Efficient siRNA delivery using novel siRNA-loaded Bubble liposomes and ultrasound

International Journal of Pharmaceutics

Volumn 422, Issue 1-2, 2012, Pages 504-509

  Endo Takahashi, Yoko ^a   Negishi, Yoichi ^a   Kato, Yasuharu ^a   Suzuki, Ryo ^b   Maruyama, Kazuo ^b   Aramaki, Yukihiko ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b TEIKYO UNIVERSITY   (Japan)

Author keywords

Bubble liposomes; siRNA delivery; Ultrasound

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; LIPOSOME; MACROGOL; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CYTOPLASM; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG SYNTHESIS; GENE SILENCING; GENETIC TRANSFECTION; NONHUMAN; PRIORITY JOURNAL; ULTRASOUND;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; FATTY ACIDS, MONOUNSATURATED; INJECTIONS; LIPOSOMES; LUCIFERASES; MICROBUBBLES; POLYETHYLENE GLYCOLS; QUATERNARY AMMONIUM COMPOUNDS; RNA INTERFERENCE; RNA STABILITY; RNA, SMALL INTERFERING; TRANSFECTION; ULTRASONICS;

EID: 84655174962     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2011.11.023     Document Type: Article

References (48)

1. T.M. Allen, C. Hansen, F. Martin, C. Redemann, and A. Yau-Young Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo Biochim. Biophys. Acta 1066 1991 29 36
2. C.Z. Behm, B.A. Kaufmann, C. Carr, M. Lankford, J.M. Sanders, C.E. Rose, S. Kaul, and J.R. Lindner Molecular imaging of endothelial vascular cell adhesion molecule-1 expression and inflammatory cell recruitment during vasculogenesis and ischemia-mediated arteriogenesis Circulation 117 2008 2902 2911 (Pubitemid 351787072)
3. G. Blume, and G. Cevc Liposomes for the sustained drug release in vivo Biochim. Biophys. Acta 1029 1990 91 97 (Pubitemid 20346426)
4. M. Delius, and G. Adams Shock wave permeabilization with ribosome inactivating proteins: a new approach to tumor therapy Cancer Res. 59 1999 5227 5232 (Pubitemid 29503986)
5. J. Du, Q.S. Shi, Y. Sun, P.F. Liu, M.J. Zhu, L.F. Du, and Y.R. Duan Enhanced delivery of monomethoxypoly(ethylene glycol)-poly(lactic-co-glycolic acid)-poly l-lysine nanoparticles loading platelet-derived growth factor BB small interfering RNA by ultrasound and/or microbubbles to rat retinal pigment epithelium cells J. Gene Med. 13 2011 312 323
6. M. Duvshani-Eshet, and M. Machluf Therapeutic ultrasound optimization for gene delivery: a key factor achieving nuclear DNA localization J. Control. Release 108 2005 513 528 (Pubitemid 41613754)
7. T. Endoh, and T. Ohtsuki Cellular siRNA delivery using cell-penetrating peptides modified for endosomal escape Adv. Drug Deliv. Rev. 61 2009 704 709
8. M. Frank-Kamenetsky, A. Grefhorst, N.N. Anderson, T.S. Racie, B. Bramlage, A. Akinc, D. Butler, K. Charisse, R. Dorkin, Y. Fan, C. Gamba-Vitalo, P. Hadwiger, M. Jayaraman, M. John, K.N. Jayaprakash, M. Maier, L. Nechev, K.G. Rajeev, T. Read, I. Röhl, J. Soutschek, P. Tan, J. Wong, G. Wang, T. Zimmermann, A. de Fougerolles, H.P. Vornlocher, R. Langer, D.G. Anderson, M. Manoharan, V. Koteliansky, J.D. Horton, and K. Fitzgerald Therapeutic RNAi targeting PCSK9 acutely lowers plasma cholesterol in rodents and LDL cholesterol in nonhuman primates Proc. Natl. Acad. Sci. U.S.A. 105 2008 11915 11920
9. W.J. Greenleaf, M.E. Bolander, G. Sarkar, M.B. Goldring, and J.F. Greenleaf Artificial cavitation nuclei significantly enhance acoustically induced cell transfection Ultrasound Med. Biol. 24 1998 587 595 (Pubitemid 28252453)
10. J. Halder, A.A. Kamat, C.N. Landen, 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, and A.K. Sood Focal adhesion kinase targeting using in vivo short interfering RNA delivery in neutral liposomes for ovarian carcinoma therapy Clin Cancer Res. 12 2006 4916 4924 (Pubitemid 44338579)
11. M. Harata, Y. Soda, K. Tani, J. Ooi, T. Takizawa, M. Chen, Y. Bai, K. Izawa, S. Kobayashi, A. Tomonari, F. Nagamura, S. Takahashi, K. Uchimaru, T. Iseki, T. Tsuji, T.A. Takahashi, K. Sugita, S. Nakazawa, A. Tojo, K. Maruyama, and S. Asano CD19-targeting liposomes containing imatinib efficiently kill Philadelphia chromosome-positive acute lymphoblastic leukemia cells Blood 104 2004 1442 1449 (Pubitemid 39166523)
12. R.P. Holmes, L.D. Yeaman, R.G. Taylor, and D.L. McCullough Altered neutrophil permeability following shock wave exposure in vitro J. Urol. 147 1992 733 737
13. S.H. Kim, J.H. Jeong, S.H. Lee, S.W. Kim, and T.G. Park Local and systemic delivery of VEGF siRNA using polyelectrolyte complex micelles for effective treatment of cancer J. Control. Release 129 2008 107 116
14. M. Kinoshita, and K. Hynynen A novel method for the intracellular delivery of siRNA using microbubble-enhanced focused ultrasound Biochem. Biophys. Res. Commun. 335 2005 393 399 (Pubitemid 41140235)
15. X.C. Kong, P. Barzaghi, and M.A. Ruegg Inhibition of synapse assembly in mammalian muscle in vivo by RNA interference EMBO Rep. 5 2004 183 188 (Pubitemid 38401199)
16. I. Lentacker, N. Wang, R.E. Vandenbroucke, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound exposure of lipoplex loaded microbubbles facilitates direct cytoplasmic entry of the lipoplexes Mol. Pharm. 6 2009 457 467
17. H. Leong-Poi, J. Christiansen, P. Heppner, C.W. Lewis, A.L. Klibanov, S. Kaul, and J.R. Lindner Assessment of endogenous and therapeutic arteriogenesis by contrast ultrasound molecular imaging of integrin expression Circulation 111 2005 3248 3254 (Pubitemid 40874997)
18. T. Li, K. Tachibana, M. Kuroki, and M. Kuroki Gene transfer with echo-enhanced contrast agents: comparison between Albunex, Optison, and Levovist in mice - initial results Radiology 229 2003 423 428 (Pubitemid 37310829)
19. K. Maruyama, O. Ishida, S. Kasaoka, T. Takizawa, N. Utoguchi, A. Shinohara, M. Chiba, H. Kobayashi, M. Eriguchi, and H. Yanagie Intracellular targeting of sodium mercaptoundecahydrododecaborate (BSH) to solid tumors by transferrin-PEG liposomes, for boron neutron-capture therapy (BNCT) J. Control. Release 98 2004 195 207 (Pubitemid 38950731)
20. K. Maruyama, T. Yuda, A. Okamoto, S. Kojima, A. Suginaka, and M. Iwatsuru Prolonged circulation time in vivo of large unilamellar liposomes composed of distearoyl phosphatidylcholine and cholesterol containing amphipathic poly(ethylene glycol) Biochim. Biophys. Acta 1128 1992 44 49
21. A.P. McCaffrey, L. Meuse, T.T. Pham, D.S. Conklin, G.J. Hannon, and M.A. Kay RNA interference in adult mice Nature 418 2002 38 39 (Pubitemid 34742563)
22. D.V. Morrissey, J.A. Lockridge, L. Shaw, K. Blanchard, K. Jensen, W. Breen, K. Hartsough, L. Machemer, S. Radka, V. Jadhav, N. Vaish, S. Zinnen, C. Vargeese, K. Bowman, C.S. Shaffer, L.B. Jeffs, A. Judge, I. MacLachlan, and B. Polisky Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs Nat. Biotechnol. 23 2005 1002 1007 (Pubitemid 41114035)
23. Y. Negishi, Y. Endo-Takahashi, K. Ishii, R. Suzuki, Y. Oguri, T. Murakami, K. Maruyama, and Y. Aramaki Development of novel nucleic acid-loaded Bubble liposomes using cholesterol-conjugated siRNA J. Drug Target 19 2011 830 836
24. Y. Negishi, Y. Endo, T. Fukuyama, R. Suzuki, T. Takizawa, D. Omata, K. Maruyama, and Y. Aramaki Delivery of siRNA into the cytoplasm by liposomal bubbles and ultrasound J. Control. Release 132 2008 124 130
25. Y. Negishi, K. Matsuo, Y. Endo-Takahashi, K. Suzuki, Y. Matsuki, N. Takagi, R. Suzuki, K. Maruyama, and Y. Aramaki Delivery of an angiogenic gene into ischemic muscle by novel bubble liposomes followed by ultrasound exposure Pharm. Res. 28 2011 712 719
26. Y. Negishi, Y. Tsunoda, Y. Endo-Takahashi, Y. Oda, R. Suzuki, K. Maruyama, M. Yamamoto, and Y. Aramaki Local gene delivery system by bubble liposomes and ultrasound exposure into joint synovium J. Drug Deliv. 2011 2011 203986
27. 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
28. S. Oliveira, M.M. Fretz, A. Høgset, G. Storm, and R.M. Schiffelers Photochemical internalization enhances silencing of epidermal growth factor receptor through improved endosomal escape of siRNA Biochim. Biophys. Acta 1768 2007 1211 1217 (Pubitemid 46553752)
29. K. Otani, K. Yamahara, S. Ohnishi, H. Obata, S. Kitamura, and N. Nagaya Nonviral delivery of siRNA into mesenchymal stem cells by a combination of ultrasound and microbubbles J. Control. Release 133 2009 146 153
30. M. Palmowski, J. Huppert, G. Ladewig, P. Hauff, M. Reinhardt, M.M. Mueller, E.C. Woenne, J.W. Jenne, M. Maurer, G.W. Kauffmann, W. Semmler, and F. Kiessling Molecular profiling of angiogenesis with targeted ultrasound imaging: early assessment of antiangiogenic therapy effects Mol. Cancer Ther. 7 2008 101 109
31. Y. Sadzuka, A. Nakade, R. Hirama, A. Miyagishima, Y. Nozawa, S. Hirota, and T. Sonobe Effects of mixed polyethyleneglycol modification on fixed aqueous layer thickness and antitumor activity of doxorubicin containing liposome Int. J. Pharm. 238 2002 171 180 (Pubitemid 34457886)
32. Y. Sato, K. Murase, J. Kato, M. Kobune, T. Sato, Y. Kawano, R. Takimoto, K. Takada, K. Miyanishi, T. Matsunaga, T. Takayama, and Y. Niitsu Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone Nat. Biotechnol. 26 2008 431 442 (Pubitemid 351501817)
33. R.M. Schiffelers, J. Xu, G. Storm, M.C. Woodle, and P.V. Scaria Effects of treatment with small interfering RNA on joint inflammation in mice with collagen-induced arthritis Arthritis Rheum. 52 2005 1314 1318 (Pubitemid 40530142)
34. P. Schratzberger, J.G. Krainin, G. Schratzberger, M. Silver, H. Ma, M. Kearney, R.F. Zuk, A.F. Brisken, D.W. Losordo, and J.M. Isner Transcutaneous ultrasound augments naked DNA transfection of skeletal muscle Mol. Ther. 6 2002 576 583 (Pubitemid 35363689)
35. E. Song, S.K. Lee, J. Wang, N. Ince, N. Ouyang, J. Min, J. Chen, P. Shankar, and J. Lieberman RNA interference targeting Fas protects mice from fulminant hepatitis Nat. Med. 9 2003 347 351 (Pubitemid 36362792)
36. S. Sonoda, K. Tachibana, E. Uchino, A. Okubo, M. Yamamoto, K. Sakoda, T. Hisatomi, K.H. Sonoda, Y. Negishi, Y. Izumi, S. Takao, and T. Sakamoto Gene transfer to corneal epithelium and keratocytes mediated by ultrasound with microbubbles Invest. Ophthalmol. Vis. Sci. 47 2006 558 564 (Pubitemid 46768382)
37. J. Suzuki, M. Ogawa, K. Takayama, Y. Taniyama, R. Morishita, Y. Hirata, R. Nagai, and M. Isobe Ultrasound-microbubble-mediated intercellular adhesion molecule-1 small interfering ribonucleic acid transfection attenuates neointimal formation after arterial injury in mice J. Am. Coll. Cardiol. 55 2010 904 913
38. R. Suzuki, T. Takizawa, Y. Negishi, K. Hagisawa, K. Tanaka, K. Sawamura, N. Utoguchi, T. Nishioka, and K. Maruyama Gene delivery by combination of novel liposomal bubbles with perfluoropropane and ultrasound J. Control. Release 117 2007 130 136 (Pubitemid 46161862)
39. R. Suzuki, T. Takizawa, Y. Negishi, N. Utoguchi, and K. Maruyama Effective gene delivery with novel liposomal bubbles and ultrasonic destruction technology Int. J. Pharm. 354 2008 49 55
40. R. Suzuki, T. Takizawa, Y. Negishi, N. Utoguchi, K. Sawamura, K. Tanaka, E. Namai, Y. Oda, Y. Matsumura, and K. Maruyama Tumor specific ultrasound enhanced gene transfer in vivo with novel liposomal bubbles J. Control. Release 125 2008 137 144 (Pubitemid 350299602)
41. Y. Takei, T. Nemoto, P. Mu, T. Fujishima, T. Ishimoto, Y. Hayakawa, Y. Yuzawa, S. Matsuo, T. Muramatsu, and K. Kadomatsu In vivo silencing of a molecular target by short interfering RNA electroporation: tumor vascularization correlates to delivery efficiency Mol. Cancer Ther. 7 2008 211 221
42. F. Takeshita, Y. Minakuchi, S. Nagahara, K. Honma, H. Sasaki, K. Hirai, T. Teratani, N. Namatame, Y. Yamamoto, K. Hanai, T. Kato, A. Sano, and T. Ochiya Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo Proc. Natl. Acad. Sci. U.S.A. 102 2005 12177 12182 (Pubitemid 41291148)
43. Y. Taniyama, K. Tachibana, K. Hiraoka, M. Aoki, S. Yamamoto, K. Matsumoto, T. Nakamura, T. Ogihara, Y. Kaneda, and R. Morishita Development of safe and efficient novel nonviral gene transfer using ultrasound: enhancement of transfection efficiency of naked plasmid DNA in skeletal muscle Gene Ther. 9 2002 372 380 (Pubitemid 34414035)
44. Y. Taniyama, K. Tachibana, K. Hiraoka, T. Namba, K. Yamasaki, N. Hashiya, M. Aoki, T. Ogihara, K. Yasufumi, and R. Morishita Local delivery of plasmid DNA into rat carotid artery using ultrasound Circulation 105 2002 1233 1239 (Pubitemid 34225826)
45. S. Tsunoda, O. Mazda, Y. Oda, Y. Iida, S. Akabame, T. Kishida, M. Shin-Ya, H. Asada, S. Gojo, J. Imanishi, H. Matsubara, and T. Yoshikawa Sonoporation using microbubble BR14 promotes pDNA/siRNA transduction to murine heart Biochem. Biophys. Res. Commun. 336 2005 118 127 (Pubitemid 41253411)
46. E.C. Unger, T. Porter, W. Culp, R. Labell, T. Matsunaga, and R. Zutshi Therapeutic applications of lipid-coated microbubbles Adv. Drug Deliv. Rev. 56 2004 1291 1314 (Pubitemid 38510475)
47. R.E. Vandenbroucke, I. Lentacker, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound assisted siRNA delivery using PEG-siPlex loaded microbubbles J. Control. Release 126 2008 265 273
48. C.F. Xia, Y. Zhang, Y. Zhang, R.J. Boado, and W.M. Pardridge Intravenous siRNA of brain cancer with receptor targeting and avidin-biotin technology Pharm. Res. 24 2007 2309 2316 (Pubitemid 350060723)