Microbubble Stability is a Major Determinant of the Efficiency of Ultrasound and Microbubble Mediated in vivo Gene Transfer

Ultrasound in Medicine and Biology

Volumn 35, Issue 6, 2009, Pages 976-984

  Alter, Julia ^a   Sennoga, Charles A ^a   Lopes, D M ^b   Eckersley, Robert J ^a   Wells, Dominic J ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b Div Neuroscience/Psychological Med   (United Kingdom)

Author keywords

DMD; Gene delivery; mdx; Microbubble; Ultrasound

Indexed keywords

DMD; GENE DELIVERY; MDX; MICROBUBBLE; ULTRASOUND;

ACOUSTIC WAVES; CONCENTRATION (PROCESS); GENES; NUCLEIC ACIDS; OLIGONUCLEOTIDES; ULTRASONIC IMAGING; ULTRASONIC TRANSMISSION; ULTRASONICS;

GENE TRANSFER;

ANTISENSE OLIGONUCLEOTIDE; GREEN FLUORESCENT PROTEIN LUCIFERASE; HYBRID PROTEIN; LUCIFERASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PERFLUBUTANE; PERFLUTREN; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER; PLASMID DNA; SONOVUE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ANALYSIS; DRUG DEGRADATION; DRUG SAFETY; DRUG STABILITY; DUCHENNE MUSCULAR DYSTROPHY; ENHANCER REGION; ENZYME ACTIVITY; GENE TRANSFER; HEART MUSCLE; IN VIVO STUDY; MICROBUBBLE; MICROBUBBLE ENHANCED GENE TRANSFER; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PARTICLE SIZE; PRIORITY JOURNAL; ULTRASOUND;

ALBUMINS; ANIMALS; CONTRAST MEDIA; DISEASE MODELS, ANIMAL; FERRIC COMPOUNDS; FLUOROCARBONS; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; IRON; MICE; MICE, INBRED MDX; MICROBUBBLES; MUSCULAR DYSTROPHY, DUCHENNE; OLIGONUCLEOTIDES, ANTISENSE; OXIDES; PARTICLE SIZE; PHOSPHOLIPIDS; PLASMIDS; SULFUR HEXAFLUORIDE; ULTRASONICS;

EID: 67349230291     PISSN: 03015629     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2008.12.015     Document Type: Article

References (37)

1. Alter J., Lou F., Rabinowitz A., Yin H., Rosenfeld J., Wilton S.D., Partridge T.A., and Lu Q.L. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 12 (2006) 175-177
2. Azuma H., Tomita N., Kaneda Y., Koike H., Ogihara T., Katsuoka Y., and Morishita R. Transfection of NFkappaB-decoy oligodeoxynucleotides using efficient ultrasound-mediated gene transfer into donor kidneys prolonged survival of rat renal allografts. Gene Ther 10 (2003) 415-425
3. Bekeredjian R., Chen S., Frenkel P.A., Grayburn P.A., and Shohet R.V. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 108 (2003) 1022-1026
4. Braide M., Rasmussen H., Albrektsson A., and Bagge U. Microvascular behavior and effects of sonazoid microbubbles in the cremaster muscle of rats after local administration. J Ultrasound Med 25 (2006) 883-890
5. Chamberlain J.S., Metzger J., Reyes M., Townsend D., and Faulkner J.A. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J 21 (2007) 2195-2204
6. Chen S., Ding J.H., Bekeredjian R., Yang B.Z., Shohet R.V., Johnston S.A., Hohmeier H.E., Newgard C.B., and Grayburn P.A. Efficient gene delivery to pancreatic islets with ultrasonic microbubble destruction technology. Proc Nat Acad Sci USA 22 (2006) 8469-8474
7. Chen S., Shohet R.V., Bekeredjian R., Frenkel P., and Grayburn P.A. Optimization of ultrasound parameters for cardiac gene delivery of adenoviral or plasmid deoxyribonucleic acid by ultrasound-targeted microbubble destruction. J Am Coll Cardiol 42 (2003) 301-308
8. Chomas J.E., Dayton P., Allen J., Morgan K., and Ferrara K.W. Mechanisms of contrast agent destruction. IEEE Trans Ultrason Ferroelectr Freq Control 48 (2001) 232-248
9. Dijkmans P.A., Juffermans L.J., Musters R.J., van Wamel A., ten Cate F.J., van Gilst W., Visser C.A., de Jong N., and Kamp O. Microbubbles and ultrasound: From diagnosis to therapy. Eur J Echocardiogr 5 (2004) 245-256
10. Duvshani-Eshet M., Adam D., and Machluf M. The effects of albumin-coated microbubbles in DNA delivery mediated by therapeutic ultrasound. J Control Release 112 (2006) 156-166
11. Duvshani-Eshet M., and Machluf M. Efficient transfection of tumors facilitated by long-term therapeutic ultrasound in combination with contrast agent: from in vitro to in vivo setting. Cancer Gene Ther 3 (2007) 306-315
12. Finsterer J. Cardiopulmonary support in duchenne muscular dystrophy. Lung 184 (2006) 205-215
13. Gebski B.L., Mann C.J., Fletcher S., and Wilton S.D. Morpholino antisense oligonucleotide induced dystrophin exon 23 skipping in mdx mouse muscle. Hum Mol Genet 12 (2003) 1801-1811
14. Guo D.P., Li X.Y., Sun P., Wang Z.G., Chen X.Y., Chen Q., Fan L.M., Zhang B., Shao L.Z., and Li X.R. Ultrasound/microbubble enhances foreign gene expression in ECV304 cells and murine myocardium. Acta Biochim Biophys Sin (Shanghai) 36 (2004) 824-831
15. Hallow D.M., Mahajan A.D., McCutchen T.E., and Prausnitz M.R. Measurement and correlation of acoustic cavitation with cellular bioeffects. Ultrasound Med Biol 32 (2006) 1111-1122
16. Hallow D.M., Mahajan A.D., and Prausnitz M.R. Ultrasonically targeted delivery into endothelial and smooth muscle cells in ex vivo arteries. J Control Release 118 (2007) 285-293
17. Hoffman E.P., Brown Jr. R.H., and Kunkel L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51 (1987) 919-928
18. Howard C.M., Forsberg F., Minimo C., Liu J.B., Merton D.A., and Claudio P.P. Ultrasound guided site specific gene delivery system using adenoviral vectors and commercial ultrasound contrast agents. J Cell Physiol 209 (2006) 413-421
19. Kondo I., Ohmori K., Oshita A., Takeuchi H., Fuke S., Shinomiya K., Noma T., Namba T., and Kohno M. Treatment of acute myocardial infarction by hepatocyte growth factor gene transfer: The first demonstration of myocardial transfer of a "functional" gene using ultrasonic microbubble destruction. J Am Coll Cardiol 44 (2004) 644-653
20. Krasovitski B., and Kimmel E. Stability of an encapsulated bubble shell. Ultrasonics 44 (2006) 216-220
21. Li T., Tachibana K., Kuroki M., and Kuroki M. Gene transfer with echo-enhanced contrast agents: Comparison between Albunex, Optison, and Levovist in mice-Initial results. Radiology 229 (2003) 423-428
22. Li X., Wang Z., Ran H., Li X., Yuan Q., Zheng Y., Ren J., Su L., Zhang W., Li Q., and Xu C. Experimental research on therapeutic angiogenesis induced by hepatocyte growth factor directed by ultrasound-targeted microbubble destruction in rats. J Ultrasound Med 27 (2008) 453-460
23. Lu Q.L., Liang H.D., Partridge T., and Blomley M.J. Microbubble ultrasound improves the efficiency of gene transduction in skeletal muscle in vivo with reduced tissue damage. Gene Ther 10 (2003) 396-405
24. Marmottant P., and Hilgenfeldt S. Controlled vesicle deformation and lysis by single oscillating bubbles. Nature 423 (2003) 153-156
25. Meijering B.D., Henning R.H., Van Gilst W.H., Gavrilovic I., Van Wamel A., and Deelman L.E. Optimization of ultrasound and microbubbles targeted gene delivery to cultured primary endothelial cells. J Drug Target 15 (2007) 664-671
26. Miao C.H., Brayman A.A., Loeb K.R., Ye P., Zhou L., Mourad P., and Crum L.A. Ultrasound enhances gene delivery of human factor IX plasmid. Hum Gene Ther 16 (2005) 893-905
27. Mukherjee D., Wong J., Griffin B., Ellis S.G., Porter T., Sen S., and Thomas J.D. Ten-fold augmentation of endothelial uptake of vascular endothelial growth factor with ultrasound after systemic administration. J Am Coll Cardiol 35 (2000) 1678-1686
28. Newman C.M., and Bettinger T. Gene therapy progress and prospects: Ultrasound for gene transfer. Gene Ther 14 (2007) 465-475
29. Rahim A., Taylor S.L., Bush N.L., ter Haar G.R., Bamber J.C., and Porter C.D. Physical parameters affecting ultrasound/microbubble-mediated gene delivery efficiency in vitro. Ultrasound Med Biol 32 (2006) 1269-1279
30. Sakakima Y., Hayashi S., Yagi Y., Hayakawa A., Tachibana K., and Nakao A. Gene therapy for hepatocellular carcinoma using sonoporation enhanced by contrast agents. Cancer Gene Ther 12 (2005) 884-889
31. Sicinski P., Geng Y., Ryder-Cook A.S., Barnard E.A., Darlison M.G., and Barnard P.J. The molecular basis of muscular dystrophy in the mdx mouse: A point mutation. Science 244 (1989) 1578-1580
32. Sonoda S., Tachibana K., Uchino E., Yamashita T., Sakoda K., Sonoda K.H., Hisatomi T., Izumi Y., and Sakamoto T. Inhibition of melanoma by ultrasound-microbubble-aided drug delivery suggests membrane permeabilization. Cancer Biol Ther 6 (2007) 1276-1283
33. Tachibana K., and Tachibana S. The use of ultrasound for drug delivery. Echocardiography 18 (2001) 323-328
34. Treat L.H., McDannold N., Vykhodtseva N., Zhang Y., Tam K., and Hynynen K. Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound. Int J Cancer 121 (2007) 901-907
35. Tsunoda S., Mazda O., Oda Y., Iida Y., Akabame S., Kishida T., Shin-Ya M., Asada H., Gojo S., Imanishi J., et al. Sonoporation using microbubble BR14 promotes pDNA/siRNA transduction to murine heart. Biochem Biophys Res Commun 336 (2005) 118-127
36. Unger E.C., McCreery T.P., Sweitzer R.H., Caldwell V.E., and Wu Y. Acoustically active lipospheres containing paclitaxel: A new therapeutic ultrasound contrast agent. Invest Radiol 33 (1998) 886-892
37. Wang X., Liang H.D., Dong B., Lu Q.L., and Blomley M.J. Gene transfer with microbubble ultrasound and plasmid DNA into skeletal muscle of mice: Comparison between commercially available microbubble contrast agents. Radiology 237 (2005) 224-229