Ultrasound in Medicine and Biology
Volume 36, Issue 3 , Pages 430-440 , March 2010

Sonoporation Mediated Immunogene Therapy of Solid Tumors

  • Garrett Casey

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • James P. Cashman

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • David Morrissey

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • Maria C. Whelan

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • John O. Larkin

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • Declan M. Soden

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • Mark Tangney

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
  • ,
  • Gerald C. O'Sullivan

      Affiliations

    • Cork Cancer Research Centre, Mercy University Hospital and Leslie C. Quick Jnr. Laboratory, BioScience Institute, University College Cork, Cork, Ireland
    • Department of Surgery, Mercy University Hospital, Grenville Place, Cork, Ireland
    • Corresponding Author InformationAddress correspondence to: Gerald C. O'Sullivan, Cork Cancer Research Centre, Mercy University Hospital, Grenville Place, Cork, Ireland.

Received 6 March 2009 ,Revised 12 November 2009 ,Accepted 12 November 2009.

References 

  1. Al-Dosari M, Zhang G, Knapp JE, Liu D. Evaluation of viral and mammalian promoters for driving transgene expression in mouse liver. Biochem Biophys Res Commun. 2006;339:673–678
  2. Andre F, Mir LM. DNA electrotransfer: Its principles and an updated review of its therapeutic applications. Gene Ther. 2004;11(Suppl 1):S33–S42
  3. Bao S, Thrall BD, Miller DL. Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med Biol. 1997;23:953–959
  4. Collins CG, Tangney M, Larkin JO, Casey G, Whelan MC, Cashman J, et al. Local gene therapy of solid tumors with GM-CSF and B7-1 eradicates both treated and distal tumors. Cancer Gene Ther. 2006;13:1061–1071
  5. Craig R, Cutrera J, Zhu S, Xia X, Lee YH, Li S. Administering plasmid DNA encoding tumor vessel-anchored IFN-alpha for localizing gene product within or into tumors. Mol Ther. 2008;16:901–906
  6. Dean DA, Machado-Aranda D, Blair-Parks K, Yeldandi AV, Young JL. Electroporation as a method for high-level nonviral gene transfer to the lung. Gene Ther. 2003;10:1608–1615
  7. Duvshani-Eshet M, Benny O, Morgenstern A, Machluf M. Therapeutic ultrasound facilitates antiangiogenic gene delivery and inhibits prostate tumor growth. Mol Cancer Ther. 2007;6:2371–2382
  8. Duvshani-Eshet M, Machluf M. Therapeutic ultrasound optimization for gene delivery: A key factor achieving nuclear DNA localization. J Control Release. 2005;108:513–528
  9. Duvshani-Eshet M, 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. 2007;14:306–315
  10. Haar GT, Coussios C. High intensity focused ultrasound: Physical principles and devices. Int J Hyperthermia. 2007;23:89–104
  11. Hauff P, Seemann S, Reszka R, Schultze-Mosgau M, Reinhardt M, Buzasi T, et al. Evaluation of gas-filled microparticles and sonoporation as gene delivery system: Feasibility study in rodent tumor models. Radiology. 2005;236:572–578
  12. Hayashi S, Mizuno M, Yoshida J, Nakao A. Effect of sonoporation on cationic liposome-mediated IFNbeta gene therapy for metastatic hepatic tumors of murine colon cancer. Cancer Gene Ther. 2009;16:638–643
  13. Heller L, Pottinger C, Jaroszeski MJ, Gilbert R, Heller R. In vivo electroporation of plasmids encoding GM-CSF or interleukin-2 into existing B16 melanomas combined with electrochemotherapy induces long-term antitumour immunity. Melanoma Res. 2000;10:577–583
  14. Herweijer H, Zhang G, Subbotin VM, Budker V, Williams P, Wolff JA. Time course of gene expression after plasmid DNA gene transfer to the liver. J Gene Med. 2001;3:280–291
  15. Huber PE, Pfisterer P. In vitro and in vivo transfection of plasmid DNA in the Dunning prostate tumor R3327-AT1 is enhanced by focused ultrasound. Gene Ther. 2000;7:1516–1525
  16. Koike H, Tomita N, Azuma H, Taniyama Y, Yamasaki K, Kunugiza Y, et al. An efficient gene transfer method mediated by ultrasound and microbubbles into the kidney. J Gene Med. 2005;7:108–116
  17. Larkin JO, Casey GD, Tangney M, Cashman J, Collins CG, Soden DM, et al. Effective tumor treatment using optimized ultrasound-mediated delivery of bleomycin. Ultrasound Med Biol. 2008;34:406–413
  18. Larkin JO, Collins CG, Aarons S, Tangney M, Whelan M, O'Reily S, et al. Electrochemotherapy: Aspects of preclinical development and early clinical experience. Ann Surg. 2007;245:469–479
  19. 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
  20. Lechardeur D, Verkman AS, Lukacs GL. Intracellular routing of plasmid DNA during non-viral gene transfer. Adv Drug Deliv Rev. 2005;57:755–767
  21. Li Y, Han W, Zhang Y, Yuan L, Shi X, Yu Y, et al. Intramuscular electroporation of a plasmid encoding human plasminogen kringle 5 induces growth inhibition of Lewis lung carcinoma in mice. Cancer Biother Radiopharm. 2008;23:332–341
  22. Liang HD, Lu QL, Xue SA, Halliwell M, Kodama T, Cosgrove DO, et al. Optimisation of ultrasound-mediated gene transfer (sonoporation) in skeletal muscle cells. Ultrasound Med Biol. 2004;30:1523–1529
  23. Lu QL, Liang HD, Partridge T, Blomley MJ. Microbubble ultrasound improves the efficiency of gene transduction in skeletal muscle in vivo with reduced tissue damage. Gene Ther. 2003;10:396–405
  24. Madersbacher S, Marberger M. High-energy shockwaves and extracorporeal high-intensity focused ultrasound. J Endourol. 2003;17:667–672
  25. Manome Y, Nakamura M, Ohno T, Furuhata H. Ultrasound facilitates transduction of naked plasmid DNA into colon carcinoma cells in vitro and in vivo. Hum Gene Ther. 2000;11:1521–1528
  26. Marberger M, Carroll PR, Zelefsky MJ, Coleman JA, Hricak H, Scardino PT, et al. New treatments for localized prostate cancer. Urology. 2008;72:S36–S43
  27. Matsubara H, Gunji Y, Maeda T, Tasaki K, Koide Y, Asano T, et al. Electroporation-mediated transfer of cytokine genes into human esophageal tumors produces anti-tumor effects in mice. Anticancer Res. 2001;21:2501–2503
  28. McMahon JM, Wells KE, Bamfo JE, Cartwright MA, Wells DJ. Inflammatory responses following direct injection of plasmid DNA into skeletal muscle. Gene Ther. 1998;5:1283–1290
  29. Mehier-Humbert S, Bettinger T, Yan F, Guy RH. Ultrasound-mediated gene delivery: Kinetics of plasmid internalization and gene expression. J Control Release. 2005;104:203–211
  30. Mehier-Humbert S, Guy RH. Physical methods for gene transfer: Improving the kinetics of gene delivery into cells. Adv Drug Deliv Rev. 2005;57:733–753
  31. Mir LM. Electrochemotherapy. Eur J Cancer Suppl. 2006;4:1–60
  32. Mitragotri S. Healing sound: The use of ultrasound in drug delivery and other therapeutic applications. Nat Rev Drug Discov. 2005;4:255–260
  33. Murat FJ, Poissonnier L, Pasticier G, Gelet A. High-intensity focused ultrasound (HIFU) for prostate cancer. Cancer Control. 2007;14:244–249
  34. Newman CM, Bettinger T. Gene therapy progress and prospects: Ultrasound for gene transfer. Gene Ther. 2007;14:465–475
  35. Roux S, Bernat C, Al-Sakere B, Ghiringhelli F, Opolon P, Carpentier AF, et al. Tumor destruction using electrochemotherapy followed by CpG oligodeoxynucleotide injection induces distant tumor responses. Cancer Immunol Immunother. 2008;57:1291–1300
  36. Sacher T, Knolle P, Nichterlein T, Arnold B, Hammerling GJ, Limmer A. CpG-ODN-induced inflammation is sufficient to cause T-cell-mediated autoaggression against hepatocytes. Eur J Immunol. 2002;32:3628–3637
  37. Sakakima Y, Hayashi S, Yagi Y, Hayakawa A, Tachibana K, Nakao A. Gene therapy for hepatocellular carcinoma using sonoporation enhanced by contrast agents. Cancer Gene Ther. 2005;12:884–889
  38. Sheyn D, Kimelman-Bleich N, Pelled G, Zilberman Y, Gazit D, Gazit Z. Ultrasound-based nonviral gene delivery induces bone formation in vivo. Gene Ther. 2008;15:257–266
  39. 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
  40. ter Haar G. Therapeutic ultrasound. Eur J Ultrasound. 1999;9:3–9
  41. ter Haar G. Therapeutic applications of ultrasound. Prog Biophys Mol Biol. 2007;93:111–129
  42. van Wamel A, Kooiman K, Harteveld M, Emmer M, ten Cate FJ, Versluis M, et al. Vibrating microbubbles poking individual cells: Drug transfer into cells via sonoporation. J Control Release. 2006;112:149–155
  43. Wei W, Zheng-zhong B, Yong-jie W, Qing-wu Z, Ya-lin M. Bioeffects of low-frequency ultrasonic gene delivery and safety on cell membrane permeability control. J Ultrasound Med. 2004;23:1569–1582
  44. Wells DJ. Gene therapy progress and prospects: Electroporation and other physical methods. Gene Ther. 2004;11:1363–1369
  45. Wilke M, Fortunati E, van den Broek M, Hoogeveen AT, Scholte BJ. Efficacy of a peptide-based gene delivery system depends on mitotic activity. Gene Ther. 1996;3:1133–1142
  46. Zarnitsyn VG, Prausnitz MR. Physical parameters influencing optimization of ultrasound-mediated DNA transfection. Ultrasound Med Biol. 2004;30:527–538

PII: S0301-5629(09)01625-1

doi: 10.1016/j.ultrasmedbio.2009.11.005

Ultrasound in Medicine and Biology
Volume 36, Issue 3 , Pages 430-440 , March 2010