Nonviral Gene Delivery Systems by the Combination of Bubble Liposomes and Ultrasound

Advances in Genetics

Volumn 89, Issue , 2015, Pages 25-48

  Omata, Daiki ^a   Negishi, Yoichi ^b   Suzuki, Ryo ^a   Oda, Yusuke ^a   Endo Takahashi, Yoko ^b   Maruyama, Kazuo ^a  

^a TEIKYO UNIVERSITY   (Japan)

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

Author keywords

Cavitation; Microbubble; MRNA; Nanobubble; Non viral gene delivery systems; SiRNA; Sonopolation; Theranostics; Ultrasound

Indexed keywords

LIPOSOME; SMALL INTERFERING RNA;

ANIMAL; CHEMISTRY; ECHOGRAPHY; GENE TRANSFER; GENETICS; HUMAN; MICROBUBBLE;

ANIMALS; GENE TRANSFER TECHNIQUES; HUMANS; LIPOSOMES; MICROBUBBLES; RNA, SMALL INTERFERING; ULTRASONOGRAPHY;

EID: 84921466966     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.adgen.2014.11.001     Document Type: Article

References (79)

1. Atkins M.B., Robertson M.J., Gordon M., Lotze M.T., DeCoste M., DuBois J.S., et al. Phase I evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 1997, 3:409-417.
2. Brunda M.J. Interleukin-12. Journal of Leukocyte Biology 1994, 55:280-288.
3. Check E. Safety panel backs principle of gene-therapy trials. Nature 2002, 420:595.
4. Check E. Second cancer case halts gene-therapy trials. Nature 2003, 421:305.
5. Chen S., Ding J.H., Bekeredjian R., Yang B.Z., Shohet R.V., Johnston S.A., et al. Efficient gene delivery to pancreatic islets with ultrasonic microbubble destruction technology. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:8469-8474.
6. Colombo M.P., Vagliani M., Spreafico F., Parenza M., Chiodoni C., Melani C., et al. Amount of interleukin 12 available at the tumor site is critical for tumor regression. Cancer Research 1996, 56:2531-2534.
7. Duvshani-Eshet M., Adam D., Machluf M. The effects of albumin-coated microbubbles in DNA delivery mediated by therapeutic ultrasound. Journal of Controlled Release: Official Journal of the Controlled Release Society 2006, 112:156-166.
8. Duvshani-Eshet M., Baruch L., Kesselman E., Shimoni E., Machluf M. Therapeutic ultrasound-mediated DNA to cell and nucleus: bioeffects revealed by confocal and atomic force microscopy. Gene Therapy 2006, 13:163-172.
9. 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 2001, 411:494-498.
10. Endo-Takahashi Y., Negishi Y., Kato Y., Suzuki R., Maruyama K., Aramaki Y. Efficient siRNA delivery using novel siRNA-loaded bubble liposomes and ultrasound. International Journal of Pharmaceutics 2012, 422:504-509.
11. Endo-Takahashi Y., Negishi Y., Nakamura A., Suzuki D., Ukai S., Sugimoto K., et al. pDNA-loaded bubble liposomes as potential ultrasound imaging and gene delivery agents. Biomaterials 2013, 34:2807-2813.
12. Endo-Takahashi Y., Negishi Y., Nakamura A., Ukai S., Ooaku K., Oda Y., et al. Systemic delivery of miR-126 by miRNA-loaded bubble liposomes for the treatment of hindlimb ischemia. Scientific Reports 2014, 4:3883.
13. Fan Z., Kumon R.E., Park J., Deng C.X. Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. Journal of Controlled Release: Official Journal of the Controlled Release Society 2010, 142:31-39.
14. Fears C.Y., Woods A. The role of syndecans in disease and wound healing. Matrix Biology: Journal of the International Society for Matrix Biology 2006, 25:443-456.
15. Fechheimer M., Boylan J.F., Parker S., Sisken J.E., Patel G.L., Zimmer S.G. Transfection of mammalian cells with plasmid DNA by scrape loading and sonication loading. Proceedings of the National Academy of Sciences of the United States of America 1987, 84:8463-8467.
16. Feril L.B., Kondo T., Zhao Q.L., Ogawa R., Tachibana K., Kudo N., et al. Enhancement of ultrasound-induced apoptosis and cell lysis by echo-contrast agents. Ultrasound in Medicine & Biology 2003, 29:331-337.
17. Feril L.B., Ogawa R., Tachibana K., Kondo T. Optimized ultrasound-mediated gene transfection in cancer cells. Cancer Science 2006, 97:1111-1114.
18. Fish J.E., Santoro M.M., Morton S.U., Yu S., Yeh R.F., Wythe J.D., et al. miR-126 regulates angiogenic signaling and vascular integrity. Developmental Cell 2008, 15:272-284.
19. Gao Z., Kennedy A.M., Christensen D.A., Rapoport N.Y. Drug-loaded nano/microbubbles for combining ultrasonography and targeted chemotherapy. Ultrasonics 2008, 48:260-270.
20. Greenleaf W.J., Bolander M.E., Sarkar G., Goldring M.B., Greenleaf J.F. Artificial cavitation nuclei significantly enhance acoustically induced cell transfection. Ultrasound in Medicine & Biology 1998, 24:587-595.
21. Guo D.P., Li X.Y., Sun P., Tang Y.B., Chen X.Y., Chen Q., et al. Ultrasound-targeted microbubble destruction improves the low density lipoprotein receptor gene expression in HepG2 cells. Biochemical and Biophysical Research Communications 2006, 343:470-474.
22. Hama S., Akita H., Ito R., Mizuguchi H., Hayakawa T., Harashima H. Quantitative comparison of intracellular trafficking and nuclear transcription between adenoviral and lipoplex systems. Molecular Therapy: The Journal of the American Society of Gene Therapy 2006, 13:786-794.
23. Hassan M.A., Buldakov M.A., Ogawa R., Zhao Q.L., Furusawa Y., Kudo N., et al. Modulation control over ultrasound-mediated gene delivery: evaluating the importance of standing waves. Journal of Controlled Release: Official Journal of the Controlled Release Society 2010, 141:70-76.
24. Hassan M.A., Feril L.B., Suzuki K., Kudo N., Tachibana K., Kondo T. Evaluation and comparison of three novel microbubbles: enhancement of ultrasound-induced cell death and free radicals production. Ultrasonics Sonochemistry 2009, 16:372-378.
25. Itaka K., Ohba S., Miyata K., Kawaguchi H., Nakamura K., Takato T., et al. Bone regeneration by regulated in vivo gene transfer using biocompatible polyplex nanomicelles. Molecular Therapy: The Journal of the American Society of Gene Therapy 2007, 15:1655-1662.
26. Juffermans L.J., Dijkmans P.A., Musters R.J., Visser C.A., Kamp O. Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. American Journal of Physiology. Heart and Circulatory Physiology 2006, 291:H1595-H1601.
27. Juffermans L.J., Kamp O., Dijkmans P.A., Visser C.A., Musters R.J. Low-intensity ultrasound-exposed microbubbles provoke local hyperpolarization of the cell membrane via activation of BK(Ca) channels. Ultrasound in Medicine & Biology 2008, 34:502-508.
28. Kalantarinia K., Belcik J.T., Patrie J.T., Wei K. Real-time measurement of renal blood flow in healthy subjects using contrast-enhanced ultrasound. American Journal of Physiology. Renal Physiology 2009, 297:F1129-F1134.
29. Kobayashi N., Kuramoto T., Yamaoka K., Hashida M., Takakura Y. Hepatic uptake and gene expression mechanisms following intravenous administration of plasmid DNA by conventional and hydrodynamics-based procedures. The Journal of Pharmacology and Experimental Therapeutics 2001, 297:853-860.
30. Kodama T., Tomita N., Horie S., Sax N., Iwasaki H., Suzuki R., et al. Morphological study of acoustic liposomes using transmission electron microscopy. Journal of Electron Microscopy 2010, 59:187-196.
31. Kogure K., Akita H., Yamada Y., Harashima H. Multifunctional envelope-type nano device (MEND) as a non-viral gene delivery system. Advanced Drug Delivery Reviews 2008, 60:559-571.
32. Kudo N., Okada K., Yamamoto K. Sonoporation by single-shot pulsed ultrasound with microbubbles adjacent to cells. Biophysical Journal 2009, 96:4866-4876.
33. Lelouvier B., Puertollano R. Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway. The Journal of Biological Chemistry 2011, 286:9826-9832.
34. Lian T., Ho R.J. Trends and developments in liposome drug delivery systems. Journal of Pharmaceutical Sciences 2001, 90:667-680.
35. Lindner J.R. Microbubbles in medical imaging: current applications and future directions, Nature reviews. Drug Discovery 2004, 3:527-532.
36. Li T., Tachibana K., Kuroki M., Kuroki M. Gene transfer with echo-enhanced contrast agents: comparison between Albunex, Optison, and Levovist in mice-initial results. Radiology 2003, 229:423-428.
37. Liu F., Conwell C.C., Yuan X., Shollenberger L.M., Huang L. Novel nonviral vectors target cellular signaling pathways: regulated gene expression and reduced toxicity. The Journal of Pharmacology and Experimental Therapeutics 2007, 321:777-783.
38. Lu P.Y., Xie F., Woodle M.C. In vivo application of RNA interference: from functional genomics to therapeutics. Advances in Genetics 2005, 54:117-142.
39. Marshall E. Gene therapy death prompts review of adenovirus vector. Science (New York, N.Y.) 1999, 286:2244-2245.
40. Mayorga L.S., Beron W., Sarrouf M.N., Colombo M.I., Creutz C., Stahl P.D. Calcium-dependent fusion among endosomes. The Journal of Biological Chemistry 1994, 269:30927-30934.
41. McManus M.T., Sharp P.A. Gene silencing in mammals by small interfering RNAs,. Nature Reviews Genetics 2002, 3:737-747.
42. Miller M.W., Miller D.L., Brayman A.A. A review of in vitro bioeffects of inertial ultrasonic cavitation from a mechanistic perspective. Ultrasound in Medicine & Biology 1996, 22:1131-1154.
43. Mulvagh S.L., DeMaria A.N., Feinstein S.B., Burns P.N., Kaul S., Miller J.G., et al. Contrast echocardiography: current and future applications. Journal of the American Society of Echocardiography: Official Publication of the American Society of Echocardiography 2000, 13:331-342.
44. Nastala C.L., Edington H.D., McKinney T.G., Tahara H., Nalesnik M.A., Brunda M.J., et al. Recombinant IL-12 administration induces tumor regression in association with IFN-gamma production. Journal of Immunology 1994, 153:1697-1706. (Baltimore, Md.: 1950).
45. Negishi Y., Endo-Takahashi Y., Ishii K., Suzuki R., Oguri Y., Murakami T., et al. Development of novel nucleic acid-loaded bubble liposomes using cholesterol-conjugated siRNA. Journal of Drug Targeting 2011, 19:830-836.
46. Negishi Y., Endo-Takahashi Y., Matsuki Y., Kato Y., Takagi N., Suzuki R., et al. Systemic delivery systems of angiogenic gene by novel bubble liposomes containing cationic lipid and ultrasound exposure. Molecular Pharmaceutics 2012, 9:1834-1840.
47. Negishi Y., Endo Y., Fukuyama T., Suzuki R., Takizawa T., Omata D., et al. Delivery of siRNA into the cytoplasm by liposomal bubbles and ultrasound. Journal of Controlled Release: Official Journal of the Controlled Release Society 2008, 132:124-130.
48. Negishi Y., Omata D., Iijima H., Hamano N., Endo-Takahashi Y., Nomizu M., et al. Preparation and characterization of laminin-derived peptide AG73-coated liposomes as a selective gene delivery tool. Biological & Pharmaceutical Bulletin 2010, 33:1766-1769.
49. Negishi Y., Omata D., Iijima H., Takabayashi Y., Suzuki K., Endo Y., et al. Enhanced laminin-derived peptide AG73-mediated liposomal gene transfer by bubble liposomes and ultrasound. Molecular Pharmaceutics 2010, 7:217-226.
50. Nomizu M., Kim W.H., Yamamura K., Utani A., Song S.Y., Otaka A., et al. Identification of cell binding sites in the laminin alpha 1 chain carboxyl-terminal globular domain by systematic screening of synthetic peptides. The Journal of Biological Chemistry 1995, 270:20583-20590.
51. Omata D., Negishi Y., Hagiwara S., Yamamura S., Endo-Takahashi Y., Suzuki R., et al. Enhanced gene delivery using Bubble liposomes and ultrasound for folate-PEG liposomes. Journal of Drug Targeting 2012, 20:355-363.
52. Omata D., Negishi Y., Hagiwara S., Yamamura S., Endo-Takahashi Y., Suzuki R., et al. Bubble liposomes and ultrasound promoted endosomal escape of TAT-PEG liposomes as gene delivery carriers. Molecular Pharmaceutics 2011, 8:2416-2423.
53. Omata D., Negishi Y., Yamamura S., Hagiwara S., Endo-Takahashi Y., Suzuki R., et al. Involvement of Ca(2)(+) and ATP in enhanced gene delivery by bubble liposomes and ultrasound exposure. Molecular Pharmaceutics 2012, 9:1017-1023.
54. Pislaru S.V., Pislaru C., Kinnick R.R., Singh R., Gulati R., Greenleaf J.F., et al. Optimization of ultrasound-mediated gene transfer: comparison of contrast agents and ultrasound modalities. European Heart Journal 2003, 24:1690-1698.
55. Sadzuka Y., Nakade A., Hirama R., Miyagishima A., Nozawa Y., Hirota S., et al. Effects of mixed polyethyleneglycol modification on fixed aqueous layer thickness and antitumor activity of doxorubicin containing liposome. International Journal of Pharmaceutics 2002, 238:171-180.
56. Sioud M. RNA interference and innate immunity. Advanced Drug Delivery Reviews 2007, 59:153-163.
57. Sledz C.A., Holko M., de Veer M.J., Silverman R.H., Williams B.R. Activation of the interferon system by short-interfering RNAs. Nature Cell Biology 2003, 5:834-839.
58. van Solingen C., Seghers L., Bijkerk R., Duijs J.M., Roeten M.K., van Oeveren-Rietdijk A.M., et al. Antagomir-mediated silencing of endothelial cell specific microRNA-126 impairs ischemia-induced angiogenesis. Journal of Cellular and Molecular Medicine 2009, 13:1577-1585.
59. Soutschek J., Akinc A., Bramlage B., Charisse K., Constien R., Donoghue M., et al. Therapeutic silencing of an endogenous gene by systemic administration of modified siRNAs. Nature 2004, 432:173-178.
60. Suzuki R., Maruyama K. Effective in vitro and in vivo gene delivery by the combination of liposomal bubbles (bubble liposomes) and ultrasound exposure. Methods in Molecular Biology 2010, 605:473-486. (Clifton, N.J.).
61. Suzuki R., Namai E., Oda Y., Nishiie N., Otake S., Koshima R., et al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. Journal of Controlled Release: Official Journal of the Controlled Release Society 2010, 142:245-250.
62. Suzuki R., Oda Y., Utoguchi N., Namai E., Taira Y., Okada N., et al. A novel strategy utilizing ultrasound for antigen delivery in dendritic cell-based cancer immunotherapy. Journal of Controlled Release: Official Journal of the Controlled Release Society 2009, 133:198-205.
63. Suzuki R., Takizawa T., Kuwata Y., Mutoh M., Ishiguro N., Utoguchi N., et al. Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. International Journal of Pharmaceutics 2008, 346:143-150.
64. Suzuki R., Takizawa T., Negishi Y., Hagisawa K., Tanaka K., Sawamura K., et al. Gene delivery by combination of novel liposomal bubbles with perfluoropropane and ultrasound. Journal of Controlled Release: Official Journal of the Controlled Release Society 2007, 117:130-136.
65. Suzuki R., Takizawa T., Negishi Y., Utoguchi N., Maruyama K. Effective gene delivery with liposomal bubbles and ultrasound as novel non-viral system. Journal of Drug Targeting 2007, 15:531-537.
66. Suzuki R., Takizawa T., Negishi Y., Utoguchi N., Sawamura K., Tanaka K., et al. Tumor specific ultrasound enhanced gene transfer in vivo with novel liposomal bubbles. Journal of Controlled Release: Official Journal of the Controlled Release Society 2008, 125:137-144.
67. Takeuchi R., Ryo A., Komitsu N., Mikuni-Takagaki Y., Fukui A., Takagi Y., et al. Low-intensity pulsed ultrasound activates the phosphatidylinositol 3 kinase/Akt pathway and stimulates the growth of chondrocytes in three-dimensional cultures: a basic science study. Arthritis Research & Therapy 2008, 10:R77.
68. Taniyama Y., Tachibana K., Hiraoka K., Namba T., Yamasaki K., Hashiya N., et al. Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 2002, 105:1233-1239.
69. Unger E.C., Hersh E., Vannan M., Matsunaga T.O., McCreery T. Local drug and gene delivery through microbubbles. Progress in Cardiovascular Diseases 2001, 44:45-54.
70. Un K., Kawakami S., Suzuki R., Maruyama K., Yamashita F., Hashida M. Enhanced transfection efficiency into macrophages and dendritic cells by a combination method using mannosylated lipoplexes and bubble liposomes with ultrasound exposure. Human Gene Therapy 2010, 21:65-74.
71. Varga C.M., Tedford N.C., Thomas M., Klibanov A.M., Griffith L.G., Lauffenburger D.A. Quantitative comparison of polyethylenimine formulations and adenoviral vectors in terms of intracellular gene delivery processes. Gene Therapy 2005, 12:1023-1032.
72. van Wamel A., Kooiman K., Harteveld M., Emmer M., ten Cate F.J., Versluis M., et al. Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation. Journal of Controlled Release: Official Journal of the Controlled Release Society 2006, 112:149-155.
73. Wang S., Aurora A.B., Johnson B.A., Qi X., McAnally J., Hill J.A., et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Developmental Cell 2008, 15:261-271.
74. Wang Y., Li X., Zhou Y., Huang P., Xu Y. Preparation of nanobubbles for ultrasound imaging and intracelluar drug delivery. International Journal of Pharmaceutics 2010, 384:148-153.
75. Wells D.J. Electroporation and ultrasound enhanced non-viral gene delivery in vitro and in vivo. Cell Biology and Toxicology 2010, 26:21-28.
76. Wolfrum C., Shi S., Jayaprakash K.N., Jayaraman M., Wang G., Pandey R.K., et al. Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nature Biotechnology 2007, 25:1149-1157.
77. Yamashita T., Sonoda S., Suzuki R., Arimura N., Tachibana K., Maruyama K., et al. A novel bubble liposome and ultrasound-mediated gene transfer to ocular surface: RC-1 cells in vitro and conjunctiva in vivo. Experimental Eye Research 2007, 85:741-748.
78. Zhang Y., Wang Z., Gemeinhart R.A. Progress in microRNA delivery. Journal of Controlled Release: Official Journal of the Controlled Release Society 2013, 172:962-974.
79. Zhou Y., Shi J., Cui J., Deng C.X. Effects of extracellular calcium on cell membrane resealing in sonoporation. Journal of Controlled Release: Official Journal of the Controlled Release Society 2008, 126:34-43.