Cell experimental studies on sonoporation: State of the art and remaining problems

Journal of Controlled Release

Volumn 174, Issue 1, 2014, Pages 151-160

  Yu, Hao ^a   Xu, Liang ^b  

^a SHENZHEN POLYTECHNIC   (China)

^b Shenzhen Institute for Drug Control   (China)

Author keywords

Cell experiment; Delivery of drug or gene; Microbubble; Sonoporation; Ultrasound

Indexed keywords

CONTROLLED DRUG DELIVERY; GENE THERAPY; TARGETED DRUG DELIVERY; ULTRASONICS;

AUXILIARY TECHNOLOGY; BIO-EFFECTS; EXPERIMENTAL METHODS; EXPERIMENTAL PARAMETERS; MICRO-BUBBLE; SONOPORATION; STATE OF THE ART; ULTRASOUND EXPOSURE;

CYTOLOGY;

BR 14; CASPASE; CYCLIN A; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN E; ECHO CONTRAST MEDIUM; F ACTIN; LIPOSOME; MACROGOL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PERFLUBUTANE; PERFLUTREN; PROTEIN BAX; PROTEIN BCL 2; SHU 508; SONOVUE; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS; ARTICLE; CALCIUM CELL LEVEL; CAMERA; CELL CYCLE PHASE; CELL CYCLE PROGRESSION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELL STRAIN HL 60; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CHANNEL GATING; DRUG DELIVERY SYSTEM; ECHOGRAPHY; ENDOSOME; EXPERIMENTAL STUDY; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE TARGETING; GENE TRANSFER; GENETIC TRANSFECTION; MEMBRANE DAMAGE; MEMBRANE RUPTURE; MICROBUBBLE; NONHUMAN; OOCYTE; PATCH CLAMP TECHNIQUE; PINOCYTOSIS; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPE; SHOCK WAVE; SONOPORATION; VIRUS CAPSID; VOLTAGE CLAMP TECHNIQUE; WESTERN BLOTTING; XENOPUS;

CELL EXPERIMENT; DELIVERY OF DRUG OR GENE; MICROBUBBLE; SONOPORATION; ULTRASOUND;

CELL MEMBRANE; DRUG DELIVERY SYSTEMS; GENE TRANSFER TECHNIQUES; HUMANS; MICROBUBBLES; POROSITY; ULTRASONICS;

EID: 84890284456     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.11.010     Document Type: Review

References (90)

1. P. Yang, S. Gai, and J. Lin Functionalized mesoporous silica materials for controlled drug delivery Chem. Soc. Rev. 41 9 2012 3679 3698
2. K. Ariga, A. Vinu, Y. Yamauchi, Q. Ji, and J.P. Hill Nanoarchitectonics for mesoporous materials Bull. Chem. Soc. Jpn. 85 1 2012 1 32
3. B.M. Wohl, and J.F. Engbersen Responsive layer-by-layer materials for drug delivery J. Control. Release 158 1 2012 2 14
4. P.K. Deshmukh, K.P. Ramani, S.S. Singh, A.R. Tekade, V.K. Chatap, G.B. Patil, and S.B. Bari Stimuli-sensitive layer-by-layer (LbL) self-assembly systems: targeting and biosensory applications J. Control. Release 166 3 2013 294 306
5. T.A. Kolesnikova, A.G. Skirtach, and H. Mohwald Red blood cells and polyelectrolyte multilayer capsules: natural carriers versus polymer-based drug delivery vehicles Expert Opin. Drug Deliv. 10 1 2013 47 58
6. Z. Lei stimuli-responsive polymer films 42 17 2013 7148 7160
7. A.G. Skirtach, A.M. Yashchenok, and H. Mohwald Encapsulation, release and applications of LbL polyelectrolyte multilayer capsules Chem. Commun. 47 48 2011 12736 12746
8. Ine Lentacker, Stefaan C. De Smedt, and Niek N. Sanders Drug loaded microbubble design for ultrasound triggered delivery Soft Matter 5 2009 2161 2170
9. C.M. Newman, and T. Bettinger Gene therapy progress and prospects: ultrasound for gene transfer Gene Ther. 14 6 2007 465 475
10. S. Sheikh, S. Pallagatti, B. Singh, N. Puri, R. Singh, and A. Kalucha Sonoporation, a redefined ultrasound modality as therapeutic aid: a review J. Clin. Exp. Dent. 3 3 2011 e228 e234
11. W.G. Pitt, and G.A. Husseini Ultrasound in drug and gene delivery Adv. Drug Deliv. Rev. 60 10 2008 1095 1096
12. S. Bao, B.D. Thrall, and D.L. Miller Transfection of a reporter plasmid into cultured cells by sonoporation in vitro Ultrasound Med. Biol. 23 1997 953 959
13. W.J. Greenleaf, M.E. Bolander, G. Sarkar, M.B. Goldring, and J.F. Greenleaf Artificial cavitation nuclei significantly enhance acoustically induced cell transfection Ultrasound Med. Biol. 24 1998 587 595
14. L.D. Miller, S.V. Pislaru, and J. Greenleaf Sonoporation: mechanical DNA delivery by ultrasonic cavitation Somat. Cell Mol. Genet. 27 6 2002 115 134
15. K. Tachibana, T. Uchida, K. Ogawa, N. Yamashita, and K. Tamura Induction of cell-membrane porosity by ultrasound Lancet 353 9162 1999 1409
16. P. Prentice, A. Cuschieri, K. Dholakia, M. Prausnitz, and P. Compbell Membrane disruption by optically controlled microbubble cavitation Nat. Phys. 1 2005 107 110
17. J.P. Ross, X. Cai, J.F. Chiu, J. Yang, and J. Wu Optical and atomic force microscopic studies on sonoporation J. Acoust. Soc. Am. 111 3 2002 1161 1164
18. P. Qin, L. Xu, W. Zhong, and A.C. Yu Ultrasound-microbubble mediated cavitation of plant cells: effects on morphology and viability Ultrasound Med. Biol. 38 6 2012 1085 1096
19. A. van Wamel, A. Bouakaz, M. Versluis, and N. de Jong Micromanipulation of endothelial cells: ultrasound-microbubble-cell interaction Ultrasound Med. Biol. 30 9 2004 1255 1258
20. A. van Wamel, K. Kooiman, M. Harteveld, M. Emmer, F.J. ten Cate, M. Versluis, and N. de Jong Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation J. Control. Release 112 2 2006 149 155
21. S. Moosavi Nejad, S.H. Hosseini, H. Akiyama, and K. Tachibana Optical observation of cell sonoporation with low intensity ultrasound Biochem. Biophys. Res. Commun. 413 2 2011 218 223
22. S. Mehier-Humbert, T. Bettinger, F. Yan, and R.H. Guy Plasma membrane poration induced by ultrasound exposure: implication for drug delivery J. Control. Release 104 1 2005 213 222
23. M. Afadzi, S.P. Strand, E.A. Nilssen, S.E. Masoy, T.F. Johansen, R. Hansen, B.A. Angelsen, and C. Davies Mechanisms of the ultrasound-mediated intracellular delivery of liposomes and dextrans IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60 1 2013 21 33
24. W. Zhong, W.H. Sit, J.M. Wan, and A.C. Yu Sonoporation induces apoptosis and cell cycle arrest in human promyelocytic leukemia cell Ultrasound Med. Biol. 37 12 2011 2149 2159
25. L. Reslan, J.L. Mestas, S. Herveau, J.C. Bera, and C. Dumontet Transfection of cells in suspension by ultrasound cavitation J. Control. Release 142 2 2010 251 258
26. K. Okada, N. Kudo, K. Niwa, and K. Yamamoto A basic study on sonoporation with microbubbles exposed to pulsed ultrasound J. Med. Ultrason. 32 1 2005 3 11
27. C.X. Deng, F. Sieling, H. Pan, and J. Cui Ultrasound-induced cell membrane porosity Ultrasound Med. Biol. 30 4 2004 519 526
28. Y. Zhou, C.K. Yang, J. Cui, J.Y. Ye, and C.X. Deng Controlled permeation of cell membrane by single bubble acoustic cavitation J. Control. Release 157 1 2012 103 111
29. Z. Fan, H. Liu, M. Mayer, and C.X. Deng Spatiotemporally controlled single cell sonoporation Proc. Natl. Acad. Sci. U. S. A. 109 41 2012 16486 16491
30. J. Sundaram, B.R. Mellein, and S. Mitragotri An experimental and theoretical analysis of ultrasound-induced permeabilization of cell membranes Biophys. J. 84 5 2003 3087 3101
31. E.A. Brujan, T. Ikeda, and Y. Matsumoto Jet formation and shock wave emission during collapse of ultrasound-induced cavitation bubbles and their role in the therapeutic applications of high-intensity focused ultrasound Phys. Med. Biol. 50 20 2005 4797 4809
32. M. Postema, A. van Wamel, F.J. ten Cate, and N. de Jong High-speed photography during ultrasound illustrates potential therapeutic applications of microbubbles Med. Phys. 32 12 2005 3707 3711
33. N. Kudo, K. Okada, and K. Yamamoto Sonoporation by single-shot pulsed ultrasound with microbubbles adjacent to cells Biophys. J. 96 12 2009 4866 4876
34. B. Wolfrum, R. Mettin, T. Kurz, and W. Lauterbon Observations of pressure-wave-excited contrast agent bubbles in the vicinity of cells Appl. Phys. Lett. 81 26 2002 5060 5062
35. H. Chen, W. Kreider, A.A. Brayman, M.R. Bailey, and T.J. Matula Blood vessel deformation on microsecond time scales by ultrasonic cavitation Phys. Rev. Lett. 106 3 2011 034301
36. C.D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse Sonoporation from jetting cavitation bubbles Biophys. J. 91 11 2006 4285 4295
37. P. Marmottant, and S. Hilgenfeldt Controlled vesicle deformation and lysis by single oscillating bubbles Nature 423 6936 2003 153 156
38. H. Chen, A.A. Brayman, and T.J. Matula Characteristic microvessel relaxation timescales associated with ultrasound-activated microbubbles Appl. Phys. Lett. 101 16 2012 163704
39. A.A. Brayman, M.L. Coppage, S. Vaidya, and M.W. Miller Transient poration and cell surface receptor removal from human lymphocytes in vitro by 1 MHz ultrasound Ultrasound Med. Biol. 25 6 1999 999 1008
40. K. Kooiman, M. Foppen-Harteveld, A.F. van der Steen, and N. de Jong Sonoporation of endothelial cells by vibrating targeted microbubbles J. Control. Release 154 1 2011 35 41
41. M. Kinoshita, and K. Hynynen key factors that affect sonoporation efficiency in in-vitro settings: the importance of standing wave in sonoporation Biochem. Biophys. Res. Commun. 359 4 2007 860 865
42. H.R. Guzman, D.X. Nquyen, S. Khan, and M.R. Prausnitz Ultrasound-mediated disruption of cell membranes. I. Quantification of molecular uptake and cell viability J. Acoust. Soc. Am. 110 1 2001 588 596
43. Y.W. Han, A. Ikegami, P. Chung, L. Zhang, and C.X. Deng Sonoporation is an efficient tool for intracellular fluorescent dextran delivery and one-step double-crossover mutant construction in Fusobacterium nucleatum Appl. Environ. Microbiol. 73 11 2007 3677 3683
44. M.M. Forbes, R.L. Steinberg, and W.D. O'Brien Jr. Examination of inertial cavitation of Optison™ in producing sonoporation of Chinese hamster ovary cells Ultrasound Med. Biol. 34 12 2008 2009 2018
45. F. Yang, N. Gu, D. Chen, X. Xi, D. Zhang, Y. Li, and J. Wu Experimental study on cell self-sealing during sonoporation J. Control. Release 131 3 2008 205 210
46. R. Karshafian, P.D. Bevan, R. Williams, S. Samac, and P.N. Burns Sonoporation by ultrasound-activated microbubble contrast agents: effect of acoustic exposure parameters on cell membrane permeability and cell viability Ultrasound Med. Biol. 35 5 2009 847 860
47. M.M. Forbes, R.L. Steinberg, and W.D. O'Brien Jr. Frequency-dependent evaluation of the role of definity in producing sonoporation of Chinese hamster ovary cells J. Ultrasound Med 30 1 2011 61 69
48. M.M. Forbes, and W.D. O'Brien 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 2012 2723 2729
49. Y. Qiu, C. Zhang, J. Tu, and D. Zhang Microbubble-induced sonoporation involved in ultrasound-mediated DNA transfection in vitro at low acoustic pressures J. Biomech. 45 8 2012 1339 1345
50. M. Bazan-Peregrino, C.D. Arvanitis, B. Rifai, L.W. Seymour, and C.C. Coussios Ultrasound-induced cavitation enhances the delivery and therapeutic efficacy of an oncolytic virus in an in vitro model J. Control. Release 157 2 2012 235 242
51. J.M. Escoffre, A. Novell, J. Piron, A. Zeghimi, A. Doinikov, and A. Bouakaz Microbubble attenuation and destruction: are they involved in sonoporation efficiency IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60 1 2013 46 52
52. ® microbubbles J. Drug Target. 21 4 2013 407 414
53. H. Ando, L.B. Feril Jr., T. Kondo, Y. Tabuchi, R. Oqawa, Q.L. Zhao, Z.G. Cui, S. Umemura, H. Yoshikawa, and T. Misaki An echo-contrast agent, Levovist, lowers the ultrasound intensity required to induce apoptosis of human leukemia cells Cancer Lett. 242 1 2006 37 45
54. Y.Z. Zhao, Y.K. Luo, C.T. Lu, J.F. Xu, J. Tang, M. Zhang, Y. Zhang, and H.D. Liang Phospholipids-based microbubbles sonoporation pore size and reseal of cell membrane cultured in vitro J. Drug Target. 16 1 2008 18 25
55. S. Cancelos, F.J. Moraga, R.T. Lahey, W. Shain, and R.H. Parsons The effect of acoustically-induced cavitation on the permeance of a bullfrog urinary bladder J. Acoust. Soc. Am. 128 5 2010 2726 2738
56. Z.K. Liao, K.C. Tsai, H.T. Wang, S.H. Tseng, W.P. Deng, W.S. Chen, and L.H. Hwang Sonoporation-mediated anti-angiogenic gene transfer into muscle effectively regresses distant orthotopic tumors Cancer Gene Ther. 19 3 2012 171 180
57. H. Pan, Y. Zhou, O. Izadneqahdar, J. Cui, and C.X. Deng Study of sonoporation dynamics affected by ultrasound duty cycle Ultrasound Med. Biol. 31 6 2005 849 856
58. Y. Zhou Study of Single Cell Sonoporation in Real Time Using Electrophysiology Techniques 2008 Case Western Reserve University
59. L. van Ruijssevelt, P. Smirnov, A. Yudina, V. Bouchaud, P. Voisin, and C. Moonen Observations on the viability of C6-glioma cells after sonoporation with low-intensity ultrasound and microbubbles IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60 1 2013 34 45
60. M. Tamosiunas, R. Jurkonis, L.M. Mir, A. Lukosevicius, M.S. Venslauskas, and S. Satkauskas Microbubble sonodestruction rate as a metric to evaluate sonoporation efficiency J. Ultrasound Med. 31 12 2012 1993 2000
61. M. Ward, J. Wu, and J.F. Chiu Experimental study of the effects of Optison concentration on sonoporation in vitro Ultrasound Med. Biol. 26 7 2000 1169 1175
62. Z. Fan, R.E. Kumon, J. Park, and C.X. Deng Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles J. Control. Release 142 1 2010 31 39
63. J. Wu, J. Pepe, and M. Rincon Sonoporation, anti-cancer drug and antibody delivery using ultrasound Ultrasonics 44 Suppl. 1 2006 e21 e25
64. S. Pichardo, M. Toqtema, R. Jackson, I. Zehbe, and L. Curiel Influence of cell line and cell cycle phase on sonoporation transfection efficiency in cervical carcinoma cells under the same physical conditions IEEE Trans. Ultrason. Freq. Control 60 2 2013 432 435
65. I. Lentacker, N. Wang, R.E. Vandenbroucke, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound exposure of lipoplex loaded microbubbles facilitates direct cytoplasmic entry of the lipoplexes Mol. Pharm. 6 2 2009 457 467
66. B. Geers, I. Lentacker, A. Alonso, N.N. Sanders, J. Demeester, S. Meairs, and S.C. De Smedt Elucidating the mechanisms behind sonoporation with adeno-associated virus-loaded microbubbles Mol. Pharm. 8 6 2011 2244 2251
67. R.E. Vandenbroucke, I. Lentacker, J. Demeester, S.C. De Smedt, and N.N. Sanders Ultrasound assisted siRNA delivery using PEG-siPlex loaded microbubbles J. Control. Release 126 2008 265 273
68. B.D. Meijering, L.J. Juffermans, A. van Wamel, R.H. Henning, I.S. Zuhorn, M. Emmer, A.M. Versteilen, W.J. Paulus, W.H. van Gilst, K. Kooiman, N. de Jong, R.J. Musters, L.E. Deelman, and O. Kamp Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation Circ. Res. 104 5 2009 679 687
69. X. Zheng, P. Ji, and J. Hu Sonoporation using microbubbles promotes lipofectamine-mediated siRNA transduction to rat retina Bosn. J. Basic Med. Sci. 11 3 2011 147 152
70. J.L. Lee, C.W. Lo, S.M. Ka, A. Chen, and W.S. Chen Prolonging the expression duration of ultrasound-mediated gene transfection using PEI nanoparticles J. Control. Release 160 1 2012 64 71
71. Y. Zhou, J. Shi, J. Cui, and C.X. Deng Effects of extracellular calcium on cell membrane resealing in sonoporation J. Control. Release 126 1 2008 34 43
72. A. van Wamel, K. Kooiman, M. Emmer, F.J. ten Cate, M. Versluis, and N. de Jong Ultrasound microbubble induced endothelial cell permeability J. Control. Release 116 2 2006 e100 e102
73. L.J. Juffermans, A. van Dijk, C.A. Jongenelen, B. Drukarch, A. Reijerkerk, H.E. de Vries, O. Kamp, and R.J. Musters Ultrasound and microbubble-induced intra- and intercellular bioeffects in primary endothelial cells Ultrasound Med. Biol. 35 11 2009 1917 1927
74. L.B. Feril Jr., T. Kondo, Z.G. Cui, Y. Tabuchi, Q.L. Zhao, H. Ando, T. Misaki, H. Yoshikawa, and S. Umemura Apoptosis induced by the sonomechanical effects of low intensity pulsed ultrasound in a human leukemia cell line Cancer Lett. 221 2 2005 145 152
75. H.L. Roderick, and S.J. Cook Ca2 + signaling checkpoints in cancer: remodeling Ca2 + for cancer cell proliferation and survival Nat. Rev. Cancer 8 5 2008 361 375
76. H. Yu, L. Xu, and S.P. Chen A transfer efficiency model for ultrasound mediated drug/gene transferring into cells Ultrason. Sonochem. 21 1 2014 113 120
77. M. Borden, S. Sirsi, S. Hernandez, S. Homma, J. Kandel, and D. Yamashiro Polyplex-microbubbles for improved ultrasound-mediated gene therapy J. Acoust. Soc. Am. 133 5 2013 3409
78. Y. Yamashita, M. Shimada, K. Tachibana, N. Harimoto, E. Tsujita, K. Shirabe, J. Miyazaki, and K. Sugimachi In vivo gene transfer into muscle via electro-sonoporation Hum. Gene Ther. 13 17 2002 2079 2084
79. Y.C. Chen, L.P. Jiang, N.X. Liu, L. Ding, X.L. Liu, Z.H. Wang, K. Hong, and Q.P. Zhang Enhanced gene transduction into skeletal muscle of mice in vivo with pluronic block copolymers and ultrasound exposure Cell Biochem. Biophys. 60 3 2011 267 273
80. D. Sheyn, N. Kimelman-Bleich, G. Pelled, Y. Zilberman, D. Gazit, and Z. Gazit Ultrasound-based nonviral gene delivery induces bone formation in vivo Gene Ther. 15 4 2008 257 266
81. M. Saito, O. Mazda, K.A. Takahashi, Y. Arai, T. Kishida, M. Shin-Ya, A. Inoue, H. Tonomura, K. Sakao, T. Morihara, J. Imanishi, M. Kawata, and T. Kubo Sonoporation mediated transduction of pDNA/siRNA into joint synovium in vivo J. Orthop. Res. 25 10 2007 1308 1316
82. M. Togtema, S. Pichardo, R. Jackson, P.F. Lambert, L. Curiel, and I. Zehbe Sonoporation delivery of monoclonal antibodies against human papillomavirus 16 E6 restores p53 expression in transformed cervical keratinocytes PLoS One 7 11 2012 e50730
83. O. Zolochevska, X. Xia, B.J. Williams, A. Ramsay, S. Li, and M.L. Figueiredo Sonoporation delivery of interleukin-27 gene therapy efficiently reduces prostate tumor cell growth in vivo Hum. Gene Ther. 22 12 2011 1537 1550
84. M. Matsuo, K. Yamaguchi, L.B. Feril Jr., H. Endo, K. Ogawa, K. Tachibana, and J. Nakayama Synergistic inhibition of malignant melanoma proliferation by melphalan combined with ultrasound and microbubbles Ultrason. Sonochem. 18 5 2011 1218 1224
85. G. Casey, J.P. Cashman, D. Morrissey, M.C. Whelan, J.O. Larkin, D.M. Soden, M. Tangney, and G.C. O'Sullivan Sonoporation mediated immunogene therapy of solid tumors Ultrasound Med. Biol. 36 3 2010 430 440
86. R. Suzuki, E. Namai, Y. Oda, N. Nishiie, S. Otake, R. Koshima, K. Hirata, Y. Taira, N. Utoguchi, Y. Negishi, S. Nakagawa, and K. Maruyama Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure J. Control. Release 142 2 2010 245 250
87. Y. Sakakima, S. Hayashi, Y. Yagi, A. Hayakawa, K. Tachibana, and A. Nakao Gene therapy for hepatocellular carcinoma using sonoporation enhanced by contrast agents Cancer Gene Ther. 12 11 2005 884 889
88. L. Lei, Z.H. Liu, S. Ohta, and G. Yamada In vivo transduction of EGFP into female mouse reproductive system by electroporation and microbubble-enhanced sonoporation Fen Zi Xi Bao Sheng Wu Xue Bao 39 4 2006 378 382
89. O. Barreiro, R.J. Aguilar, E. Tejera, D. Megías, F. de Torres-Alba, A. Evangelista, and F. Sánchez-Madrid Specific targeting of human inflamed endothelium and in situ vascular tissue transfection by the use of ultrasound contrast agents JACC Cardiovasc. Imaging 2 8 2009 997 1005
90. L. Kowalczuk, M. Boudinet, M. El Sanharawi, E. Touchard, M.C. Naud, A. Saïed, J.C. Jeanny, F. Behar-Cohen, and P. Laugier In vivo gene transfer into the ocular ciliary muscle mediated by ultrasound and microbubbles Ultrasound Med. Biol. 37 11 2011 1814 1827