Physical methods for drug and gene delivery through the cell plasma membrane

Advances in Anatomy Embryology and Cell Biology

Volumn 227, Issue , 2017, Pages 73-92

  Jakutavičiūtė, Milda ^a   Ruzgys, Paulius ^a   Tamošiūnas, Mindaugas ^a   Maciulevičius, Martynas ^a   Šatkauskas, Saulius ^a  

^a VYTAUTAS MAGNUS UNIVERSITY   (Lithuania)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE; DRUG DELIVERY SYSTEM; ELECTROCHEMOTHERAPY; ELECTROPORATION; GENE TRANSFER; HUMAN; METABOLISM;

CELL MEMBRANE; DRUG DELIVERY SYSTEMS; ELECTROCHEMOTHERAPY; ELECTROPORATION; GENE TRANSFER TECHNIQUES; HUMANS;

EID: 85030705346     PISSN: 03015556     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-3-319-56895-9_5     Document Type: Chapter

References (137)

1. Antov Y, Barbul A, Mantsur H, Korenstein R (2005) Electroendocytosis: exposure of cells to pulsed low electric fields enhances adsorption and uptake of macromolecules. Biophys J 88:22062223. doi:10.1529/biophysj.104.051268
2. Balmayor ER, Azevedo HS, Reis RL (2011) Controlled delivery systems: from pharmaceuticals to cells and genes. Pharm Res 28:1241-1258. doi:10.1007/s11095-011-0392-y
3. Belehradek M, Domenge C, Luboinski B et al (1993) Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial. Cancer 72:3694-3700
4. Bernhardt J, Pauly H (1973) On the generation of potential differences across the membranes of ellipsoidal cells in an alternating electrical field. Biophysik 10:89-98
5. Bonamassa B, Hai L, Liu D (2011) Hydrodynamic gene delivery and its applications in pharmaceutical research. Pharm Res 28:694-701. doi:10.1007/s11095-010-0338-9
6. Boulaiz H, Marchal JA, Prados J et al (2005) Non-viral and viral vectors for gene therapy. Cell Mol Biol (Noisy-le-Grand) 51:3-22
7. Bureau MF, Gehl J, Deleuze V et al (2000) Importance of association between permeabilization and electrophoretic forces for intramuscular DNA electrotransfer. Biochim Biophys Acta 1474:353-359
8. Calvet CY, Mir LM (2016) The promising alliance of anti-cancer electrochemotherapy with immunotherapy. Cancer Metastasis Rev 35:165-177. doi:10.1007/s10555-016-9615-3
9. Canatella PJ, Karr JF, Petros JA, Prausnitz MR (2001) Quantitative study of electroporation-mediated molecular uptake and cell viability. Biophys J 80:755-764. doi: 10.1016/S0006-3495(01)76055-9
10. Casey G, Cashman JP, Morrissey D et al (2010) Sonoporation mediated immunogene therapy of solid tumors. Ultrasound Med Biol 36:430-440. doi:10.1016/j.ultrasmedbio.2009.11.005
11. Celis JE (1977) Injection of tRNAs into somatic cells: search for in vivo systems to assay potential nonsense mutations in somatic cells. Brookhaven Symp Biol 29:178-196
12. Cepurniene K, Ruzgys P, Treinys R et al (2010) Influence of plasmid concentration on DNA electrotransfer in vitro using high-voltage and low-voltage pulses. J Membr Biol 236:81-85. doi:10.1007/s00232-010-9270-5
13. Chang C-C, Wu M, Yuan F (2014) Role of specific endocytic pathways in electrotransfection of cells. Mol Ther Methods Clin Dev 1:14058. doi:10.1038/mtm.2014.58
14. Chen D-R, Wendt CH, Pui DYH (2000) A novel approach for introducing bio-materials into cells. J Nanopart Res 2:133-139. doi:10.1023/A:1010084032006
15. Chen J-Y, Liao Y-L, Wang T-H, Lee W-C (2006) Transformation of Escherichia coli mediated by magnetic nanoparticles in pulsed magnetic field. Enzym Microb Technol 39:366-370. doi:10.1016/j.enzmictec.2005.11.035
16. Das AK, Gupta P, Chakraborty D (2015) Physical methods of gene transfer: Kinetics of gene delivery into cells: A Review. Agric Rev 36:61. doi:10.5958/0976-0741.2015.00007.0
17. Daud AI, DeConti RC, Andrews S et al (2008) Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 26:5896-5903. doi:10.1200/JCO.2007.15.6794
18. De Cock I, Zagato E, Braeckmans K et al (2015) Ultrasound and microbubble mediated drug delivery: acoustic pressure as determinant for uptake via membrane pores or endocytosis. J Control Release 197:20-28. doi:10.1016/j.jconrel.2014.10.031
19. Deng CX, Sieling F, Pan H, Cui J (2004) Ultrasound-induced cell membrane porosity. Ultrasound Med Biol 30:519-526. doi:10.1016/j.ultrasmedbio.2004.01.005
20. Didenko YT, McNamara III WB, Suslick KS (1999) Hot spot conditions during cavitation in water. J Am Chem Soc. doi: 10.1021/JA9844635
21. Dimcevski G, Kotopoulis S, Bjanes T et al (2016) A human clinical trial using ultrasound and microbubbles to enhance gemcitabine treatment of inoperable pancreatic cancer. J Control Release 243:172-181. doi:10.1016/j.jconrel.2016.10.007
22. Djuzenova CS, Zimmermann U, Frank H et al (1996) Effect of medium conductivity and composition on the uptake of propidium iodide into electropermeabilized myeloma cells. Biochim Biophys Acta 1284:143-152
23. Doukas AG, Flotte TJ, Akhamanov S et al (1996) Physical characteristics and biological effects oflaser-induced stress waves. Ultrasound Med Biol 22:151-164. doi:10.1016/0301-5629(95)02026-8
24. Duvshani-Eshet M, Baruch L, Kesselman E et al (2006) Therapeutic ultrasound-mediated DNA to cell and nucleus: bioeffects revealed by confocal and atomic force microscopy. Gene Ther 13:163-172. doi:10.1038/sj.gt.3302642
25. Endo-Takahashi Y, Negishi Y, Nakamura A et al (2013) pDNA-loaded bubble liposomes as potential ultrasound imaging and gene delivery agents. Biomaterials 34:2807-2813. doi:10.1016/j. biomaterials.2012.12.018
26. Endo-Takahashi Y, Negishi Y, Nakamura A et al (2014) Systemic delivery of miR-126 by miRNA-loaded bubble liposomes for the treatment of hindlimb ischemia. Sci Rep 4:3883. doi:10.1038/srep03883
27. Escoffre J-M, Portet T, Favard C et al (2011) Electromediated formation of DNA complexes with cell membranes and its consequences for gene delivery. Biochim Biophys Acta Biomembr 1808:1538-1543. doi:10.1016/j.bbamem.2010.10.009
28. Escoffre J-M, Novell A, Piron J et al (2013a) Microbubble attenuation and destruction: are they involved in sonoporation efficiency? IEEE Trans Ultrason Ferroelectr Freq Control 60:46-52. doi:10.1109/TUFFC.2013.2536
29. Escoffre J-M, Zeghimi A, Novell A, Bouakaz A (2013b) In-vivo gene delivery by sonoporation: recent progress and prospects. Curr Gene Ther 13:2-14
30. Eynard N, Sixou S, Duran N, Teissie J (1992) Fast kinetics studies of Escherichia coli electrotransformation. Eur J Biochem 209:431-436
31. Fan Z, Kumon RE, Park J, Deng CX (2010) Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J Control Release 142:31-39. doi:10.1016/j. jconrel.2009.09.031
32. Faurie C, Golzio M, Moller P et al (2003) Cell and animal imaging of electrically mediated gene transfer. DNA Cell Biol 22:777-783. doi:10.1089/104454903322624984
33. Faurie C, Phez E, Golzio M et al (2004) Effect of electric field vectoriality on electrically mediated gene delivery in mammalian cells. Biochim Biophys Acta Biomembr 1665:92-100. doi:10.1016/j.bbamem.2004.06.018
34. Faurie C, Rebersek M, Golzio M et al (2010) Electro-mediated gene transfer and expression are controlled by the life-time of DNA/membrane complex formation. J Gene Med 12:117-125. doi:10.1002/jgm.1414
35. Fraites T, Mah CS, Zolotukhin I (2000) Microsphere-mediated delivery of recombinant AAV vectors in vitro and in vivo. Mol Ther 1:S239
36. Gabriel B, Teissie J (1997) Direct observation in the millisecond time range of fluorescent molecule asymmetrical interaction with the electropermeabilized cell membrane. Biophys J 73:2630-2637. doi:10.1016/S0006-3495(97)78292-4
37. Gabriel B, Teissie J (1998) Mammalian cell electropermeabilization as revealed by millisecond imaging of fluorescence changes of ethidium bromide in interaction with the membrane. Bioelectrochem Bioenerg 47:113-118. doi:10.1016/S0302-4598(98)00174-3
38. Gabriel B, Teissie J (1999) Time courses of mammalian cell electropermeabilization observed by millisecond imaging of membrane property changes during the pulse. Biophys J 76:21582165. doi:10.1016/S0006-3495(99)77370-4
39. Geers B, Lentacker I, Sanders NN et al (2011) Self-assembled liposome-loaded microbubbles: the missing link for safe and efficient ultrasound triggered drug-delivery. J Control Release 152:249-256. doi:10.1016/j.jconrel.2011.02.024
40. Golzio M, Teissié J, Rols M-P (2002) Cell synchronization effect on mammalian cell permeabili-zation and gene delivery by electric field. Biochim Biophys Acta 1563:23-28
41. Haberl S, Kanduser M, Flisar K et al (2013) Effect of different parameters used for in vitro gene electrotransfer on gene expression efficiency, cell viability and visualization of plasmid DNA at the membrane level. J Gene Med 15:169-181. doi:10.1002/jgm.2706
42. Hibino M, Shigemori M, Itoh H et al (1991) Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys J 59:209-220. doi:10.1016/S0006-3495(91)82212-3
43. Hibino M, Itoh H, Kinosita K (1993) Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. Biophys J 64:1789-1800. doi:10.1016/S0006-3495(93)81550-9
44. Hooper JW, Kamrud KI, Elgh F et al (1999) DNA vaccination with hantavirus M segment elicits neutralizing antibodies and protects against Seoul virus infection. Virology 255:269-278. doi:10.1006/viro.1998.9586
45. Hradetzky D, Boehringer S, Geiser T, Gazdhar A (2012) An approach towards bronchoscopic-based gene therapy using electrical field accelerated plasmid droplets. In: 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE, pp 5753-5756
46. Ikemoto K, Sakata I, Sakai T (2012) Collision of millimetre droplets induces DNA and protein transfection into cells. Sci Rep. doi:10.1038/srep00289
47. Irvine KR, Rao JB, Rosenberg SA, Restifo NP (1996) Cytokine enhancement of DNA immunization leads to effective treatment of established pulmonary metastases. J Immunol 156:238-245
48. Juffermans LJM, Meijering BDM, Henning RH, Deelman LE (2014) Ultrasound and microbubble-targeted delivery of small interfering RNA into primary endothelial cells is more effective than delivery of plasmid DNA. Ultrasound Med Biol 40:532-540. doi:10.1016/j. ultrasmedbio.2013.09.031
49. Kanduser M, Miklavcic D, Pavlin M (2009) Mechanisms involved in gene electrotransfer using high-and low-voltage pulses-an in vitro study. Bioelectrochemistry 74:265-271. doi:10.1016/j.bioelechem.2008.09.002
50. Kardos TJ, Rabussay DP (2012) Contactless magneto-permeabilization for intracellular plasmid DNA delivery in-vivo. Hum Vaccin Immunother 8:1707-1713. doi:10.4161/hv.21576
51. Klatzmann D, Chérin P, Bensimon G et al (1998) A phase I/II dose-escalation study of herpes simplex virus type 1 thymidine kinase “suicide” gene therapy for metastatic melanoma. Hum Gene Ther 9:2585-2594. doi:10.1089/hum.1998.9.17-2585
52. Klein TM, Wolf ED, Wu R, Sanford JC (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327:70-73. doi:10.1038/327070a0
53. Klenchin VA, Frye JJ, Jones MH et al (2011) Structure-function analysis of the C-terminal domain of CNM67, a core component of the Saccharomyces cerevisiae spindle pole body. J Biol Chem 286:18240-18250. doi: 10.1074/jbc.M111.227371
54. Kobayashi N, Nishikawa M, Hirata K, Takakura Y (2004) Hydrodynamics-based procedure involves transient hyperpermeability in the hepatic cellular membrane: implication of a nonspecific process in efficient intracellular gene delivery. J Gene Med 6:584-592. doi:10.1002/jgm.541
55. Kooiman K, Foppen-Harteveld M, van der Steen AFW, de Jong N (2011) Sonoporation of endothelial cells by vibrating targeted microbubbles. J Control Release 154:35-41. doi:10.1016/j. jconrel.2011.04.008
56. Kotopoulis S, Dimcevski G, Gilja OH et al (2013) Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med Phys 40:72902. doi:10.1118/1.4808149
57. Kudo N, Okada K, Yamamoto K (2009) Sonoporation by single-shot pulsed ultrasound with microbubbles adjacent to cells. Biophys J 96:4866-4876. doi:10.1016/j.bpj.2009.02.072
58. Lai C-Y, Wu C-H, Chen C-C, Li P-C (2006) Quantitative relations of acoustic inertial cavitation with sonoporation and cell viability. Ultrasound Med Biol 32:1931-1941. doi:10.1016/j. ultrasmedbio.2006.06.020
59. Lakshmanan S, Gupta GK, Avci P et al (2014) Physical energy for drug delivery; poration, concentration and activation. Adv Drug Deliv Rev 71:98-114. doi:10.1016/j.addr.2013.05.010
60. ® microbubbles. J Drug Target 21:407-414. doi:10.3109/1061186X.2012.761223
61. Lentacker I, Geers B, Demeester J et al (2010) Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: cytotoxicity and mechanisms involved. Mol Ther 18:101-108. doi:10.1038/mt.2009.160
62. Lentacker I, De Cock I, Deckers R et al (2014) Understanding ultrasound induced sonoporation: definitions and underlying mechanisms. Adv Drug Deliv Rev 72:49-64. doi:10.1016/j. addr.2013.11.008
63. Lin MTS, Pulkkinen L, Uitto J, Yoon K (2000) The gene gun: current applications in cutaneous gene therapy. Int J Dermatol 39:161-170. doi:10.1046/j.1365-4362.2000.00925.x
64. Liu F, Song YK, Liu D (1999) Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther 6:1258-1266. doi:10.1038/sj.gt.3300947
65. Liu D, Wang L, Wang Z, Cuschieri A (2012) Magnetoporation and magnetolysis of cancer cells via carbon nanotubes induced by rotating magnetic fields. Nano Lett 12:5117-5121. doi:10.1021/nl301928z
66. Maciulevicius M, Tamosiunas M, Jurkonis R et al (2015) Analysis of metrics for molecular Sonotransfer in vitro. Mol Pharm 12:3620-3627. doi:10.1021/acs.molpharmaceut.5b00347
67. Markovskaja S, Novickij V, Grainys A, Novickij J (2014) Irreversible magnetoporation of microorganisms in high pulsed magnetic fields. IET Nanobiotechnol 8:157-162. doi:10.1049/iet-nbt.2013.0005
68. Marmottant P, Hilgenfeldt S (2003) Controlled vesicle deformation and lysis by single oscillating bubbles. Nature 423:153-156. doi:10.1038/nature01613
69. Marty M, Sersa G, Garbay JR et al (2006) Electrochemotherapy-an easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: results of ESOPE (European standard operating procedures of Electrochemotherapy) study. Eur J Cancer Suppl 4:3-13. doi:10.1016/j.ejcsup.2006.08.002
70. Mehier-Humbert S, Bettinger T, Yan F, Guy RH (2005a) Plasma membrane poration induced by ultrasound exposure: implication for drug delivery. J Control Release 104:213-222. doi:10.1016/j.jconrel.2005.01.007
71. Mehier-Humbert S, Bettinger T, Yan F, Guy RH (2005b) Ultrasound-mediated gene delivery: kinetics of plasmid internalization and gene expression. J Control Release 104:203-211. doi:10.1016/j.jconrel.2005.01.011
72. Meijering BDM, Juffermans LJM, van Wamel A et al (2009) Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ Res 104:679-687. doi:10.1161/CIRCRESAHA.108.183806
73. Mir O (1999) Mechanisms of electrochemotherapy. Adv Drug Deliv Rev 35:107-118
74. Mohanty SK, Sharma M, Gupta PK (2003) Laser-assisted microinjection into targeted animal cells. Biotechnol Lett 25:895-899
75. Namgung R, Singha K, Yu MK et al (2010) Hybrid superparamagnetic iron oxide nanoparticle-branched polyethylenimine magnetoplexes for gene transfection of vascular endothelial cells. Biomaterials 31:4204-4213. doi:10.1016/j.biomaterials.2010.01.123
76. Neumann E, Rosenheck K (1972) Permeability changes induced by electric impulses in vesicular membranes. J Membr Biol 10:279-290
77. Noack J, Vogel A (1995) Streak-photographic investigation of shock wave emission after laser-induced plasma formation in water. In: Jacques SL (ed). International Society for Optics and Photonics, p 284
78. Ohl C-D, Arora M, Ikink R et al (2006) Sonoporation from jetting cavitation bubbles. Biophys J 91:4285-4295. doi:10.1529/biophysj.105.075366
79. Okubo Y, Ikemoto K, Koike K et al (2008) DNA introduction into living cells by water droplet impact with an electrospray process. Angew Chemie Int Ed 47:1429-1431. doi:10.1002/anie.200704429
80. Panje CM, Wang DS, Pysz MA et al (2012) Ultrasound-mediated gene delivery with cationic versus neutral microbubbles: effect of DNA and microbubble dose on in vivo transfection efficiency. Theranostics 2:1078-1091. doi:10.7150/thno.4240
81. Paterson L, Agate B, Comrie M et al (2005) Photoporation and cell transfection using a violet diode laser. Opt Express 13:595-600
82. Pavlin M, Kanduser M (2015) New insights into the mechanisms of gene electrotransfer-experimental and theoretical analysis. Sci Rep 5:9132. doi:10.1038/srep09132
83. Pavlin M, Flisar K, Kanduser M (2010) The role of electrophoresis in gene electrotransfer. J Membr Biol 236:75-79. doi:10.1007/s00232-010-9276-z
84. Pitsillides CM, Joe EK, Wei X et al (2003) Selective cell targeting with light-absorbing microparticles and nanoparticles. Biophys J 84:4023-4032. doi:10.1016/S0006-3495(03)75128-5
85. Pucihar G, Kotnik T, Miklavcic D, Teissié J (2008) Kinetics of transmembrane transport of small molecules into electropermeabilized cells. Biophys J 95:2837-2848. doi:10.1529/biophysj.108.135541
86. Qiu Y, Luo Y, Zhang Y et al (2010) The correlation between acoustic cavitation and sonopora-tion involved in ultrasound-mediated DNA transfection with polyethylenimine (PEI) in vitro. J Control Release 145:40-48. doi:10.1016/j.jconrel.2010.04.010
87. Rapoport N, Gao Z, Kennedy A (2007) Multifunctional nanoparticles for combining ultrasonic tumor imaging and targeted chemotherapy. JNCI J Natl Cancer Inst 99:1095-1106. doi: 10.1093/jnci/djm043
88. Rapoport NY, Kennedy AM, Shea JE et al (2009) Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles. J Control Release 138:268-276. doi:10.1016/j.jconrel.2009.05.026
89. Rols MP, Teissié J (1990) Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. Biophys J 58:1089-1098. doi:10.1016/S0006-3495(90)82451-6
90. Rols M-P, Teissié J (1998) Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. Biophys J 75:1415-1423. doi:10.1016/S0006-3495(98)74060-3
91. Rosazza C, Escoffre J-M, Zumbusch A, Rols M-P (2011) The actin cytoskeleton has an active role in the electrotransfer of plasmid DNA in mammalian cells. Mol Ther 19:913-921. doi:10.1038/mt.2010.303
92. Rosazza C, Buntz A, Rieß T et al (2013) Intracellular tracking of single-plasmid DNA particles after delivery by electroporation. Mol Ther 21:2217-2226. doi:10.1038/mt.2013.182
93. Rosazza C, Deschout H, Buntz A et al (2016) Endocytosis and endosomal trafficking of DNA after gene electrotransfer in vitro. Mol Ther Nucleic Acids 5:e286. doi:10.1038/mtna.2015.59
94. Sadik MM, Li J, Shan JW et al (2013) Quantification of propidium iodide delivery using millisecond electric pulses: experiments. Biochim Biophys Acta 1828:1322-1328. doi:10.1016/j. bbamem.2013.01.002
95. Sakakima Y, Hayashi S, Yagi Y et al (2005) Gene therapy for hepatocellular carcinoma using sonoporation enhanced by contrast agents. Cancer Gene Ther 12:884-889. doi:10.1038/sj.cgt.7700850
96. Satkauskas S, Bureau MF, Puc M et al (2002) Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther 5:133140. doi:10.1006/mthe.2002.0526
97. Satkauskas S, André F, Bureau MF et al (2005) Electrophoretic component of electric pulses determines the efficacy of in vivo DNA electrotransfer. Hum Gene Ther 16:1194-1201. doi:10.1089/hum.2005.16.1194
98. Schlicher RK, Radhakrishna H, Tolentino TP et al (2006) Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med Biol 32:915-924. doi:10.1016/j.ultrasmedbio.2006.02.1416
99. Sersa G, Stabuc B, Cemazar M et al (1998) Electrochemotherapy with cisplatin: potentiation of local cisplatin antitumour effectiveness by application of electric pulses in cancer patients. Eur J Cancer 34:1213-1218
100. Suda T, Liu D (2007) Hydrodynamic gene delivery: its principles and applications. Mol Ther 15:2063-2069. doi:10.1038/sj.mt.6300314
101. Sukharev SI, Klenchin VA, Serov SM et al (1992) Electroporation and electrophoretic DNA transfer into cells. The effect of DNA interaction with electropores. Biophys J 63:1320-1327. doi:10.1016/S0006-3495(92)81709-5
102. Sundaram J, Mellein BR, Mitragotri S (2003) An experimental and theoretical analysis of ultrasound-induced permeabilization of cell membranes. Biophys J 84:3087-3101. doi:10.1016/S0006-3495(03)70034-4
103. Suzuki R, Namai E, Oda Y et al (2010) Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release 142:245-250. doi:10.1016/j. jconrel.2009.10.027
104. Tamosiünas M, Jurkonis R, Mir LM et al (2012a) Adjustment of ultrasound exposure duration to microbubble sonodestruction kinetics for optimal cell sonoporation in vitro. Technol Cancer Res Treat 11:375-387. doi:10.7785/tcrt.2012.500285
105. Tamosiünas M, Jurkonis R, Mir LM et al (2012b) Microbubble sonodestruction rate as a metric to evaluate sonoporation efficiency. J Ultrasound Med 31:1993-2000
106. Tamosiünas M, Mir LM, Chen W-S et al (2016) Intracellular delivery of bleomycin by combined application of electroporation and sonoporation in vitro. J Membr Biol 249:677-689. doi:10.1007/s00232-016-9911-4
107. Tao W, Wilkinson J, Stanbridge EJ, Berns MW (1987) Direct gene transfer into human cultured cells facilitated by laser micropuncture of the cell membrane. Proc Natl Acad Sci U S A 84:4180-4184
108. Teissié J, Rols MP (1993) An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization. Biophys J 65:409-413. doi:10.1016/S0006-3495(93)81052-X
109. Tekle E, Astumian RD, Chock PB (1994) Selective and asymmetric molecular transport across electroporated cell membranes. Proc Natl Acad Sci U S A 91:11512-11516
110. Ting C-Y, Fan C-H, Liu H-L et al (2012) Concurrent blood-brain barrier opening and local drug delivery using drug-carrying microbubbles and focused ultrasound for brain glioma treatment. Biomaterials 33:704-712. doi:10.1016/j.biomaterials.2011.09.096
111. Tiwari G, Tiwari R, Sriwastawa B et al (2012) Drug delivery systems: an updated review. Int J Pharm Investig 2:2-11. doi:10.4103/2230-973X.96920
112. Tlaxca JL, Rychak JJ, Ernst PB et al (2013) 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 165:216-225. doi:10.1016/j. jconrel.2012.10.021
113. Treat LH, McDannold N, Zhang Y et al (2012) Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma. Ultrasound Med Biol 38:1716-1725. doi:10.1016/j.ultrasmedbio.2012.04.015
114. Tresilwised N, Pithayanukul P, Mykhaylyk O et al (2010) Boosting oncolytic adenovirus potency with magnetic nanoparticles and magnetic force. Mol Pharm 7:1069-1089. doi:10.1021/mp100123t
115. Tsukakoshi M, Kurata S, Nomiya Y et al (1984) A novel method of DNA transfection by laser microbeam cell surgery. Appl Phys B Photophysics Laser Chem 35:135-140. doi:10.1007/BF00697702
116. Umebayashi Y, Miyamoto Y, Wakita M et al (2003) Elevation of plasma membrane permeability on laser irradiation of extracellular latex particles. J Biochem 134:219-224
117. Vaughan EE, Dean DA (2006) Intracellular trafficking of plasmids during transfection is mediated by microtubules. Mol Ther 13:422-428. doi:10.1016/j.ymthe.2005.10.004
118. Venslauskas MS, Satkauskas S, Rodaitè-Risevicienè R (2010) Efficiency of the delivery of small charged molecules into cells in vitro. Bioelectrochemistry 79:130-135. doi:10.1016/j.bioelechem.2009.10.003
119. Vogel A, Busch S (1994) Time-resolved measurements of shock-wave emission and cavitation-bubble generation in intraocular laser surgery with ps-and ns-pulses. Springer Netherlands, New York, pp 105-117
120. van Wamel A, Kooiman K, Harteveld M et al (2006) Vibrating microbubbles poking individual cells: drug transfer into cells via sonoporation. J Control Release 112:149-155. doi:10.1016/j.jconrel.2006.02.007
121. Wang DS, Panje C, Pysz MA et al (2012) Cationic versus neutral microbubbles for ultrasoundmediated gene delivery in cancer. Radiology 264:721-732. doi:10.1148/radiol.12112368
122. Wang W, Li W, Ma N, Steinhoff G (2013) Non-viral gene delivery methods. Curr Pharm Biotechnol 14:46-60
123. Weaver JC, Chizmadzhev YA (1996) Theory of electroporation: a review. Bioelectrochem Bioenerg 41:135-160. doi:10.1016/S0302-4598(96)05062-3
124. Williams RS, Johnston SA, Riedy M et al (1991) Introduction of foreign genes into tissues of living mice by DNA-coated microprojectiles. Proc Natl Acad Sci U S A 88:2726-2730. doi:10.1073/PNAS.88.7.2726
125. Wolf H, Rols MP, Boldt E et al (1994) Control by pulse parameters of electric field-mediated gene transfer in mammalian cells. Biophys J 66:524-531
126. Wu M, Yuan F (2011) Membrane binding of plasmid DNA and endocytic pathways are involved in electrotransfection of mammalian cells. PLoS One 6:e20923. doi:10.1371/journal. pone.0020923
127. Yan F, Li L, Deng Z et al (2013) Paclitaxel-liposome-microbubble complexes as ultrasound-triggered therapeutic drug delivery carriers. J Control Release 166:246-255. doi:10.1016/j.jconrel.2012.12.025
128. Yao C-P, Zhang Z-X, Rahmanzadeh R, Huettmann G (2008) Laser-based gene transfection and gene therapy. IEEE Trans Nanobioscience 7:111-119. doi:10.1109/TNB.2008.2000742
129. Yin T, Wang P, Li J et al (2013) Ultrasound-sensitive siRNA-loaded nanobubbles formed by hetero-assembly of polymeric micelles and liposomes and their therapeutic effect in gliomas. Biomaterials 34:4532-4543. doi:10.1016/j.biomaterials.2013.02.067
130. Yin T, Wang P, Li J et al (2014) Tumor-penetrating codelivery of siRNA and paclitaxel with ultrasound-responsive nanobubbles hetero-assembled from polymeric micelles and liposomes. Biomaterials 35:5932-5943. doi:10.1016/j.biomaterials.2014.03.072
131. Yu M, Tan W, Lin H (2012) A stochastic model for DNA translocation through an electropore.Biochim Biophys Acta 1818:2494-2501. doi:10.1016/j.bbamem.2012.05.025
132. Zeghimi A, Escoffre JM, Bouakaz A (2015) Role of endocytosis in sonoporation-mediated membrane permeabilization and uptake of small molecules: a electron microscopy study. Phys Biol 12:66007. doi:10.1088/1478-3975/12/6/066007
133. Zeira E, Manevitch A, Khatchatouriants A et al (2003) Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression. Mol Ther 8:342-350
134. Zhang G, Gao X, Song YK et al (2004) Hydroporation as the mechanism of hydrodynamic delivery. Gene Ther 11:675-682. doi:10.1038/sj.gt.3302210
135. Zhigang W, Zhiyu L, Haitao R et al (2004) Ultrasound-mediated microbubble destruction enhances VEGF gene delivery to the infarcted myocardium in rats. Clin Imaging 28:395-398. doi:10.1016/j.clinimag.2004.04.003
136. Zhou Y, Cui J, Deng CX (2008) Dynamics of sonoporation correlated with acoustic cavitation activities. Biophys J 94(7):L51-L53. doi: 10.1529/biophysj.107.125617
137. Zhou Y, Kumon RE, Cui J, Deng CX (2009) The size of sonoporation pores on the cell membrane. Ultrasound Med Biol 35:1756-1760. doi:10.1016/j.ultrasmedbio.2009.05.012