.L., Ku, S.H., Lee, S.J., Park, J.H., Kim, W.J., Kwon, I.C., Kim, S.H., Jeong, J.H., Hyaluronic acid-siRNA conjugate/reducible polyethylenimine complexes for targeted siRNA delivery. J. Nanosci. Nanotechnol. 14 (2014), 7388–7394.
87. [87] Park, K., Yang, J.-A., Lee, M.-Y., Lee, H., Hahn, S.K., Reducible hyaluronic acid–siRNA conjugate for target specific gene silencing. Bioconjug. Chem. 24 (2013), 1201–1209.
88. [88] Dassie, J.P., Liu, X.-y., Thomas, G.S., Whitaker, R.M., Thiel, K.W., Stockdale, K.R., Meyerholz, D.K., McCaffrey, A.P., McNamara Ii, J.O., Giangrande, P.H., Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat. Biotechnol. 27 (2009), 839–846.
89. [89] McNamara, J.O., Andrechek, E.R., Wang, Y., Viles, K.D., Rempel, R.E., Gilboa, E., Sullenger, B.A., Giangrande, P.H., Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat. Biotechnol. 24 (2006), 1005–1015.
90. [90] Lai, W.-Y., Wang, W.-Y., Chang, Y.-C., Chang, C.-J., Yang, P.-C., Peck, K., Synergistic inhibition of lung cancer cell invasion, tumor growth and angiogenesis using aptamer-siRNA chimeras. Biomaterials 35 (2014), 2905–2914.
91. [91] Whitehead, K.A., Langer, R., Anderson, D.G., Knocking down barriers: advances in siRNA delivery (vol 8, pg 129, 2009). Nat. Rev. Drug Discov., 9, 2010, 412-412.
92. [92] Akita, H., Harashima, H., Advances in non-viral gene delivery: using multifunctional envelope-type nano-device. Expert Opin. Drug Deliv. 5 (2008), 847–859.
93. [93] Kebbekus, P., Draper, D.E., Hagerman, P., Persistence length of Rna. Biochemistry 34 (1995), 4354–4357.
94. [94] Bartlett, D.W., Su, H., Hildebrandt, I.J., Weber, W.A., Davis, M.E., Impact of tumor-specific targeting on the biodistribution and efficacy of siRNA nanoparticles measured by multimodality in vivo imaging. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 15549–15554.
95. [95] Mok, H., Park, T.G., Self-crosslinked and reducible fusogenic peptides for intracellular delivery of siRNA. Biopolymers 89 (2008), 881–888.
96. [96] Lv, H.T., Zhang, S.B., Wang, B., Cui, S.H., Yan, J., Toxicity of cationic lipids and cationic polymers in gene delivery. J. Control. Release 114 (2006), 100–109.
97. [97] Bolcato-Bellemin, A.L., Bonnet, M.E., Creusatt, G., Erbacher, P., Behr, J.P., Sticky overhangs enhance siRNA-mediated gene silencing. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 16050–16055.
98. [98] Mok, H., Lee, S.H., Park, J.W., Park, T.G., Multimeric small interfering ribonucleic acid for highly efficient sequence-specific gene silencing. Nat. Mater. 9 (2010), 272–278.
99. [99] Lee, S.Y., Huh, M.S., Lee, S., Lee, S.J., Chung, H., Park, J.H., Oh, Y.K., Choi, K., Kim, K., Kwon, I.C., Stability and cellular uptake of polymerized siRNA (poly-siRNA)/polyethylenimine (PEI) complexes for efficient gene silencing. J. Control. Release 141 (2010), 339–346.
100. [100] Meng, F.H., Hennink, W.E., Zhong, Z., Reduction-sensitive polymers and bioconjugates for biomedical applications. Biomaterials 30 (2009), 2180–2198.
101. [101] Sioud, M., RNA interference and innate immunity. Adv. Drug Deliv. Rev. 59 (2007), 153–163.
102. [102] Rothemund, P.W.K., Folding DNA to create nanoscale shapes and patterns. Nature 440 (2006), 297–302.
103. [103] Pinheiro, A.V., Han, D.R., Shih, W.M., Yan, H., Challenges and opportunities for structural DNA nanotechnology. Nat. Nanotechnol. 6 (2011), 763–772.
104. [104] Hong, C.A., Lee, S.H., Kim, J.S., Park, J.W., Bae, K.H., Mok, H., Park, T.G., Lee, H., Gene silencing by siRNA microhydrogels via polymeric nanoscale condensation. J. Am. Chem. Soc. 133 (2011), 13914–13917.
105. [105] Lee, J.B., Hong, J., Bonner, D.K., Poon, Z., Hammond, P.T., Self-assembled RNA interference microsponges for efficient siRNA delivery. Nat. Mater. 11 (2012), 316–322.
106. [106] Daubendiek, S.L., Ryan, K., Kool, E.T., Rolling-circle RNA-synthesis – circular oligonucleotides as efficient substrates for T7 RNA-polymerase. J. Am. Chem. Soc. 117 (1995), 7818–7819.
107. [107] Guo, P.X., The emerging field of RNA nanotechnology. Nat. Nanotechnol. 5 (2010), 833–842.
108. [108] Shu, Y., Pi, F.M., Sharma, A., Rajabi, M., Haque, F., Shu, D., Leggas, M., Evers, B.M., Guo, P.X., Stable RNA nanoparticles as potential new generation drugs for cancer therapy. Adv. Drug Deliv. Rev. 66 (2014), 74–89.
109. [109] Guo, P.X., Erickson, S., Anderson, D., A small viral-RNA is required for in vitro packaging of bacteriophage-Phi-29 DNA. Science 236 (1987), 690–694.
110. [110] Khaled, A., Guo, S.C., Li, F., Guo, P.X., Controllable self-assembly of nanoparticles for specific delivery of multiple therapeutic molecules to cancer cells using RNA nanotechnology. Nano Lett. 5 (2005), 1797–1808.
111. [111] Grabow, W.W., Zakrevsky, P., Afonin, K.A., Chworos, A., Shapiro, B.A., Jaeger, L., Self-assembling RNA nanorings based on RNAI/II inverse kissing complexes. Nano Lett. 11 (2011), 878–887.
112. [112] Afonin, K.A., Kireeva, M., Grabow, W.W., Kashlev, M., Jaeger, L., Shapiro, B.A., Co-transcriptional assembly of chemically modified RNA nanoparticles functionalized with siRNAs. Nano Lett. 12 (2012), 5192–5195.
113. [113] Eguchi, Y., Tomizawa, J., Complex formed by complementary RNA stem-loops and its stabilization by a protein - function of Cole1 rom protein. Cell 60 (1990), 199–209.
114. [114] Petros, R.A., DeSimone, J.M., Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Discov. 9 (2010), 615–627.
115. [115] Lee, H., Lytton-Jean, A.K.R., Chen, Y., Love, K.T., Park, A.I., Karagiannis, E.D., Sehgal, A., Querbes, W., Zurenko, C.S., Jayaraman, M., Peng, C.G., Charisse, K., Borodovsky, A., Manoharan, M., Donahoe, J.S., Truelove, J., Nahrendorf, M., Langer, R., Anderson, D.G., Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat. Nanotechnol. 7 (2012), 389–393.