Cationic versus neutral microbubbles for ultrasound-mediated gene delivery in cancer

Radiology

Volumn 264, Issue 3, 2012, Pages 721-732

  Wang, David S ^a   Panje, Cedric ^a   Pysz, Marybeth A ^a   Paulmurugan, Ramasamy ^a   Rosenberg, Jarrett ^a   Gambhir, Sanjiv S ^a   Schneider, Michel ^b   Willmann, Jürgen K ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Bracco Suisse SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; DEOXYRIBONUCLEASE; LUCIFERASE; PLASMID DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLUMINESCENCE; CANCER GENE THERAPY; CATIONIC MICROBUBBLE; CELL CULTURE; CONTROLLED STUDY; DNA BINDING; ENDOTHELIUM CELL; EX VIVO STUDY; FEMALE; GENE DELIVERY SYSTEM; GENE EXPRESSION; HINDLIMB; IN VIVO STUDY; LIMB TUMOR; MICROBUBBLE; MOUSE; NEUTRAL MICROBUBBLE; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; ULTRASOUND;

ANALYSIS OF VARIANCE; ANIMALS; CATIONS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HINDLIMB; LUCIFERASES; LUMINESCENT MEASUREMENTS; MICE; MICE, NUDE; MICROBUBBLES; NEOPLASMS; PLASMIDS; POLYMERASE CHAIN REACTION; ULTRASONICS;

EID: 84865423296     PISSN: 00338419     EISSN: 15271315     Source Type: Journal    
DOI: 10.1148/radiol.12112368     Document Type: Article

References (42)

1. Miller DL, Pislaru SV, Greenleaf JE. Sonoporation: mechanical DNA delivery by ultrasonic cavitation. Somat Cell Mol Genet 2002;27(1-6):115-134.
2. Tachibana K, Uchida T, Ogawa K, Yamashita N, Tamura K. Induction of cellmembrane porosity by ultrasound. Lancet 1999;353(9162):1409.
3. Brayman AA, Coppage ML, Vaidya S, Miller MW. Transient poration and cell surface receptor removal from human lymphocytes in vitro by 1 MHz ultrasound. Ultrasound Med Biol 1999;25(6):999-1008.
4. 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 Ther 2006;13(2):163-172.
5. Kimmel E. Cavitation bioeffects. Crit Rev Biomed Eng 2006;34(2):105-161.
6. Schlicher RK, Radhakrishna H, Tolentino TP, Apkarian RP, Zarnitsyn V, Prausnitz MR. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med Biol 2006;32(6):915-924.
7. Collis J, Manasseh R, Liovic P, et al. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics 2010;50(2):273-279.
8. Nyborg WL. Ultrasonic microstreaming and related phenomena. Br J Cancer Suppl 1982;5:156-160.
9. Greenleaf WJ, Bolander ME, Sarkar G, Goldring MB, Greenleaf JF. Artificial cavitation nuclei significantly enhance acoustically induced cell transfection. Ultrasound Med Biol 1998;24(4):587-595.
10. Liang HD, Lu QL, Xue SA, et al. Optimisation of ultrasound-mediated gene transfer (sonoporation) in skeletal muscle cells. Ultrasound Med Biol 2004;30(11):1523-1529.
11. Kim HJ, Greenleaf JF, Kinnick RR, Bronk JT, Bolander ME. Ultrasound-mediated transfection of mammalian cells. Hum Gene Ther 1996;7(11):1339-1346.
12. Meijering BD, Henning RH, Van Gilst WH, Gavrilovic I, Van Wamel A, Deelman LE. Optimization of ultrasound and microbubbles targeted gene delivery to cultured primary endothelial cells. J Drug Target 2007;15(10):664-671.
13. Carson AR, McTiernan CF, Lavery L, et al. Gene therapy of carcinoma using ultrasound-targeted microbubble destruction. Ultrasound Med Biol 2011;37(3):393-402.
14. Christiansen JP, French BA, Klibanov AL, Kaul S, Lindner JR. Targeted tissue transfection with ultrasound destruction of plasmid-bearing cationic microbubbles. Ultrasound Med Biol 2003;29(12):1759-1767.
15. Chen S, Ding JH, Bekeredjian R, et al. Efficient gene delivery to pancreatic islets with ultrasonic microbubble destruction technology. Proc Natl Acad Sci U S A 2006;103(22):8469-8474.
16. Li YS, Davidson E, Reid CN, McHale AP. Optimising ultrasound-mediated gene transfer (sonoporation) in vitro and prolonged expression of a transgene in vivo: potential applications for gene therapy of cancer. Cancer Lett 2009;273(1):62-69.
17. Bekeredjian R, Chen S, Frenkel PA, Grayburn PA, Shohet RV. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 2003;108(8):1022-1026.
18. Shohet RV, Chen S, Zhou YT, et al. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 2000;101(22):2554-2556.
19. Ferrara K, Pollard R, Borden M. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng 2007;9:415-447.
20. Liang HD, Tang J, Halliwell M. Sonoporation, drug delivery, and gene therapy. Proc Inst Mech Eng H 2010;224(2):343-361.
21. Luo D, Saltzman WM. Enhancement of transfection by physical concentration of DNA at the cell surface. Nat Biotechnol 2000;18(8):893-895.
22. Lentacker I, De Geest BG, Vandenbroucke RE, et al. Ultrasound-responsive polymer-coated microbubbles that bind and protect DNA. Langmuir 2006;22(17):7273-7278.
23. Frenkel PA, Chen S, Thai T, Shohet RV, Grayburn PA. DNA-loaded albumin microbubbles enhance ultrasound-mediated transfection in vitro. Ultrasound Med Biol 2002;28(6):817-822.
24. Tinkov S, Bekeredjian R, Winter G, Coester C. Microbubbles as ultrasound triggered drug carriers. J Pharm Sci 2009;98(6):1935-1961.
25. Hernot S, Klibanov AL. Microbubbles in ultrasound-triggered drug and gene delivery. Adv Drug Deliv Rev 2008;60(10):1153-1166.
26. Leong-Poi H, Kuliszewski MA, Lekas M, et al. Therapeutic arteriogenesis by ultrasound-mediated VEGF165 plasmid gene delivery to chronically ischemic skeletal muscle. Circ Res 2007;101(3):295-303.
27. Vannan M, McCreery T, Li P, et al. Ultrasound-mediated transfection of canine myocardium by intravenous administration of cationic microbubble-linked plasmid DNA. J Am Soc Echocardiogr 2002;15(3):214-218.
28. Borden MA, Caskey CF, Little E, Gillies RJ, Ferrara KW. DNA and polylysine adsorption and multilayer construction onto cationic lipid-coated microbubbles. Langmuir 2007;23(18):9401-9408.
29. Haag P, Frauscher F, Gradl J, et al. Micro-bubble-enhanced ultrasound to deliver an antisense oligodeoxynucleotide targeting the human androgen receptor into prostate tumours. J Steroid Biochem Mol Biol 2006;102(1-5):103-113.
30. Tlaxca JL, Anderson CR, Klibanov AL, et al. Analysis of in vitro transfection by sonoporation using cationic and neutral microbubbles. Ultrasound Med Biol 2010;36(11):1907-1918.
31. Ray P, Gambhir SS. Noninvasive imaging of molecular events with bioluminescent reporter genes in living subjects. Methods Mol Biol 2007;411:131-144.
32. Willmann JK, Cheng Z, Davis C, et al. Targeted microbubbles for imaging tumor angiogenesis: assessment of whole-body biodistribution with dynamic micro-PET in mice. Radiology 2008;249(1):212-219.
33. Perkins AC, Frier M, Hindle AJ, et al. Human biodistribution of an ultrasound contrast agent (Quantison) by radiolabelling and gamma scintigraphy. Br J Radiol 1997;70(834):603-611.
34. Girden ER. ANOVA: repeated measures. Thousand Oaks, Calif: Sage, 1991.
35. Glover DJ, Lipps HJ, Jans DA. Towards safe, non-viral therapeutic gene expression in humans. Nat Rev Genet 2005;6(4):299-310.
36. Newman CM, Bettinger T. Gene therapy progress and prospects: ultrasound for gene transfer. Gene Ther 2007;14(6):465-475.
37. Otani K, Yamahara K, Ohnishi S, Obata H, Kitamura S, Nagaya N. Nonviral delivery of siRNA into mesenchymal stem cells by a combination of ultrasound and microbubbles. J Control Release 2009;133(2):146-153.
38. Nomikou N, Tiwari P, Trehan T, Gulati K, McHale AP. Studies on neutral, cationic and biotinylated cationic microbubbles in enhancing ultrasound-mediated gene delivery in vitro and in vivo. Acta Biomater 2012;8(3):1273-1280.
39. Houk BE, Hochhaus G, Hughes JA. Kinetic modeling of plasmid DNA degradation in rat plasma. AAPS PharmSci 1999;1(3):E9.
40. Liu F, Shollenberger LM, Conwell CC, Yuan X, Huang L. Mechanism of naked DNA clearance after intravenous injection. J Gene Med 2007;9(7):613-619.
41. Koike H, Tomita N, Azuma H, et al. An efficient gene transfer method mediated by ultrasound and microbubbles into the kidney. J Gene Med 2005;7(1):108-116.
42. Willmann JK, Paulmurugan R, Chen K, et al. US imaging of tumor angiogenesis with microbubbles targeted to vascular endothelial growth factor receptor type 2 in mice. Radiology 2008;246(2):508-518.