Ultrasound in Medicine and Biology
Volume 36, Issue 9 , Pages 1470-1480 , September 2010

Targeted Gene Transfection from Microbubbles into Vascular Smooth Muscle Cells Using Focused, Ultrasound-Mediated Delivery

  • Linsey C. Phillips

      Affiliations

    • Department of Biomedical Engineering, University of Virginia, Charlottesville, VA
    • ,
  • Alexander L. Klibanov

      Affiliations

    • Department of Medicine, Cardiovascular Division, University of Virginia, Charlottesville, VA
    • ,
  • Brian R. Wamhoff

      Affiliations

    • Department of Medicine, Cardiovascular Division, University of Virginia, Charlottesville, VA
    • Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, VA
    • Contributed equally to the work.
    • ,
  • John A. Hossack

      Affiliations

    • Department of Biomedical Engineering, University of Virginia, Charlottesville, VA
    • Contributed equally to the work.
    • Corresponding Author InformationAddress correspondence to: John A. Hossack, Dept. of Biomedical Engineering, 415 Lane Road, MR5 Bldg., PO Box 800759, Charlottesville, VA 22908.

Received 28 January 2010 ,Revised 27 May 2010 ,Accepted 12 June 2010.

References 

  1. Anwer K, Kao G, Proctor B, Anscombe I, Florack V, Earls R, et al. Ultrasound enhancement of cationic lipid-mediated gene transfer to primary tumors following systemic administration. Gene Ther. 2000;7:1833–1839
  2. Byrne RA, Sarafoff N, Kastrati A, Schmig A. Drug-eluting stents in percutaneous coronary intervention: A benefit-risk assessment. Drug Safety. 2009;32:749–770
  3. Camenzind E, Steg PG, Wijns W. Stent thrombosis late after implantation of first-generation drug-eluting stents—a cause for concern. Circulation. 2007;115:1440–1455
  4. Chomas J, Dayton P, Morgan K, Allen J, Ferrara K. Optimization of microbubble destruction. IEEE Ultrasonics Symposium, 1999 Proceedings. 1999;2:1689–1692
  5. 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;29:1759–1767
  6. Clowes AW, Reidy MA, Clowes MM. Mechanisms of stenosis after arterial injury. Lab Invest. 1983;49:208–215
  7. Dayton PA, Morgan KE, Klibanov AL, Brandenburger GH, Ferrara KW. Optical and acoustical observations of the effects of ultrasound on contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control. 1999;46:220–232
  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 Ther. 2006;13:163–172
  9. Eisenstein EL, Anstrom KJ, Kong DF, Shaw LK, Tuttle RH, Mark DB, et al. Clopidogrel use and long-term clinical outcomes after drug-eluting stent implantation. JAMA. 2007;297:159–168
  10. Feril LB, Ogawa R, Tachibana K, Kondo T. Optimized ultrasound-mediated gene transfection in cancer cells. Cancer Sci. 2006;97:1111–1114
  11. Ferrara K, Pollard R, Bordeni M. Ultrasound microbubble contrast agents: Fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng. 2007;9:415–447
  12. Greenleaf WJ, Bolander ME, Sarkar G, Goldring MB, Greenleaf JF. Artificial cavitation nuclei significantly enhance acoustically induced cell transfection. Ultrasound Med Biol. 1998;24:587–595
  13. Guzman HR, Nguyen DX, Khan S, Prausnitz MR. Ultrasound-mediated disruption of cell membranes. I. Quantification of molecular uptake and cell viability. J Acoust Soc Am. 2001;110:588–596
  14. Guzman HR, Nguyen DX, Khan S, Prausnitz MR. Ultrasound-mediated disruption of cell membranes. II. Heterogeneous effects on cells. J Acoust Soc Am. 2001;110:597–606
  15. Karshafian R, Bevan PD, Williams R, Samac S, Burns PN. Sonoporation by ultrasound-activated microbubble contrast agents: Effect of acoustic exposure parameters on cell membrane permeability and cell viability. Ultrasound Med Biol. 2009;35:847–860
  16. Kim HJ, Greenleaf JF, Kinnick RR, Bronk JT, Bolander ME. Ultrasound-mediated transfection of mammalian cells. Human Gene Ther. 1996;7:1339–1346
  17. Kinoshita M, Hynynen K. Key factors that affect sonoporation efficiency in in vitro settings: The importance of standing wave in sonoporation. Biochem Biophys Res Commun. 2007;359:860–865
  18. Lawrie A, Brisken AF, Francis SE, Cumberland DC, Crossman DC, Newman CM. Microbubble-enhanced ultrasound for vascular gene delivery. Gene Ther. 2000;7:2023–2027
  19. Mayer CR, Bekeredjian R. Ultrasonic gene and drug delivery to the cardiovascular system. Adv Drug Del Rev. 2008;60:1177–1192
  20. Meijering BDM, 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;15:664–671
  21. Meijering BDM, Juffermans LJM, van Wamel A, Henning RH, Zuhorn IS, Emmer M, et al. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ Res. 2009;104:679–687
  22. Miller DL, Dou CY, Song JM. DNA transfer and cell killing in epidermoid cells by diagnostic ultrasound activation of contrast agent gas bodies in vitro. Ultrasound Med Biol. 2003;29:601–607
  23. Orr AW, Lee MY, Lemmon JA, Yurdagul A, Gomez MF, Schoppee Bortz PD, et al. Molecular mechanisms of collagen isotype-specific modulation of smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol. 2009;29:225–231
  24. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767–801
  25. Phillips LC, Klibanov AL, Bowles DK, Ragosta M, Hossack JA, Wamhoff BR. Focused in vivo delivery of plasmid DNA to the porcine vascular wall via intravascular ultrasound destruction of microbubbles. J Vasc Res. 2010;47:270–274
  26. Phillips PJ. Contrast pulse sequences (CPS): Imaging nonlinear microbubbles. IEEE Ultrasonics Symposium, 2001 Proceedings. 2001;2:1739–1745
  27. Rahim A, Taylor SL, Bush NL, Ter Haar GR, Bamber JC, Porter CD. Physical parameters affecting ultrasound/microbubble-mediated gene delivery efficiency in vitro. Ultrasound Med Biol. 2006;32:1269–1279
  28. Rahim AA, Taylor SL, Bush NL, ter Haar GR, Bamber JC, Porter CD. Spatial and acoustic pressure dependence of microbubble-mediated gene delivery targeted using focused ultrasound. J Gene Med. 2006;8:1347–1357
  29. Ren JL, Wang ZG, Zhang Y, Zheng YY, Li XS, Zhang QX, et al. Transfection efficiency of TDL compound in Huvec enhanced by ultrasound-targeted microbubble destruction. Ultrasound Med Biol. 2008;34:1857–1867
  30. Ruysschaert JM, Elouahabi A, Willeaume V, Huez G, Fuks R, Vandenbranden M, et al. A novel cationic ampiphile for transfection of mammalian-cells. Biochem Biophys Res Commun. 1994;203:1622–1628
  31. Shi WT, Forsberg F, Vaidyanathan P, Tornes A, Ostensen J, Goldberg BB. The influence of acoustic transmit parameters on the destruction of contrast microbubbles in vitro. Phys Med Biol. 2006;51:4031–4045
  32. Shin-Yuan S, Wen-Shiang C, Chih-Kuang Y. P2B-8 effect of acoustic insonation parameters on ultrasonic contrast agents destruction. IEEE Ultrasonics Symposium, 2006 Proceedings. 2006;1600–1603
  33. 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
  34. Tsai KC, Fang SY, Yang SJ, Shieh MJ, Lin WL, Chen WS. Time dependency of ultrasound-facilitated gene transfection. J Gene Med. 2009;11:729–736
  35. Unger EC, Hersh E, Vannan M, Matsunaga TO, McCreery M. Local drug and gene delivery through microbubbles. Progr Cardiovasc Dis. 2001;44:45–54
  36. Unger EC, McCreery TP, Sweitzer RH. Ultrasound enhances gene expression of liposomal transfection. Invest Radiol. 1997;32:723–727
  37. Unger EC, Porter T, Culp W, Labell R, Matsunaga T, Zutshi R. Therapeutic applications of lipid-coated microbubbles. Adv Drug Del Rev. 2004;56:1291–1314
  38. Wu JR, Ross JP, Chiu JF. Reparable sonoporation generated by microstreaming. J Acoust Soc Am. 2002;111:1460–1464
  39. Zarnitsyn VG, Prausnitz MR. Physical parameters influencing optimization of ultrasound-mediated DNA transfection. Ultrasound Med Biol. 2004;30:527–538

PII: S0301-5629(10)00301-7

doi: 10.1016/j.ultrasmedbio.2010.06.010

Ultrasound in Medicine and Biology
Volume 36, Issue 9 , Pages 1470-1480 , September 2010

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