Non-Viral Delivery and Therapeutic Application of Small Interfering RNAs

Cover Page

Cite item

Abstract

RNA interference (RNAi) is a powerful method used for gene expression regulation. The increasing knowledge about the molecular mechanism of this phenomenon creates new avenues for the application of the RNAi technology in the treatment of various human diseases. However, delivery of RNA interference mediators, small interfering RNAs (siRNAs), to target cells is a major hurdle. Effective and safe pharmacological use of siRNAs requires carriers that can deliver siRNA to its target site and the development of methods for protection of these fragile molecules from in vivo degradation. This review summarizes various strategies for siRNA delivery, including chemical modification and non-viral approaches, such as the polymer-based, peptide-based, lipid-based techniques, and inorganic nanosystems. The advantages, disadvantages, and prospects for the therapeutic application of these methods are also examined in this paper.

About the authors

N. A. Nikitenko

Engelhardt Institute of Molecular Biology, Russian Academy of Sciences

Author for correspondence.
Email: nanthalia@gmail.com
Россия

V. S. Prassolov

Engelhardt Institute of Molecular Biology, Russian Academy of Sciences

Email: nanthalia@gmail.com
Россия

References

  1. Milhavet O., Gary D.S., Mattson M.P. // Pharmacol. Rev. 2003, V.55, №4, P.629-648
  2. Burnett J.C., Rossi J.J. // Chem. Biol. 2012, V.19, №1, P.60-71
  3. Vilgelm A.E., Chumakov S.P., Prassolov V.S. // Mol. Biol. 2006, V.40, №3, P.339-354
  4. Shrivastava N., Srivastava A. // Biotechnol. J. 2008, V.3, №3, P.339-353
  5. Scherr M., Morgan M.A., Eder M. // Curr. Med. Chem. 2003, V.10, №3, P.245-256
  6. Lima W.F., Murray H., Nichols J.G., Wu H., Sun H., Prakash T.P., Berdeja A.R., Gaus H.J., Crooke S.T. // J. Biol. Chem. 2009, V.284, №4, P.2535-2548
  7. Ma J.B., Ye K., Patel D.J. // Nature 2004, V.429, №6989, P.318-322
  8. Macrae I.J., Zhou K., Li F., Repic A., Brooks A.N., Cande W.Z., Adams P.D., Doudna J.A. // Science. 2006, V.311, P.195-198
  9. Zhang H., Kolb F.A., Jaskiewicz L., Westhof E., Filipowicz W. // Cell. 2004, V.118, №1, P.57-68
  10. Kim V.N., Han J., Siomi M.C. // Nat. Rev. Mol. Cell Biol. 2009, V.10, №2, P.126-139
  11. Hammond S.M. // FEBS Lett. 2005, V.579, №26, P.5822-5829
  12. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., Carthew R.W. // Cell. 2004, V.117, №1, P.69-81
  13. Wang Y., Juranek S., Li H., Sheng G., Tuschl T., Patel D.J. // Nature 2008, V.456, №7224, P.921-926
  14. MacRae I.J., Ma E., Zhou M., Robinson C.V., Doudna J.A. // Proc. Natl. Acad. Sci. USA. 2008, V.105, №2, P.512-517
  15. Miyoshi K., Okada T.N., Siomi H., Siomi M.C. // RNA. 2009, V.15, №7, P.1282-1291
  16. Wang Y., Juranek S., Li H., Sheng G., Wardle G.S., Tuschl T., Patel D.J. // Nature 2009, V.461, №7265, P.754-761
  17. Nowotny M., Yang W. // Curr. Opin. Struct. Biol. 2009, V.19, №3, P.286-293
  18. Birney E., Stamatoyannopoulos J.A., Dutta A., Guigo R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T., Thurman R.E. // Nature 2007, V.447, №7146, P.799-816
  19. Carthew R.W., Sontheimer E.J. // Cell. 2009, V.136, №4, P.642-655
  20. Titov I.I., Vorozheykin P.S. // Vavilov Journal of Genetics and Breeding. 2011, V.15, №1, P.139-147
  21. Makarova J.A., Kramerov D.A. // Biochemistry (Moscow). 2007, V.72, №11, P.1427-1448
  22. Yekta S., Shih I.H., Bartel D.P. // Science. 2004, V.304, №5670, P.594-596
  23. Ameres S.L., Martinez J., Schroeder R. // Cell. 2007, V.130, №1, P.101-112
  24. Selbach M., Schwanhausser B., Thierfelder N., Fang Z., Khanin R., Rajewsky N. // Nature 0208, V.455, №7209, P.58-63
  25. Kawakami S., Hashida M. // Drug Metabolism and Рharmacokinetics. 2007, V.22, №3, P.142-151
  26. Watts J.K., Deleavey G.F., Damha M.J. // Drug Discovery Today. 2008, V.13, №19-20, P.842-855
  27. Hartmann G. // J. Clin. Invest. 2009, V.119, №3, P.438-442
  28. Fang J., Sawa T., Maeda H. // Adv. Exp. Med. Biology. 2003, V.519, P.29-49
  29. Zamecnik J., Vargova L., Homola A., Kodet R., Sykova E. // Neuropathol. Appl. Neurobiol. 2004, V.30, №4, P.338-350
  30. Singh S., Narang A.S., Mahato R.I. // Pharmaceut. Res. 2011, V.28, №12, P.2996-3015
  31. Perez-Martinez F.C., Guerra J., Posadas I., Cena V. // Pharmaceut. Res. 2011, V.28, №8, P.1843-1858
  32. Arias J.L., Clares B., Morales M.E., Gallardo V., Ruiz M.A. // Curr. Drug Targets. 2011, V.12, №8, P.1151-1165
  33. Leucuta S.E. // Curr. Clin. Pharmacol. 2012, V.7, №4, P.282-317
  34. Khatri N., Rathi M., Baradia D., Trehan S., Misra A. // Crit. Rev. Therapeutic Drug Carrier Systems. 2012, V.29, №6, P.487-527
  35. Sakurai Y., Hatakeyama H., Sato Y., Akita H., Takayama K., Kobayashi S., Futaki S., Harashima H. // Biomaterials. 2011, V.32, №24, P.5733-5742
  36. Duan J., Zhang Y., Chen W., Shen C., Liao M., Pan Y., Wang J., Deng X., Zhao J. // J. Biomed. Biotechnol. 2009, V.2009, P.149-254
  37. Pack D.W., Hoffman A.S., Pun S., Stayton P.S. // Nat. Rev. Drug Discovery. 2005, V.4, №7, P.581-593
  38. Sonawane N.D., Szoka F.C., Jr. I.O., Verkman A.S. // J. Biol. Chem. 2003, V.278, №45, P.44826-44831
  39. Eliyahu H., Barenholz Y., Domb A.J. // Molecules. 2005, V.10, №1, P.34-64
  40. Nguyen J., Szoka F.C. // Accounts Chem. Res. 2012, V.45, №7, P.1153-1162
  41. Zelphati O., Szoka F.C., Jr. I.O. // Proc. Natl. Acad. Sci. USA. 1996, V.93, №21, P.11493-11498
  42. Hafez I.M., Maurer N., Cullis P.R. // Gene Therapy. 2001, V.8, №15, P.1188-1196
  43. Chu C.Y., Rana T.M. // RN A. 2008, V.14, №9, P.1714-1719
  44. Zou Y., Tiller P., Chen I.W., Beverly M., Hochman J. // Rapid Comm. Mass Spectrometry: RC M. 2008, V.22, №12, P.1871-1881
  45. Bramsen J.B., Kjems J. // Meth. Mol. Biol. 2011, V.721, P.77-103
  46. Chernolovskaya E.L., Zenkova M.A. // Curr. Opin. Mol. Therapeutics. 2010, V.12, №2, P.158-167
  47. Rose S.D., Kim D.H., Amarzguioui M., Heidel J.D., Collingwood M.A., Davis M.E., Rossi J.J., Behlke M.A. // Nucleic Acids Research 2005, V.33, №13, P.4140-4156
  48. Dore-Savard L., Roussy G., Dansereau M.A., Collingwood M.A., Lennox K.A., Rose S.D., Beaudet N., Behlke M.A., Sarret P. // Mol. Therapy: J. Am. Soc. Gene Therapy. 2008, V.16, №7, P.1331-1339
  49. Deleavey G.F., Watts J.K., Damha M.J. // Curr. Prot. Nucl. Acids Chem. 2009, SSuppl. 39, P.16.3.1-16.3.22
  50. Phelps K., Morris A., Beal P.A. // ACS Chem. Biol. 2012, V.7, №1, P.100-109
  51. Detzer A., Sczakiel G. // Curr. Topics Med. Chem. 2009, V.9, №12, P.1109-1116
  52. Mescalchin A., Detzer A., Wecke M., Overhoff M., Wunsche W., Sczakiel G. // Expert. Opinion Biol. Therapy. 2007, V.7, №10, P.1531-1538
  53. Harborth J., Elbashir S.M., Vandenburgh K., Manninga H., Scaringe S.A., Weber K., Tuschl T. // Harborth J., Elbashir S.M., Vandenburgh K., Manninga H., Scaringe S.A., Weber K., Tuschl T. 2003, V.13, №2, P.83-105
  54. Li Z.Y., Mao H., Kallick D.A., Gorenstein D.G. // Biochem. Biophys. Res. Commun. 2005, V.329, №3, P.1026-1030
  55. Prakash T.P., Allerson C.R., Dande P., Vickers T.A., Sioufi N., Jarres R., Baker B.F., Swayze E.E., Griffey R.H., Bhat B. // J. Med. Chem. 2005, V.48, №13, P.4247-4253
  56. Gaglione M., Messere A. // Mini Rev. Med. Chem. 2010, V.10, №7, P.578-595
  57. Kraynack B.A., Baker B.F. // RN A. 2006, V.12, №1, P.163-176
  58. Pallan P.S., Greene E.M., Jicman P.A., Pandey R.K., Manoharan M., Rozners E., Egli M. // Nucleic Acids Research 2011, V.39, №8, P.3482-3495
  59. Allerson C.R., Sioufi N., Jarres R., Prakash T.P., Naik N., Berdeja A., Wanders L., Griffey R.H., Swayze E.E., Bhat B. // J. Med. Chem. 2005, V.48, №4, P.901-904
  60. Muhonen P., Tennila T., Azhayeva E., Parthasarathy R.N., Janckila A.J., Vaananen H.K., Azhayev A., Laitala-Leinonen T. // Chem. Biodiversity. 2007, V.4, №5, P.858-873
  61. Morrissey D.V., Lockridge J.A., Shaw L., Blanchard K., Jensen K., Breen W., Hartsough K., Machemer L., Radka S., Jadhav V. // Nat. Biotechnol. 2005, V.23, №8, P.1002-1007
  62. Ferrari N., Bergeron D., Tedeschi A.L., Mangos M.M., Paquet L., Renzi P.M., Damha M.J. // Ann. N.Y. Acad. Sci. 2006, V.1082, P.91-102
  63. Dowler T., Bergeron D., Tedeschi A.L., Paquet L., Ferrari N., Damha M.J. // Nucl. Аcids Res. 2006, V.34, №6, P.1669-1675
  64. Watts J.K., Choubdar N., Sadalapure K., Robert F., Wahba A.S., Pelletier J., Pinto B.M., Damha M.J. // Nucleic Acids Research 2007, V.35, №5, P.1441-1451
  65. Lima W.F., Wu H., Nichols J.G., Sun H., Murray H.M., Crooke S.T. // J. Biol. Chem. 2009, V.284, №38, P.26017-26028
  66. Vickers T.A., Zhang H., Graham M.J., Lemonidis K.M., Zhao C., Dean N.M. // J. Immunol. 2006, V.176, №6, P.3652-3661
  67. Moschos S.A., Frick M., Taylor B., Turnpenny P., Graves H., Spink K.G., Brady K., Lamb D., Collins D., Rockel T.D. // Mol. Therapy: J. Am. Soc. Gene Therapy. 2011, V.19, №12, P.2163-2168
  68. Elmen J., Thonberg H., Ljungberg K., Frieden M., Westergaard M., Xu Y., Wahren B., Liang Z., Orum H., Koch T. // Nucleic Acids Research 2005, V.33, №1, P.439-447
  69. Mook O.R., Baas F., de Wissel M.B., Fluiter K. // Mol. Cancer Therapeut. 2007, V.6, №3, P.833-843
  70. Swayze E.E., Siwkowski A.M., Wancewicz E.V., Migawa M.T., Wyrzykiewicz T.K., Hung G., Monia B.P., Bennett C.F. // Nucleic Acids Research 2007, V.35, №2, P.687-700
  71. Hoffmann S., Hoos J., Klussmann S., Vonhoff S. // Curr. Prot. Nucl. Acids Chem. 2011, SSuppl. 46, P.4.46.1-4.46.30
  72. Luo D., Saltzman W.M. // Nat. Biotechnol. 2000, V.18, №8, P.893-895
  73. Paulo C.S., Pires das Neves R., Ferreira L.S. // Nanotechnology. 2011, V.22, №49, P.494002
  74. Jafari M., Soltani M., Naahidi S., Karunaratne D.N., Chen P. // Curr. Med. Chem. 2012, V.19, №2, P.197-208
  75. Xing J., Deng L., Guo S., Dong A., Liang X.J. // Mini Rev. Med. Chem. 2010, V.10, №2, P.126-137
  76. Tros de Ilarduya C., Sun Y., Duzgunes N. // Eur. J. Pharmaceut.Sci. // Official J. Eur. Fed. Pharmaceut. Sci. 2010, V.40, №3, P.159-170
  77. Jere D., Jiang H.L., Arote R., Kim Y.K., Choi Y.J., Cho M.H., Akaike T., Cho C.S. // Expert Opin. Drug Delivery. 2009, V.6, №8, P.827-834
  78. Nimesh S. // Curr. Clin. Pharm. 2012, V.7, №2, P.121-130
  79. Singha K., Namgung R., Kim W.J. // Nucl. Acid Therapeut. 2011, V.21, №3, P.133-147
  80. Hong S., Leroueil P.R., Janus E.K., Peters J.L., Kober M.M., Islam M.T., Orr B.G., Baker J.R., Jr. I.O., Banaszak Holl M.M. // Bioconjugate Chem. 2006, V.17`, №3, P.728-734
  81. Wightman L., Kircheis R., Rossler V., Carotta S., Ruzicka R., Kursa M., Wagner E. // The Journal of Gene Medicine 2001, V.3, №4, P.362-372
  82. Luten J., van Nostrum C.F., De Smedt S.C., Hennink W.E. // J. Controlled Release: Official J. Controlled Release Soc. 2008, V.126, №2, P.97-110
  83. Gary D.J., Puri N., Won Y.Y. // J. Controlled Release: Official J. Controlled Release Soc. 2007, V.121, №1-2, P.64-73
  84. Cun D., Foged C., Yang M., Frokjaer S., Nielsen H.M. // Internat. J. Pharmaceut. 2010, V.390, №1, P.70-75
  85. Presumey J., Salzano G., Courties G., Shires M., Ponchel F., Jorgensen C., Apparailly F., De Rosa G. // Eur. J. Pharmaceut. Biopharmaceut. // Official J. Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V. 2012, V.82, №3, P.457-464
  86. Steinbach J.M., Weller C.E., Booth C.J., Saltzman W.M. // J. Controlled Release: Official J. Controlled Release Soc. 2012, V.162, №1, P.102-110
  87. Svenson S., Tomalia D.A. // Adv. Drug Delivery Rev. 2005, V.57, №15, P.2106-2129
  88. Quadir M.A., Haag R. // J. Controlled Release: Official J. Controlled Release Soc. 2012, V.161, №2, P.484-495
  89. Morgan M.T., Nakanishi Y., Kroll D.J., Griset A.P., Carnahan M.A., Wathier M., Oberlies N.H., Manikumar G., Wani M.C., Grinstaff M.W. // Cancer Research 2006, V.66, №24, P.11913-11921
  90. Dufes C., Uchegbu I.F., Schatzlein A.G. // Adv. Drug Delivery Rev. 2005, V.57, №15, P.2177-2202
  91. Tomalia D.A., Reyna L.A., Svenson S. // Biochem. Soc. Transactions. 2007, V.35 Pt1, P.61-67
  92. Wang Y., Li Z., Han Y., Liang L.H., Ji A. // Curr. Drug Metabolism. 2010, V.11, №2, P.182-196
  93. Minko T., Patil M.L., Zhang M., Khandare J.J., Saad M., Chandna P., Taratula O. // Meth. Mol. Biol. 2010, V.624, P.281-294
  94. Kim I.D., Lim C.M., Kim J.B., Nam H.Y., Nam K., Kim S.W., Park J.S., Lee J.K. // J. Controlled Release: Official J. Controlled Release Soc. 2010, V.142, №3, P.422-430
  95. Tang Y., Li Y.B., Wang B., Lin R.Y., van Dongen M., Zurcher D.M., Gu X.Y., Banaszak Holl M.M., Liu G., Qi R. // Mol. Pharmaceut. 2012, V.9, №6, P.1812-1821
  96. Taratula O., Garbuzenko O.B., Kirkpatrick P., Pandya I., Savla R., Pozharov V.P., He H., Minko T. // J. Controlled Release: Official J. Controlled Release Soc. 2009, V.140, №3, P.284-293
  97. Rudzinski W.E., Aminabhavi T.M. // Internat. J. Pharmaceut. 2010, V.399, №1-2, P.1-11
  98. Saranya N., Moorthi A., Saravanan S., Devi M.P., Selvamurugan N. // Internat. J. Biol. Macromolecules. 2011, V.48, №2, P.234-238
  99. Alameh M., Dejesus D., Jean M., Darras V., Thibault M., Lavertu M., Buschmann M.D., Merzouki A. // Internat. J. Nanomed. 2012, V.7, P.1399-1414
  100. Katas H., Alpar H.O. // J. Controlled Release: Official J. Controlled Release Soc. 2006, V.115, №2, P.216-225
  101. Howard K.A., Rahbek U.L., Liu X., Damgaard C.K., Glud S.Z., Andersen M.O., Hovgaard M.B., Schmitz A., Nyengaard J.R., Besenbacher F. // Mol. Therapy: J. Am. Soc. Gene Therapy. 2006, V.14, №4, P.476-484
  102. Nielsen E.J., Nielsen J.M., Becker D., Karlas A., Prakash H., Glud S.Z., Merrison J., Besenbacher F., Meyer T.F., Kjems J. // Pharmaceut. Res. 2010, V.27, №12, P.2520-2527
  103. Howard K.A., Paludan S.R., Behlke M.A., Besenbacher F., Deleuran B., Kjems J. // Mol. Therapy: J. Am. Soc. Gene Therapy. 2009, V.17, №1, P.162-168
  104. Tripathi S.K., Goyal R., Kashyap M.P., Pant A.B., Haq W., Kumar P., Gupta K.C. // Biomaterials. 2012, V.33, №16, P.4204-4219
  105. Lee D.W., Yun K.S., Ban H.S., Choe W., Lee S.K., Lee K.Y. // J. Controlled Release: Official J. Controlled Release Soc. 2009, V.139, №2, P.146-152
  106. Ji A.M., Su D., Che O., Li W.S., Sun L., Zhang Z.Y., Yang B., Xu F. // Nanotechnology. 2009, V.20, №40, P.405103
  107. Pille J.Y., Li H., Blot E., Bertrand J.R., Pritchard L.L., Opolon P., Maksimenko A., Lu H., Vannier J.P., Soria J. // Hum. Gene Therapy. 2006, V.17, №10, P.1019-1026
  108. O'Mahony A.M., Godinho B.M., Ogier J., Devocelle M., Darcy R., Cryan J.F., O'Driscoll C.M. // ACS Chem. Neurosci. 2012, V.3, №10, P.744-752
  109. Alabi C., Vegas A., Anderson D. // Curr. Opin. Pharmacol. 2012, V.12, №4, P.427-433
  110. Hu-Lieskovan S., Heidel J.D., Bartlett D.W., Davis M.E., Triche T.J. // Cancer Research 2005, V.65, №19, P.8984-8992
  111. Davis M.E., Zuckerman J.E., Choi C.H., Seligson D., Tolcher A., Alabi C.A., Yen Y., Heidel J.D., Ribas A. // Nature 2010, V.464, №7291, P.1067-1070
  112. Heidel J.D., Yu Z., Liu J.Y., Rele S.M., Liang Y., Zeidan R.K., Kornbrust D.J., Davis M.E. // Proc. Natl. Acad. Sci. USA. 2007, V.104, №14, P.5715-5721
  113. Zhang S., Zhi D., Huang L. // J. Drug Targeting. 2012, V.20, №9, P.724-735
  114. Delong R.K., Risor A., Kanomata M., Laymon A., Jones B., Zimmerman S.D., Williams J., Witkowski C., Warner M., Ruff M. // Nanomedicine (Lond.). 2012, V.7, №12, P.1851-1862
  115. Gavrilov K., Saltzman W.M. // Yale J. Biol. Med. 2012, V.85, №2, P.187-200
  116. Aliabadi H.M., Landry B., Sun C., Tang T., Uludag H. // Biomaterials. 2012, V.33, №8, P.2546-2569
  117. Northfelt D.W., Dezube B.J., Thommes J.A., Levine R., von Roenn J.H., Dosik G.M., Rios A., Krown S.E., DuMond C., Mamelok R.D. // J. Clin. Oncol.: Official J. Am. Soc. Clin. Oncol. 1997, V.15, №2, P.653-659
  118. Gooding M., Browne L.P., Quinteiro F.M., Selwood D.L. // Chem. Biol. Drug Design. 2012, V.80, №6, P.787-809
  119. Venturini M., Bighin C., Puglisi F., Olmeo N., Aitini E., Colucci G., Garrone O., Paccagnella A., Marini G., Crino L. // Breast. 2010, V.19, №5, P.333-338
  120. Landen C.N., Jr. I.O., Chavez-Reyes A., Bucana C., Schmandt R., Deavers M.T., Lopez-Berestein G., Sood A.K. // Cancer Research 2005, V.65, №15, P.6910-6918
  121. Kang S.H., Cho H.J., Shim G., Lee S., Kim S.H., Choi H.G., Kim C.W., Oh Y.K. // Pharmaceut. Res. 2011, V.28, №12, P.3069-3078
  122. Briane D., Slimani H., Tagounits A., Naejus R., Haddad O., Coudert R., Charnaux N., Cao A. // J. Drug Targeting. 2012, V.20, №4, P.347-354
  123. Un K., Kawakami S., Higuchi Y., Suzuki R., Maruyama K., Yamashita F., Hashida M. // J. Controlled Release: Official J. Controlled Release Soc. 2011, V.156, №3, P.355-363
  124. Un K., Kawakami S., Suzuki R., Maruyama K., Yamashita F., Hashida M. // Biomaterials. 2010, V.31, №30, P.7813-7826
  125. Un K., Kawakami S., Suzuki R., Maruyama K., Yamashita F., Hashida M. // Mol. Pharmaceut. 2011, V.8, №2, P.543-554
  126. Un K., Kawakami S., Yoshida M., Higuchi Y., Suzuki R., Maruyama K., Yamashita F., Hashida M. // Hepatology. 2012, V.56, №1, P.259-269
  127. Wu S.Y., McMillan N.A. // AAPS J. 2009, V.11, №4, P.639-652
  128. Zimmermann T.S., Lee A.C., Akinc A., Bramlage B., Bumcrot D., Fedoruk M.N., Harborth J., Heyes J.A., Jeffs L.B., John M. // Nature 2006, V.411, №7089, P.111-114
  129. Laufer S.D., Restle T. // Curr. Pharmaceut. Design. 2008, V.11, №34, P.3637-3655
  130. Herce H.D., Garcia A.E. // J. Biol. Physics. 2007, V.33, №5-6, P.345-356
  131. Fonseca S.B., Pereira M.P., Kelley S.O. // Adv. Drug Delivery Rev. 2009, V.61, №11, P.953-964
  132. Sebbage V. // Biosci. Horizons. 2009, V.2, №1, P.64-72
  133. Stewart K.M., Horton K.L., Kelley S.O. // Organic Biomol. Chem. 2008, V.6, №13, P.2242-2255
  134. Trabulo S., Cardoso A.L., Mano M., De Lima M.C.P. // Pharmaceuticals. 2010, V.3, №4, P.961-993
  135. Vives E., Schmidt J., Pelegrin A. // Biochim. Biophys. Acta. 2008, V.1786, №2, P.126-138
  136. Finstad C.L., Wang C.Y., Kowalski J., Zhang M., Li M.L., Li X.M., Xia W.G., Bosland M.C., Murthy K.K., Walfield A.M. // Vaccine. 2004, V.22, №9-10, P.1300-1313
  137. Pooga M., Langel U. // Meth. Mol. Biol. 2005, V.298, P.77-89
  138. Muratovska A., Eccles M.R. // FEBS Lett. 2004, V.558, №1-3, P.63-68
  139. Moschos S.A., Jones S.W., Perry M.M., Williams A.E., Erjefalt J.S., Turner J.J., Barnes P.J., Sproat B.S., Gait M.J., Lindsay M.A. // Bioconjugate Chem. 2007, V.18, №5, P.1450-1459
  140. Morris M.C., Gros E., Aldrian-Herrada G., Choob M., Archdeacon J., Heitz F., Divita G. // Nucleic Acids Research 2007, V.35, №7, P.e49
  141. Crombez L., Charnet A., Morris M.C., Aldrian-Herrada G., Heitz F., Divita G. // Biochem. Soc. Transact. 2007, V.35 Pt1, P.44-46
  142. Liu B.R., Chou J.C., Lee H.J. // J. Membrane Biol. 2008, V.222, №1, P.1-15
  143. Meade B.R., Dowdy S.F. // Adv. Drug Delivery Rev. 2008, V.60, №4-5, P.530-536
  144. Hoyer J., Neundorf I. // J. Controlled Release: Official J. Controlled Release Soc. 2012, V.161, №3, P.823-834
  145. Johnson L.N., Cashman S.M., Kumar-Singh R. // Mol. Therapy: J. Am. Soc. Gene Therapy. 2008, V.16, №1, P.107-114
  146. Cheung W., Pontoriero F., Taratula O., Chen A.M., He H. // Adv. Drug Delivery Rev. 2010, V.62, №6, P.633-649
  147. Qi L., Gao X. // ACS Nano. 2008, V.2, №7, P.1403-1410
  148. Boisselier E., Astruc D. // Chem. Soc. Rev. 2009, V.38, №6, P.1759-1782
  149. Zhang S., Zhao Y., Zhi D. // Bioorganic Chem. 2012, V.40, №1, P.10-18
  150. Son S.J., Bai X., Lee S.B. // Drug Discovery Today. 2007, V.12, №15-16, P.650-656
  151. Liu G., Swierczewska M., Lee S., Chen X. // Nano Today. 2010, V.5, №6, P.524-539
  152. Neagoe I.B., Braicu C., Matea C., Bele C., Florin G., Gabriel K., Veronica C., Irimie A. // J. Biomed. Nanotechnol. 2012, V.8, №4, P.567-574
  153. Wang X., Ren J., Qu X. // ChemMedChem. 2008, V.3, №6, P.940-945
  154. Gao J., Chen K., Xie R., Xie J., Yan Y., Cheng Z., Peng X., Chen X. // Bioconjugate Chem. 2010, V.21, №4, P.604-609
  155. Jung J., Solanki A., Memoli K.A., Kamei K., Kim H., Drahl M.A., Williams L.J., Tseng H.R., Lee K. // Angew Chem. Int. Ed. Engl. 2010, V.49, №1, P.103-107
  156. Bumcrot D., Manoharan M., Koteliansky V., Sah D.W. // Nat. Chem. Biol. 2006, V.2, №12, P.711-719
  157. Tan W.B., Jiang S., Zhang Y. // Biomaterials. 2007, V.28, №8, P.1565-1571
  158. Yezhelyev M.V., Qi L., O'Regan R.M., Nie S., Gao X. // J. Am. Chem. Soc. 2008, V.130, №28, P.9006-9012
  159. Subramaniam P., Lee S.J., Shah S., Patel S., Starovoytov V., Lee K.B. // Adv. Mater. 2012, V.24, №29, P.4014-4019
  160. Kim S.T., Chompoosor A., Yeh Y.C., Agasti S.S., Solfiell D.J., Rotello V.M. // Small. 2012, V.8, №21, P.3253-3256
  161. Duncan R. // Curr. Opin. Biotechnol. 2011, V.22, №4, P.492-501
  162. Summers H.D., Rees P., Holton M.D., Brown M.R., Chappell S.C., Smith P.J., Errington R.J. // Nat. Nanotechnol. 2011, V.6, №3, P.170-174
  163. Serda R.E., Godin B., Blanco E., Chiappini C., Ferrari M. // Biochim. Biophys. Acta. 2011, V.1810, №3, P.317-329
  164. Ferrari M. // Trends Biotechnol. 2010, V.28, №4, P.181-188
  165. Souza G.R., Christianson D.R., Staquicini F.I., Ozawa M.G., Snyder E.Y., Sidman R.L., Miller J.H., Arap W., Pasqualini R. // Proc. Natl. Acad. Sci. USA. 2006, V.103, №5, P.1215-1220
  166. Sengupta S., Eavarone D., Capila I., Zhao G., Watson N., Kiziltepe T., Sasisekharan R. // Nature 2005, V.436, №7050, P.568-572
  167. Tasciotti E., Liu X., Bhavane R., Plant K., Leonard A.D., Price B.K., Cheng M.M., Decuzzi P., Tour J.M., Robertson F. // Nat. Nanotechnol. 2008, V.3, №3, P.151-157

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2013 Nikitenko N.A., Prassolov V.S.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies