Mechanisms of microbubble-facilitated sonoporation for drug and gene delivery

Therapeutic Delivery

Volumn 5, Issue 4, 2014, Pages 467-486

  Fan, Zhenzhen ^a   Kumon, Ronald E ^b   Deng, Cheri X ^c  

^a INSTITUTE OF ACOUSTICS   (China)

^b KETTERING UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTINEOPLASTIC AGENT; BLEOMYCIN; CALCIUM ION; COMPLEMENTARY DNA; CONTRAST MEDIUM; DOXORUBICIN; EPIRUBICIN; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; FREE RADICAL; LIGAND; MOLECULAR MARKER; NANOPARTICLE; PEPTIDE; PLASMID DNA; POLYMER; PROPIDIUM IODIDE; VIRUS VECTOR; VITAMIN;

ACOUSTICS; APOPTOSIS; ATOMIC FORCE MICROSCOPY; BLOOD BRAIN BARRIER; BRAIN CANCER; CANCER CELL; CANCER GENE THERAPY; CARDIOVASCULAR SYSTEM; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CHANNEL GATING; CYTOSKELETON; DRUG DELIVERY SYSTEM; DRUG TARGETING; ENDOCYTOSIS; FLUID FLOW; FLUORESCENCE MICROSCOPY; FORCE; GENE EXPRESSION; GENE THERAPY; GENETIC TRANSFECTION; HIGH TEMPERATURE; HUMAN; INTRACELLULAR TRANSPORT; KINETICS; LIQUID; LUMINESCENCE; MACROMOLECULE; MEDICAL TECHNOLOGY; MELANOMA; MEMBRANE POTENTIAL; MICROBUBBLE; MICROSTREAMING; MOLECULAR IMAGING; MOTION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NUCLEAR MAGNETIC RESONANCE IMAGING; PATCH CLAMP TECHNIQUE; PHOTON; PRESSURE; PRIORITY JOURNAL; REVIEW; SCANNING ELECTRON MICROSCOPY; SOLID; SOLID TUMOR; SONOLUMINESCENCE; TRANSMISSION ELECTRON MICROSCOPY; TUMOR MODEL; ULTRASOUND; ULTRASOUND MEDIATED DELIVERY;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE PERMEABILITY; DRUG DELIVERY SYSTEMS; GENE TRANSFER TECHNIQUES; HUMANS; MICROBUBBLES; POROSITY; ULTRASONICS;

EID: 84901345704     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.14.10     Document Type: Review

References (133)

1. Klibanov AL. Microbubble contrast agents: targeted ultrasound imaging and ultrasound-assisted drug-delivery applications. Invest. Radiol. 41(3), 354-362 (2006). (Pubitemid 44406198)
2. Kaufmann BA, Lindner JR. Molecular imaging with targeted contrast ultrasound. Curr. Opin. Biotechnol. 18(1), 11-16 (2007). (Pubitemid 46237740)
3. 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. Circulation 98(13), 1264-1267 (1998). (Pubitemid 28443388)
4. 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). (Pubitemid 30336669)
5. 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).
6. Xie A, Belcik T, Qi Y et al. Ultrasound-mediated vascular gene transfection by cavitation of endothelial-targeted cationic microbubbles. JACC Cardiovasc. Imaging 5(12), 1253-1262 (2012).
7. Husseini GA, Pitt WG. Micelles and nanoparticles for ultrasonic drug and gene delivery. Adv. Drug Deliv. Rev. 60(10), 1137-1152 (2008).
8. Prentice P, Cuschieri A, Dholakia K, Prausnitz M, Campbell P. Membrane disruption by optically controlled microbubble cavitation. Nat. Phy. 1(2), 107 (2005).
9. 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). (Pubitemid 43903070)
10. Fan Z, Kumon RE, Park J, Deng CX. Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J. Control. Release 142(1), 31-39 (2010).
11. Leighton TG. The Acoustic Bubble. Academic Press, San Diego, CA, USA. (1994).
12. 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).
13. 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). (Pubitemid 350246663)
14. Kaul S. Myocardial contrast echocardiography: A 25-year retrospective. Circulation 118(3), 291-308 (2008).
15. Borden MA, Longo M. Dissolution behavior of lipid monolayer-coated, air-filled microbubbles: effect of lipid hydrophobic chain length. Langmuir 18, 9225-9233 (2002). (Pubitemid 35458180)
16. 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). (Pubitemid 47302197)
17. Klibanov AL. Preparation of targeted microbubbles: ultrasound contrast agents for molecular imaging. Med. Biol. Eng. Comput. 47(8), 875-882 (2009).
18. 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).
19. Delalande A, Kotopoulis S, Rovers T, Pichon C, Postema M. Sonoporation at a low mechanical indiex. Bubble Sci. Engin. Technol. 3, 3-11 (2011).
20. Marmottant P, Hilgenfeldt S. Controlled vesicle deformation and lysis by single oscillating bubbles. Nature 423(6936), 153-156 (2003). (Pubitemid 36569534)
21. Longuet-Higgins MS. Viscous streaming from an oscillating spherical bubble. Proc. R. Soc. London A 454, 725-742 (1998). (Pubitemid 128734672)
22. Wu J. Shear stress in cells generated by ultrasound. Prog. Biophys. Mol. Biol. 93(1-3), 363-373 (2007). (Pubitemid 44809397)
23. 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). (Pubitemid 44809398)
24. Crum LA, Roy RA. Sonoluminescence. Science 266(5183), 233-234 (1994). (Pubitemid 24343931)
25. Miller DL, Thomas RM. Ultrasound contrast agents nucleate inertial cavitation in vitro. Ultrasound Med. Biol. 21(8), 1059-1065 (1995).
26. 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). (Pubitemid 27024654)
27. Lauterborn W, Ohl CD. Cavitation bubble dynamics. Ultrason. Sonochem. 4(2), 65-75 (1997).
28. 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). (Pubitemid 36531757)
29. 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). (Pubitemid 43994294)
30. Zhou Y, Cui J, Deng CX. Dynamics of sonoporation correlated with acoustic cavitation activities. Biophys. J. 94(7), L51-53 (2008).
31. Husseini GA, Diaz de la Rosa MA, Richardson ES, Christensen DA, Pitt WG. The role of cavitation in acoustically activated drug delivery. J. Control. Release 107(2), 253-261 (2005). (Pubitemid 41316288)
32. 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).
33. Lauterborn W, Bolle H. Experimental investigation of cavitation-bubble collapse in the neighbourhood of a solid boundary. J. Fluid. Mech. 72, 391-399 (1975).
34. Prosperetti A. Bubble phenomena in sound fields: part 2. Ultrasonics 22, 115-124 (1984).
35. 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).
36. Tomita Y, Shima A. Mechanisms of impulsive pressure generation and damage pit formation by bubble collapse. J. Fluid. Mech. 169, 535-564 (1986).
37. Postema M, Kotopoulis S, Delalande A, Gilja OH. Sonoporation: Why microbubbles create pores. Ultraschall Med. 33(1), 97-98 (2012).
38. Delalande A, Kotopoulis S, Postema M, Midoux P, Pichon C. Sonoporation: Mechanistic insights and ongoing challenges for gene transfer. Gene 525(2), 191-199 (2013).
39. Okada K, Kudo N, Niwa K, Yamamoto K. A basic study on sonoporation with microbubbles exposed to pulsed ultrasound. J. Med. Ultrasonics 32, 3-11 (2005). (Pubitemid 40591190)
40. Kudo N, Okada K, Yamamoto K. Sonoporation by singleshot pulsed ultrasound with microbubbles adjacent to cells. Biophys. J. 96(12), 4866-4876 (2009).
41. Van Wamel A, Kooiman K, Harteveld M et al. Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation. J. Control. Release 112(2), 149-155 (2006).
42. Kooiman K, Foppen-Harteveld M, Van Der Steen AF, De Jong N. Sonoporation of endothelial cells by vibrating targeted microbubbles. J. Control. Release 154(1), 35-41 (2011).
43. 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).
44. Forbes MM, Steinberg RL, O'Brien WD Jr. Frequencydependent evaluation of the role of Definity in producing sonoporation of Chinese hamster ovary cells. J. Ultrasound Med. 30(1), 61-69 (2011).
45. 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).
46. Krasovitski B, Frenkel V, Shoham S, Kimmel E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc. Natl Acad. Sci. USA 108(8), 3258-3263 (2011).
47. Zhou Y, Yang K, Cui J, Ye JY, Deng CX. Controlled permeation of cell membrane by single bubble acoustic cavitation. J. Control. Release 157(1), 103-111 (2012).
48. 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). (Pubitemid 29465793)
49. 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. Release 111(1-2), 128-134 (2006). (Pubitemid 43290001)
50. 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).
51. Postema M, Marmottant P, Lancee CT, Hilgenfeldt S, de Jong N. Ultrasound-induced microbubble coalescence. Ultrasound Med. Biol. 30(10), 1337-1344 (2004). (Pubitemid 39576185)
52. Kokhuis TJ, Garbin V, Kooiman K et al. Secondary Bjerknes forces deform targeted microbubbles. Ultrasound Med. Biol. 39((3),), 490-506 ( (2013).).
53. 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).
54. Fan Z, Chen D, Deng CX. Improving ultrasound gene transfection efficiency by controlling ultrasound excitation of microbubbles. J. Control. Release 170(3), 401-413 (2013).
55. 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). (Pubitemid 32036768)
56. Mehier-Humbert S, Bettinger T, Yan F, Guy RH. Plasma membrane poration induced by ultrasound exposure: Implication for drug delivery. J. Control. Release 104(1), 213-222 (2005). (Pubitemid 40615248)
57. 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).
58. Chen H, Brayman AA, Kreider W, Bailey MR, Matula TJ. Observations of translation and jetting of ultrasoundactivated microbubbles in mesenteric microvessels. Ultrasound Med. Biol. 37(12), 2139-2148 (2011).
59. Tachibana K, Uchida T, Ogawa K, Yamashita N, Tamura K. Induction of cell-membrane porosity by ultrasound. Lancet 353(9162), 1409 (1999). (Pubitemid 29192415)
60. Ohl CD, Arora M, Ikink R et al. Sonoporation from jetting cavitation bubbles. Biophys. J. 91(11), 4285-4295 (2006). (Pubitemid 44887286)
61. 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).
62. 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). (Pubitemid 43039908)
63. 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).
64. Yang F, Gu N, Chen D et al. Experimental study on cell self-sealing during sonoporation. J. Control. Release 131(3), 205-210 (2008).
65. Zarnitsyn V, Rostad CA, Prausnitz MR. Modeling transmembrane transport through cell membrane wounds created by acoustic cavitation. Biophys. J. 95(9), 4124-4138 (2008).
66. 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).
67. Fan Z, Liu H, Mayer M, Deng CX. Spatiotemporally controlled single cell sonoporation. Proc. Natl Acad. Sci. USA 109(41), 16486-16491 (2012).
68. Deng CX, Sieling F, Pan H, Cui J. Ultrasound-induced cell membrane porosity. Ultrasound Med. Biol. 30(4), 519-526 (2004). (Pubitemid 38581152)
69. 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). (Pubitemid 40776083)
70. Zhou Y, Shi J, Cui J, Deng CX. Effects of extracellular calcium on cell membrane resealing in sonoporation. J. Control. Release 126(1), 34-43 (2008).
71. McNeil PL, Miyake K, Vogel SS. The endomembrane requirement for cell surface repair. Proc. Natl Acad. Sci. USA 100(8), 4592-4597 (2003). (Pubitemid 36457775)
72. McNeil PL, Kirchhausen T. An emergency response team for membrane repair. Nat. Rev. Mol. Cell Biol. 6(6), 499-505 (2005). (Pubitemid 40780561)
73. Hassan MA, Campbell P, Kondo T. The role of Ca2+ in ultrasound-elicited bioeffects: progress, perspectives and prospects. Drug Discov. Today 15(21-22), 892-906 (2010). Provides a critical review of the literature regarding ultrasound-induced calcium transients and other bioeffects.
74. 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).
75. 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). (Pubitemid 34680232)
76. 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).
77. Duvshani-Eshet M, Adam D, Machluf M. The effects of albumin-coated microbubbles in DNA delivery mediated by therapeutic ultrasound. J. Control. Release 112(2), 156-166 (2006).
78. Mehier-Humbert S, Bettinger T, Yan F, Guy RH. Ultrasoundmediated gene delivery: Kinetics of plasmid internalization and gene expression. J. Control. Release 104(1), 203-211 (2005). (Pubitemid 40615247)
79. 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).
80. Escoffre JM, Teissie J, Rols MP. Gene transfer: how can the biological barriers be overcome? J. Membr. Biol. 236(1), 61-74 (2010).
81. Duvshani-Eshet M, Machluf M. Therapeutic ultrasound optimization for gene delivery: A key factor achieving nuclear DNA localization. J. Control. Release 108(2-3), 513-528 (2005). (Pubitemid 41613754)
82. Lindell J, Girard P, Muller N, Jordan M, Wurm F. Calfection: A novel gene transfer method for suspension cells. Biochim. Biophys. Acta 1676(2), 155-161 (2004). (Pubitemid 38121466)
83. Hassan MA, Ahmed IS, Campbell P, Kondo T. Enhanced gene transfection using calcium phosphate co-precipitates and lowintensity pulsed ultrasound. Eur. J. Pharm. Sci. 47(4), 768-773 (2012).
84. Geers B, Lentacker I, Alonso A et al. Elucidating the mechanisms behind sonoporation with adeno-associated virusloaded microbubbles. Mol. Pharm. 8(6), 2244-2251 (2011).
85. Yudina A, Moonen C. Ultrasound-induced cell permeabilisation and hyperthermia: strategies for local delivery of compounds with intracellular mode of action. Int. J. Hyperthermia 28(4), 311-319 (2012).
86. 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).
87. Deng CX. Targeted drug delivery across the blood-brain barrier using ultrasound technique. Ther. Deliv. 1(6), 819-848 (2010).
88. Burgess A, Hynynen K. Noninvasive and targeted drug delivery to the brain using focused ultrasound. ACS Chem. Neurosci. 4(4), 519-526 (2013).
89. Mayer CR, Bekeredjian R. Ultrasonic gene and drug delivery to the cardiovascular system. Adv. Drug Deliv. Rev. 60(10), 1177-1192 (2008).
90. 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).
91. Frenkel V. Ultrasound mediated delivery of drugs and genes to solid tumors. Adv. Drug Deliv. Rev. 60(10), 1193-1208 (2008).
92. 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). (Pubitemid 351590383)
93. Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 220(3), 640-646 (2001). (Pubitemid 32799969)
94. 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).
95. 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. Cancer 121(4), 901-907 (2007). (Pubitemid 47106223)
96. 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).
97. 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. USA 107(34), 15205-15210 (2010).
98. Waehler R, Russell SJ, Curiel DT. Engineering targeted viral vectors for gene therapy. Nat. Rev. Genet. 8(8), 573-587 (2007). (Pubitemid 47077278)
99. 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). (Pubitemid 351232078)
100. Nayak S, Herzog RW. Progress and prospects: immune responses to viral vectors. Gene Ther. 17(3), 295-304 (2010).
101. 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).
102. 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). (Pubitemid 44750646)
103. 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. Control 60(1), 46-52 (2013).
104. 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. Release 165(3), 216-225 (2013).
105. Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268(5208), 239-247 (1995).
106. Bers DM. Cardiac excitation-contraction coupling. Nature 415(6868), 198-205 (2002). (Pubitemid 34059525)
107. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4(7), 517-529 (2003). (Pubitemid 36773404)
108. 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). (Pubitemid 47437567)
109. 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).
110. 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).
111. 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).
112. Boitano S, Dirksen ER, Sanderson MJ. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 258(5080), 292-295 (1992).
113. Sauer H, Hescheler J, Wartenberg M. Mechanical straininduced Ca2+ waves are propagated via ATP release and purinergic receptor activation. Am. J. Physiol. Cell Physiol. 279(2), C295-307 (2000).
114. 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).
115. 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).
116. 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). (Pubitemid 36355855)
117. 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). (Pubitemid 38739375)
118. 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). (Pubitemid 40460401)
119. 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).
120. 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).
121. 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). (Pubitemid 351625455)
122. 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). (Pubitemid 44959325)
123. 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. Control 55(1), 43-49 (2008).
124. 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).
125. 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). (Pubitemid 30060778)
126. Noriega S, Hasanova G, Subramanian A. The effect of ultrasound stimulation on the cytoskeletal organization of chondrocytes seeded in three-dimensional matrices. Cells Tissues Organs 197(1), 14-26 (2013).
127. 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).
128. 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).
129. 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). (Pubitemid 44093795)
130. 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). (Pubitemid 350201319)
131. Hansma HG, Vesenka J, Siegerist C et al. Reproducible imaging and dissection of plasmid DNA under liquid with the atomic force microscope. Science 256(5060), 1180-1184 (1992).
132. Furusawa Y, Fujiwara Y, Campbell P et al. DNA doublestrand breaks induced by cavitational mechanical effects of ultrasound in cancer cell lines. PLoS ONE 7(1), e29012 (2012).
133. Pysz MA, Gambhir SS, Willmann JK. Molecular imaging: current status and emerging strategies. Clin. Radiol. 65(7), 500-516 (2010).