Mechanisms of Microbubble-Facilitated Sonoporation for Drug and Gene Delivery

References

• Klibanov AL . Microbubble contrast agents: targeted ultrasound imaging and ultrasound-assisted drug-delivery applications . Invest. Radiol.41 ( 3 ), 354 – 362 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Kaufmann BA Lindner JR . Molecular imaging with targeted contrast ultrasound . Curr. Opin. Biotechnol.18 ( 1 ), 11 – 16 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Price RJ Skyba DM Kaul S Skalak TC . Delivery of colloidal particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound . Circulation98 ( 13 ), 1264 – 1267 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Miller DL Quddus J . Sonoporation of monolayer cells by diagnostic ultrasound activation of contrast-agent gas bodies . Ultrasound Med. Biol.26 ( 4 ), 661 – 667 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Phillips LC Klibanov AL Wamhoff BR Hossack JA . Targeted gene transfection from microbubbles into vascular smooth muscle cells using focused, ultrasound-mediated delivery . Ultrasound Med. Biol.36 ( 9 ), 1470 – 1480 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Xie A Belcik T Qi Y et al. Ultrasound-mediated vascular gene transfection by cavitation of endothelial-targeted cationic microbubbles . JACC Cardiovasc. Imaging5 ( 12 ), 1253 – 1262 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Husseini GA Pitt WG . Micelles and nanoparticles for ultrasonic drug and gene delivery . Adv. Drug Deliv. Rev.60 ( 10 ), 1137 – 1152 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Prentice P Cuschieri A Dholakia K Prausnitz M Campbell P . Membrane disruption by optically controlled microbubble cavitation . Nat. Phy.1 ( 2 ), 107 ( 2005 ).
   Web of Science ®Google Scholar
• Schlicher RK Radhakrishna H Tolentino TP Apkarian RP Zarnitsyn V Prausnitz MR . Mechanism of intracellular delivery by acoustic cavitation . Ultrasound Med. Biol.32 ( 6 ), 915 – 924 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Fan Z Kumon RE Park J Deng CX . Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles . J. Control. Release142 ( 1 ), 31 – 39 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Leighton TG . The Acoustic Bubble.Academic Press , San Diego, CA, USA . ( 1994 ).
   Google Scholar
• Qin S Caskey CF Ferrara KW . Ultrasound contrast microbubbles in imaging and therapy: physical principles and engineering . Phys. Med. Biol.54 ( 6 ), R27 – R57 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Ferrara K Pollard R Borden M . Ultrasound microbubble contrast agents: Fundamentals and application to gene and drug delivery . Annu. Rev. Biomed. Eng.9 , 415 – 447 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Kaul S . Myocardial contrast echocardiography: a 25-year retrospective . Circulation118 ( 3 ), 291 – 308 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Borden MA Longo M . Dissolution behavior of lipid monolayer-coated, air-filled microbubbles: effect of lipid hydrophobic chain length . Langmuir18 , 9225 – 9233 ( 2002 ).
   Web of Science ®Google Scholar
• Goertz DE De Jong N Van der Steen AF . Attenuation and size distribution measurements of Definity and manipulated Definity populations . Ultrasound Med. Biol.33 ( 9 ), 1376 – 1388 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Klibanov AL . Preparation of targeted microbubbles: ultrasound contrast agents for molecular imaging . Med. Biol. Eng. Comput.47 ( 8 ), 875 – 882 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Ferrara KW Borden MA Zhang H . Lipid-shelled vehicles: engineering for ultrasound molecular imaging and drug delivery . Acc. Chem. Res.42 ( 7 ), 881 – 892 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Delalande A Kotopoulis S Rovers T Pichon C Postema M . Sonoporation at a low mechanical indiex . Bubble Sci. Engin. Technol.3 , 3 – 11 ( 2011 ).
   Google Scholar
• Marmottant P Hilgenfeldt S . Controlled vesicle deformation and lysis by single oscillating bubbles . Nature423 ( 6936 ), 153 – 156 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Longuet-Higgins MS . Viscous streaming from an oscillating spherical bubble . Proc. R. Soc. London A454 , 725 – 742 ( 1998 ).
   Web of Science ®Google Scholar
• Wu J . Shear stress in cells generated by ultrasound . Prog. Biophys. Mol. Biol.93 ( 1–3 ), 363 – 373 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Van Bavel E . Effects of shear stress on endothelial cells: possible relevance for ultrasound applications . Prog. Biophys. Mol. Biol.93 ( 1–3 ), 374 – 383 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Crum LA Roy RA . Sonoluminescence . Science266 ( 5183 ), 233 – 234 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• Miller DL Thomas RM . Ultrasound contrast agents nucleate inertial cavitation in vitro . Ultrasound Med. Biol.21 ( 8 ), 1059 – 1065 ( 1995 ).
   PubMed Web of Science ®Google Scholar
• Miller MW Miller DL Brayman AA . A review of in vitro bioeffects of inertial ultrasonic cavitation from a mechanistic perspective . Ultrasound Med. Biol.22 ( 9 ), 1131 – 1154 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Lauterborn W Ohl CD . Cavitation bubble dynamics . Ultrason. Sonochem.4 ( 2 ), 65 – 75 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Sundaram J Mellein BR Mitragotri S . An experimental and theoretical analysis of ultrasound-induced permeabilization of cell membranes . Biophys. J.84 ( 5 ), 3087 – 3101 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Hallow DM Mahajan AD McCutchen TE Prausnitz MR . Measurement and correlation of acoustic cavitation with cellular bioeffects . Ultrasound Med. Biol.32 ( 7 ), 1111 – 1122 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Zhou Y Cui J Deng CX . Dynamics of sonoporation correlated with acoustic cavitation activities . Biophys. J.94 ( 7 ), L51 – 53 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Husseini GA Diaz de la Rosa MA Richardson ES Christensen DA Pitt WG . The role of cavitation in acoustically activated drug delivery . J. Control. Release107 ( 2 ), 253 – 261 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Benjamin TB Ellis AT . The collapse of cavitation bubbles and the pressures thereby produced against solid boundaries . Phil. Trans. Roy. Soc.A260 , 221 – 240 . ( 1966 ).
   Google Scholar
• Lauterborn W Bolle H . Experimental investigation of cavitation-bubble collapse in the neighbourhood of a solid boundary . J. Fluid. Mech.72 , 391 – 399 ( 1975 ).
   Web of Science ®Google Scholar
• Prosperetti A . Bubble phenomena in sound fields: part 2 . Ultrasonics22 , 115 – 124 ( 1984 ).
   Google Scholar
• Plesset MS Chapman RB . Collapse of an initially spherical vapour cavity in the neighbourhood of a solid boundary . J. Fluid. Mech.47 , 283 – 290 ( 1971 ).
   Web of Science ®Google Scholar
• Tomita Y Shima A . Mechanisms of impulsive pressure generation and damage pit formation by bubble collapse . J. Fluid. Mech.169 , 535 – 564 ( 1986 ).
   Web of Science ®Google Scholar
• Postema M Kotopoulis S Delalande A Gilja OH . Sonoporation: Why microbubbles create pores . Ultraschall Med.33 ( 1 ), 97 – 98 ( 2012 ).
   Google Scholar
• Delalande A Kotopoulis S Postema M Midoux P Pichon C . Sonoporation: Mechanistic insights and ongoing challenges for gene transfer . Gene525 ( 2 ), 191 – 199 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Okada K Kudo N Niwa K Yamamoto K . A basic study on sonoporation with microbubbles exposed to pulsed ultrasound . J. Med. Ultrasonics32 , 3 – 11 ( 2005 ).
   PubMedGoogle Scholar
• Kudo N Okada K Yamamoto K . Sonoporation by single-shot pulsed ultrasound with microbubbles adjacent to cells . Biophys. J.96 ( 12 ), 4866 – 4876 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Van Wamel A Kooiman K Harteveld M et al. Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation . J. Control. Release112 ( 2 ), 149 – 155 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Kooiman K Foppen-Harteveld M Van Der Steen AF De Jong N . Sonoporation of endothelial cells by vibrating targeted microbubbles . J. Control. Release154 ( 1 ), 35 – 41 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Forbes MM Steinberg RL O'Brien WD Jr . Examination of inertial cavitation of Optison in producing sonoporation of chinese hamster ovary cells . Ultrasound Med. Biol.34 ( 12 ), 2009 – 2018 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Forbes MM Steinberg RL O'Brien WD Jr . Frequency-dependent evaluation of the role of Definity in producing sonoporation of Chinese hamster ovary cells . J. Ultrasound Med.30 ( 1 ), 61 – 69 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Forbes MM O'Brien WD Jr . Development of a theoretical model describing sonoporation activity of cells exposed to ultrasound in the presence of contrast agents . J. Acoust. Soc. Am.131 ( 4 ), 2723 – 2729 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Krasovitski B Frenkel V Shoham S Kimmel E . Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects . Proc. Natl Acad. Sci. USA108 ( 8 ), 3258 – 3263 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Zhou Y Yang K Cui J Ye JY Deng CX . Controlled permeation of cell membrane by single bubble acoustic cavitation . J. Control. Release157 ( 1 ), 103 – 111 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Dayton P Klibanov A Brandenburger G Ferrara K . Acoustic radiation force in vivo: a mechanism to assist targeting of microbubbles . Ultrasound Med. Biol.25 ( 8 ), 1195 – 1201 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Lum AF Borden MA Dayton PA Kruse DE Simon SI Ferrara KW . Ultrasound radiation force enables targeted deposition of model drug carriers loaded on microbubbles . J. Control. Release111 ( 1–2 ), 128 – 134 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Garbin V Overvelde M Dollet B de Jong N Lohse D Versluis M . Unbinding of targeted ultrasound contrast agent microbubbles by secondary acoustic forces . Phys. Med. Biol.56 ( 19 ), 6161 – 6177 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Postema M Marmottant P Lancee CT Hilgenfeldt S de Jong N . Ultrasound-induced microbubble coalescence . Ultrasound Med. Biol.30 ( 10 ), 1337 – 1344 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Kokhuis TJ Garbin V Kooiman K et al. Secondary Bjerknes forces deform targeted microbubbles . Ultrasound Med. Biol.39 ( (3 ), ), 490 – –506 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Mannaris C Averkiou MA . Investigation of microbubble response to long pulses used in ultrasound-enhanced drug delivery . Ultrasound Med. Biol.38 ( 4 ), 681 – 691 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Fan Z Chen D Deng CX . Improving ultrasound gene transfection efficiency by controlling ultrasound excitation of microbubbles . J. Control. Release170 ( 3 ), 401 – 413 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lawrie A Brisken AF Francis SE Cumberland DC Crossman DC Newman CM . Microbubble-enhanced ultrasound for vascular gene delivery . Gene Ther.7 ( 23 ), 2023 – 2027 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Mehier-Humbert S Bettinger T Yan F Guy RH . Plasma membrane poration induced by ultrasound exposure: Implication for drug delivery . J. Control. Release104 ( 1 ), 213 – 222 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• 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.35 ( 5 ), 847 – 860 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Chen H Brayman AA Kreider W Bailey MR Matula TJ . Observations of translation and jetting of ultrasound-activated microbubbles in mesenteric microvessels . Ultrasound Med. Biol.37 ( 12 ), 2139 – 2148 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Tachibana K Uchida T Ogawa K Yamashita N Tamura K . Induction of cell-membrane porosity by ultrasound . Lancet353 ( 9162 ), 1409 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Ohl CD Arora M Ikink R et al. Sonoporation from jetting cavitation bubbles . Biophys. J.91 ( 11 ), 4285 – 4295 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Zeghimi A Uzbekov R Arbeille B Escoffre JM Bouakaz A . Ultrastuctural modifications of cell membranes and organelles induced by sonoporation . IEEE Int. Ultrason. Symp.2045 – 2048 ( 2012 ).
   Google Scholar
• 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.13 ( 2 ), 163 – 172 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Zhao YZ Luo YK Lu CT et al. Phospholipids-based microbubbles sonoporation pore size and reseal of cell membrane cultured in vitro . J. Drug Target.16 ( 1 ), 18 – 25 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Yang F Gu N Chen D et al. Experimental study on cell self-sealing during sonoporation . J. Control. Release131 ( 3 ), 205 – 210 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Zarnitsyn V Rostad CA Prausnitz MR . Modeling transmembrane transport through cell membrane wounds created by acoustic cavitation . Biophys. J.95 ( 9 ), 4124 – 4138 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Zhou Y Kumon RE Cui J Deng CX . The size of sonoporation pores on the cell membrane . Ultrasound Med. Biol.35 ( 10 ), 1756 – 1760 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Fan Z Liu H Mayer M Deng CX . Spatiotemporally controlled single cell sonoporation . Proc. Natl Acad. Sci. USA109 ( 41 ), 16486 – 16491 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Deng CX Sieling F Pan H Cui J . Ultrasound-induced cell membrane porosity . Ultrasound Med. Biol.30 ( 4 ), 519 – 526 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Pan H Zhou Y Izadnegahdar O Cui J Deng CX . Study of sonoporation dynamics affected by ultrasound duty cycle . Ultrasound Med. Biol.31 ( 6 ), 849 – 856 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Zhou Y Shi J Cui J Deng CX . Effects of extracellular calcium on cell membrane resealing in sonoporation . J. Control. Release126 ( 1 ), 34 – 43 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• McNeil PL Miyake K Vogel SS . The endomembrane requirement for cell surface repair . Proc. Natl Acad. Sci. USA100 ( 8 ), 4592 – 4597 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• McNeil PL Kirchhausen T . An emergency response team for membrane repair . Nat. Rev. Mol. Cell Biol.6 ( 6 ), 499 – 505 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Hassan MA Campbell P Kondo T . The role of Ca2+ in ultrasound-elicited bioeffects: progress, perspectives and prospects . Drug Discov. Today15 ( 21–22 ), 892 – 906 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Kumon RE Aehle M Sabens D et al. Spatiotemporal effects of sonoporation measured by real-time calcium imaging . Ultrasound Med. Biol.35 ( 3 ), 494 – 506 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Guzman HR Nguyen DX Mcnamara AJ Prausnitz MR . Equilibrium loading of cells with macromolecules by ultrasound: effects of molecular size and acoustic energy . J. Pharm. Sci.91 ( 7 ), 1693 – 1701 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Meijering BD Juffermans LJ Van Wamel A . Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation . Circ. Res.104 ( 5 ), 679 – 687 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Duvshani-Eshet M Adam D Machluf M . The effects of albumin-coated microbubbles in DNA delivery mediated by therapeutic ultrasound . J. Control. Release112 ( 2 ), 156 – 166 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Mehier-Humbert S Bettinger T Yan F Guy RH . Ultrasound-mediated gene delivery: Kinetics of plasmid internalization and gene expression . J. Control. Release104 ( 1 ), 203 – 211 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Tlaxca JL Anderson CR Klibanov AL et al. Analysis of in vitro transfection by sonoporation using cationic and neutral microbubbles . Ultrasound Med. Biol.36 ( 11 ), 1907 – 1918 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Escoffre JM Teissie J Rols MP . Gene transfer: how can the biological barriers be overcome?J. Membr. Biol.236 ( 1 ), 61 – 74 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Duvshani-Eshet M Machluf M . Therapeutic ultrasound optimization for gene delivery: a key factor achieving nuclear DNA localization . J. Control. Release108 ( 2–3 ), 513 – 528 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Lindell J Girard P Muller N Jordan M Wurm F . Calfection: a novel gene transfer method for suspension cells . Biochim. Biophys. Acta1676 ( 2 ), 155 – 161 ( 2004 ).
   PubMedGoogle Scholar
• Hassan MA Ahmed IS Campbell P Kondo T . Enhanced gene transfection using calcium phosphate co-precipitates and low-intensity pulsed ultrasound . Eur. J. Pharm. Sci.47 ( 4 ), 768 – 773 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Geers B Lentacker I Alonso A et al. Elucidating the mechanisms behind sonoporation with adeno-associated virus-loaded microbubbles . Mol. Pharm.8 ( 6 ), 2244 – 2251 ( 2011 ).
   PubMedGoogle Scholar
• Yudina A Moonen C . Ultrasound-induced cell permeabilisation and hyperthermia: strategies for local delivery of compounds with intracellular mode of action . Int. J. Hyperthermia28 ( 4 ), 311 – 319 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Escoffre JM Zeghimi A Novell A Bouakaz A . In vivo gene delivery by sonoporation: recent progress and prospects . Curr. Gene Ther.13 ( 1 ), 2 – 14 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Deng CX . Targeted drug delivery across the blood-brain barrier using ultrasound technique . Ther. Deliv.1 ( 6 ), 819 – 848 ( 2010 ).
   PubMedGoogle Scholar
• Burgess A Hynynen K . Noninvasive and targeted drug delivery to the brain using focused ultrasound . ACS Chem. Neurosci.4 ( 4 ), 519 – 526 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Mayer CR Bekeredjian R . Ultrasonic gene and drug delivery to the cardiovascular system . Adv. Drug Deliv. Rev.60 ( 10 ), 1177 – 1192 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Meairs S Kern R Alonso A . Why and how do microbubbles enhance the effectiveness of diagnostic and therapeutic interventions in cerebrovascular disease?Curr. Pharm. Des.18 ( 15 ), 2223 – 2235 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Frenkel V . Ultrasound mediated delivery of drugs and genes to solid tumors . Adv. Drug Deliv. Rev.60 ( 10 ), 1193 – 1208 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Sonoda S Tachibana K Uchino E et al. Inhibition of melanoma by ultrasound-microbubble-aided drug delivery suggests membrane permeabilization . Cancer Biol. Ther.6 ( 8 ), 1276 – 1283 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Hynynen K McDannold N Vykhodtseva N Jolesz FA . Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits . Radiology220 ( 3 ), 640 – 646 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Deng CX Huang X . Improved outcome of targeted delivery of chemotherapy drugs to the brain using a combined strategy of ultrasound, magnetic targeting and drug-loaded nanoparticles . Ther. Deliv.2 ( 2 ), 137 – 141 ( 2011 ).
   PubMedGoogle Scholar
• Treat LH McDannold N Vykhodtseva N Zhang Y Tam K Hynynen K . Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound . Int. J. Cancer121 ( 4 ), 901 – 907 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Lentacker I Geers B Demeester J De Smedt SC Sanders NN . Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved . Mol. Ther.18 ( 1 ), 101 – 108 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Liu HL Hua MY Yang HW et al. Magnetic resonance monitoring of focused ultrasound/magnetic nanoparticle targeting delivery of therapeutic agents to the brain . Proc. Natl Acad. Sci. USA107 ( 34 ), 15205 – 15210 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Waehler R Russell SJ Curiel DT . Engineering targeted viral vectors for gene therapy . Nat. Rev. Genet.8 ( 8 ), 573 – 587 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Hartman ZC Appledorn DM Amalfitano A . Adenovirus vector induced innate immune responses: impact upon efficacy and toxicity in gene therapy and vaccine applications . Virus Res.132 ( 1–2 ), 1 – 14 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Nayak S Herzog RW . Progress and prospects: immune responses to viral vectors . Gene Ther.17 ( 3 ), 295 – 304 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• 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.273 ( 1 ), 62 – 69 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Haag P Frauscher F Gradl J et al. Microbubble-enhanced ultrasound to deliver an antisense oligodeoxynucleotide targeting the human androgen receptor into prostate tumours . J. Steroid Biochem. Mol. Biol.102 ( 1–5 ), 103 – 113 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Escoffre JM Novell A Piron J Zeghimi A Doinikov A Bouakaz A . Microbubble attenuation and destruction: are they involved in sonoporation efficiency ? IEEE Trans. Ultrason. Ferroelectr. Freq. Control60 ( 1 ), 46 – 52 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Tlaxca JL Rychak JJ Ernst PB et al. Ultrasound-based molecular imaging and specific gene delivery to mesenteric vasculature by endothelial adhesion molecule targeted microbubbles in a mouse model of Crohn's disease . J. Control. Release165 ( 3 ), 216 – 225 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Ghosh A Greenberg ME . Calcium signaling in neurons: molecular mechanisms and cellular consequences . Science268 ( 5208 ), 239 – 247 ( 1995 ).
   PubMed Web of Science ®Google Scholar
• Bers DM . Cardiac excitation-contraction coupling . Nature415 ( 6868 ), 198 – 205 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Berridge MJ Bootman MD Roderick HL . Calcium signalling: dynamics, homeostasis and remodelling . Nat. Rev. Mol. Cell Biol.4 ( 7 ), 517 – 529 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Kumon RE Aehle M Sabens D Parikh P Kourennyi D Deng CX . Ultrasound-induced calcium oscillations and waves in Chinese hamster ovary cells in the presence of microbubbles . Biophys. J.93 ( 6 ), L29 – 31 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Juffermans LJ van Dijk A Jongenelen CA et al. Ultrasound and microbubble-induced intra- and intercellular bioeffects in primary endothelial cells . Ultrasound Med. Biol.35 ( 11 ), 1917 – 1927 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Park J Fan Z Kumon RE El-Sayed ME Deng CX . Modulation of intracellular Ca2+ concentration in brain microvascular endothelial cells in vitro by acoustic cavitation . Ultrasound Med. Biol.36 ( 7 ), 1176 – 1187 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Park J Fan Z Deng CX . Effects of shear stress cultivation on cell membrane disruption and intracellular calcium concentration in sonoporation of endothelial cells . J. Biomech.44 ( 1 ), 164 – 169 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Boitano S Dirksen ER Sanderson MJ . Intercellular propagation of calcium waves mediated by inositol trisphosphate . Science258 ( 5080 ), 292 – 295 ( 1992 ).
   PubMed Web of Science ®Google Scholar
• Sauer H Hescheler J Wartenberg M . Mechanical strain-induced Ca2+ waves are propagated via ATP release and purinergic receptor activation . Am. J. Physiol. Cell Physiol.279 ( 2 ), C295 – 307 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Schlicher RK Hutcheson JD Radhakrishna H Apkarian RP Prausnitz MR . Changes in cell morphology due to plasma membrane wounding by acoustic cavitation . Ultrasound Med. Biol.36 ( 4 ), 677 – 692 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Hutcheson JD Schlicher RK Hicks HK Prausnitz MR . Saving cells from ultrasound-induced apoptosis: quantification of cell death and uptake following sonication and effects of targeted calcium chelation . Ultrasound Med. Biol.36 ( 6 ), 1008 – 1021 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Feril LB , Jr. Kondo T Zhao QL et al. Enhancement of ultrasound-induced apoptosis and cell lysis by echo-contrast agents . Ultrasound Med. Biol.29 ( 2 ), 331 – 337 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Honda H Kondo T Zhao QL Feril LB , Jr. Kitagawa H . Role of intracellular calcium ions and reactive oxygen species in apoptosis induced by ultrasound . Ultrasound Med. Biol.30 ( 5 ), 683 – 692 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Feril LB , Jr. Kondo T Cui ZG et al. Apoptosis induced by the sonomechanical effects of low intensity pulsed ultrasound in a human leukemia cell line . Cancer Lett.221 ( 2 ), 145 – 152 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Zhong W Sit WH Wan JM Yu AC . Sonoporation induces apoptosis and cell cycle arrest in human promyelocytic leukemia cells . Ultrasound Med. Biol.37 ( 12 ), 2149 – 2159 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Frampton JP Fan Z Simon A Chen D Deng CX Takayama S . Aqueous two-phase system patterning of microbubbles: Localized induction of apoptosis in sonoporated cells . Adv. Funct. Mater.23 , 3420 – 3431 ( 2013 ).
   Web of Science ®Google Scholar
• Juffermans LJ Kamp O Dijkmans PA Visser CA Musters RJ . Low-intensity ultrasound-exposed microbubbles provoke local hyperpolarization of the cell membrane via activation of BKCa channels . Ultrasound Med. Biol.34 ( 3 ), 502 – 508 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Tran TA Roger S Le Guennec JY Tranquart F Bouakaz A . Effect of ultrasound-activated microbubbles on the cell electrophysiological properties . Ultrasound Med. Biol.33 ( 1 ), 158 – 163 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Tran TA Le Guennec JY Bougnoux P Tranquart F Bouakaz A . Characterization of cell membrane response to ultrasound activated microbubbles . IEEE Trans. Ultrason. Ferroelectr. Freq. Control55 ( 1 ), 43 – 49 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Tran TA Le Guennec JY Babuty D Bougnoux P Tranquart F Bouakaz A . On the mechanisms of ultrasound contrast agents-induced arrhythmias . Ultrasound Med. Biol.35 ( 6 ), 1050 – 1056 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Lukacs GL Haggie P Seksek O Lechardeur D Freedman N Verkman AS . Size-dependent DNA mobility in cytoplasm and nucleus . J. Biol. Chem.275 ( 3 ), 1625 – 1629 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Noriega S Hasanova G Subramanian A . The effect of ultrasound stimulation on the cytoskeletal organization of chondrocytes seeded in three-dimensional matrices . Cells Tissues Organs197 ( 1 ), 14 – 26 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Fan Z Sun Y Di C et al. Acoustic tweezing cytometry for live-cell subcellular modulation of intracellular cytoskeleton contractility . Sci. Rep.3 , 2176 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Mayer CR Geis NA Katus HA Bekeredjian R . Ultrasound targeted microbubble destruction for drug and gene delivery . Expert Opin. Drug Deliv.5 ( 10 ), 1121 – 1138 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• 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.32 ( 8 ), 1269 – 1279 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• 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.15 ( 10 ), 664 – 671 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Hansma HG Vesenka J Siegerist C et al. Reproducible imaging and dissection of plasmid DNA under liquid with the atomic force microscope . Science256 ( 5060 ), 1180 – 1184 ( 1992 ).
   PubMed Web of Science ®Google Scholar
• Furusawa Y Fujiwara Y Campbell P et al. DNA double-strand breaks induced by cavitational mechanical effects of ultrasound in cancer cell lines . PLoS ONE7 ( 1 ), e29012 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Pysz MA Gambhir SS Willmann JK . Molecular imaging: current status and emerging strategies . Clin. Radiol.65 ( 7 ), 500 – 516 ( 2010 ).
   PubMed Web of Science ®Google Scholar