Time dependence of electric field effects on cell membranes. A review for a critical selection of pulse duration for therapeutical applications

Neumann E, Sowers AE, Jordan CA. Electroporation and electrofusion in cell biology. York: Plenum press; 1989.10.1007/978-1-4899-2528-2Search in Google Scholar

Orlowski S, Mir LM. Cell electropermeabilization: a new tool for biochemical and pharmacological studies. Biochim Biophys Acta 1993; 1154: 51-63.10.1016/0304-4157(93)90016-HSearch in Google Scholar

Eynard N, Rols MP, Ganeva V, Galutzov B, Sabri N, Teissié J. Electrotransformation pathways of procaryotic and eucaryotic cells: recents developments. Bioelectrochem Bioenerg 1997; 44: 103-10.10.1016/S0302-4598(97)00038-XSearch in Google Scholar

Mir LM, Roth C, Orlowski S, Quintin Colonna F, Fradelizi D, et al. Systemic antitumor effects of electrochemotherapy combined with histoincompatible cells secreting interleukin-2. Systemic antitumor effects of electrochemotherapy combined with histoincompatible cells secreting interleukin-2. J Immunother Emphasis Tumor Immunol 1995; 17: 30-8.10.1097/00002371-199501000-00004Search in Google Scholar

Cemazar M, Sersa G. Electrotransfer of therapeutic molecules into tissues. Curr Opin Mol Ther 2007; 9: 554-62.Search in Google Scholar

Sersa G, Miklavcic D, Cemazar M, Rudolf Z, Pucihar G, Snoj M. Electrochemotherapy in treatment of tumours. Eur J Surg Oncol 2008; 34: 232-40.10.1016/j.ejso.2007.05.016Search in Google Scholar

Mir LM, Gehl J, Sersa G, Collins CG, Garbay JR, Billard V, et al. Standard operating procedures of the electrochemotherapy: Instructions for the use of bleomycin or cisplatin administered either systemically or locally and electric pulses delivered by the CliniporatorTM by means of invasive or non-invasive electrodes Eur J Cancer 2006; 42(Suppl 4): 14-25.10.1016/j.ejcsup.2006.08.003Search in Google Scholar

Mir LM, Glass LF, Sersa G, Teissie J, Domenge C, Miklavcic D, et al. Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. Br J Cancer 1998; 77: 2336-42.10.1038/bjc.1998.388Search in Google Scholar

Prausnitz MR, Bose VG, Langer R, Weaver JC. Electroporation of mammalian skin: a mechanism to enhance transdermal drug delivery. Proc Natl Acad Sci USA 1993; 90: 10504-8.10.1073/pnas.90.22.10504Search in Google Scholar

Titomirov A, Sukarev S, Kistanova E. In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim Biophys Acta 1991; 1088: 131-4.10.1016/0167-4781(91)90162-FSearch in Google Scholar

Heller R, Jaroszeski M, Atkin A, Moradpour D, Gilbert R, Wands J, et al. In vivo gene electroinjection and expression in rat liver. FEBS Lett 1996; 389: 225-8.10.1016/0014-5793(96)00590-XSearch in Google Scholar

Rols MP, Delteil C, Golzio M, Dumond P, Cros S, Teissie J. In vivo electrically mediated protein and gene transfer in murine melanoma. Nat Biotechnol 1998; 16: 168-71.10.1038/nbt0298-168Search in Google Scholar

Aihara H, Miyazaki J. Gene transfer into muscle by electroporation in vivo. Nat Biotechnology 1998; 16: 867-70.10.1038/nbt0998-867Search in Google Scholar

Mir LM, Bureau MF, Rangara R, Schwartz B, Sherman D. Long-term, high level in vivo gene expression after electric pulse- mediated gene transfer into skeletal muscle. C R Acad Sci III 1998; 321: 893-9.10.1016/S0764-4469(99)80003-1Search in Google Scholar

Muramatsu T, Nakamura A, Park M. In vivo electroporation: A powerful and convenient means of nonviral gene transfer to tissues of living animals. [Review]. Int J Mol Med 1998; 1: 55-62.Search in Google Scholar

Pliquett U, Joshi RP, Sridhara V, Schoenbach KH. High electrical field effects on cell membranes. Bioelectrochemistry 2007; 70: 275-82.10.1016/j.bioelechem.2006.10.004Search in Google Scholar

Pakhomov AG, Kolb JF, White JA, Joshi RP, Xiao S, Schoenbach KH. Long-lasting plasma membrane permeabilization in mammalian cells by nanosecond pulsed electric field (nsPEF). Bioelectromagnetics 2007; 28: 655-63.10.1002/bem.20354Search in Google Scholar

Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1982; 1: 841-5.10.1002/j.1460-2075.1982.tb01257.xSearch in Google Scholar

Gross D, Loew LM, Webb WW. Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys J 1986; 50: 339-48.10.1016/S0006-3495(86)83467-1Search in Google Scholar

Lojewska Z, Farkas DL, Ehrenberg B, Loew LM. Analysis of the effect of medium and membrane conductance on the amplitude and kinetics of membrane potentials induced by externally applied electric fields. Biophys J 1989; 56: 121-8.10.1016/S0006-3495(89)82657-8Search in Google Scholar

Hibino M, Shigemori M, Itoh H, Nagayama K, Kinosita K jr. Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys J 1991; 59: 209-20.10.1016/S0006-3495(91)82212-3Search in Google Scholar

Kotnik T, Pucihar G, Rebersek M, Miklavcic D, Mir LM. Role of pulse shape in cell membrane electropermeabilization. Biochim Biophys Acta 2003; 1614: 193-200.10.1016/S0005-2736(03)00173-1Search in Google Scholar

Pucihar G, Kotnik T, Valic B, Miklavcic D. Numerical determination of transmembrane voltage induced on irregularly shaped cells. Ann Biomed Eng 2006; 34: 642-52.10.1007/s10439-005-9076-2Search in Google Scholar

Valic B, Golzio M, Pavlin M, Schatz A, Faurie C, Gabriel B, et al. Effect of electric field induced transmembrane potential on spheroidal cells: theory and experiment. Eur Biophys J 2003; 32: 519-28.10.1007/s00249-003-0296-9Search in Google Scholar

Teissié J, Tsong TY. Electric field induced transient pores in phospholipid bilayer vesicles. Biochemistry 1981; 20: 1548-54.10.1021/bi00509a022Search in Google Scholar

Teissié J, Rols MP. An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization. Biophys J 1993; 65: 409-13.10.1016/S0006-3495(93)81052-XSearch in Google Scholar

Rols MP, Teissie J. Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. Biophys J 1990; 58: 1089-98.10.1016/S0006-3495(90)82451-6Search in Google Scholar

Gabriel B, Teissie J. Direct observation in the millisecond time range of fluorescent molecule asymmetrical interaction with the electropermeabilized cell membrane. Biophys J 1997; 73: 2630-7.10.1016/S0006-3495(97)78292-4Search in Google Scholar

Gabriel B, Teissie J. Time courses of mammalian cell electropermeabilization observed by millisecond imaging of membrane property changes during the pulse. Biophys J 1999; 76: 2158-65.10.1016/S0006-3495(99)77370-4Search in Google Scholar

Pucihar G, Kotnik T, Miklavic D, Teissie J. Kinetics of transmembrane transport of small molecules into electropermeabilized cells. Biophys J 2008; 95: 2837-48.10.1529/biophysj.108.135541Search in Google Scholar

Rols MP, Delteil C, Golzio M, Teissie J. Control by ATP and ADP of voltage-induced mammalian-cell-membrane permeabilization, gene transfer and resulting expression. Eur J Biochem 1998; 254: 382-8.10.1046/j.1432-1327.1998.2540382.xSearch in Google Scholar

Pucihar G, Mir LM, Miklavcic D. The effect of pulse repetition frequency on the uptake into electropermeabilized cells in vitro with possible applications in electrochemotherapy. Bioelectrochemistry 2002; 57: 167-72.10.1016/S1567-5394(02)00116-0Search in Google Scholar

Teissie J, Rols MP. Manipulation of cell cytoskeleton affects the lifetime of cell membrane electropermeabilization. Ann N Y Acad Sci 1994; 720: 98-110.10.1111/j.1749-6632.1994.tb30438.xSearch in Google Scholar

Kinosita K Jr, Tsong TY. Voltage-induced conductance in human erythrocyte membranes. Biochim Biophys Acta 1979; 554: 479-97.10.1016/0005-2736(79)90386-9Search in Google Scholar

Gabriel B, Teissie J. Generation of reactive-oxygen species induced by electropermeabilization of Chinese hamster ovary cells and their consequence on cell viability. Eur J Biochem 1994; 223: 25-33.10.1111/j.1432-1033.1994.tb18962.xSearch in Google Scholar

Kinosita K Jr, Tsong TY. Hemolysis of human erythrocytes by transient electric field. Proc Natl Acad Sci USA 1977; 74: 1923-7.10.1073/pnas.74.5.1923Search in Google Scholar

Golzio M, Mora MP, Raynaud C, Deltei C, Teissie J, Rols MP. Control by osmotic pressure of voltage-induced permeabilization and gene transfer in mammalian cells. Biophys J 1998; 74: 3015-22.10.1016/S0006-3495(98)78009-9Search in Google Scholar

Tsong TY. Electroporation of cell membranes. Biophys J 1991; 60: 297-306.10.1016/S0006-3495(91)82054-9Search in Google Scholar

Haest CW, Kamp D, Deuticke B. Transbilayer reorientation of phospholipid probes in the human erythrocyte membrane. Lessons from studies on electroporated and resealed cells. Biochim Biophys Acta 1997; 1325: 17-33.10.1016/S0005-2736(96)00239-8Search in Google Scholar

Rols MP, Teissie J. Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. Biophys J 1998; 75: 1415-23.10.1016/S0006-3495(98)74060-3Search in Google Scholar

Al-Sakere B, Andre F, Bernat C, Connault E, Opolon P, Davalos RV, et al. Tumor ablation with irreversible electroporation. PLoS ONE 2007; 2(11): e1135.10.1371/journal.pone.0001135Search in Google Scholar

Klenchin VA, Sukharev SI, Serov SM, Chernomordik LV, Chizmadzev YuA. Electrically induced DNA uptake by cells is a fast process involving DNA electrophoresis. Biophys J 1991; 60: 804-11.10.1016/S0006-3495(91)82115-4Search in Google Scholar

Wolf H, Rols MP, Boldt E, Neumann E, Teissie J. Control by pulse parameters of electric field-mediated gene transfer in mammalian cells. Biophys J 1994; 66: 524-31.10.1016/S0006-3495(94)80805-7Search in Google Scholar

Rols MP, Teissie J. Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. Biophys J 1998; 75: 1415-23.10.1016/S0006-3495(98)74060-3Search in Google Scholar

Golzio M, Teissie J, Rols MP. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci U S A 2002; 99: 1292-7.10.1073/pnas.02264649912218311818537Search in Google Scholar

Neumann E, Werner E, Sprafke A, Kruger K. Electroporation phenomena. Electrooptics of plasmid DNA and of lipid bilayer vesicles. In: Jennings BR, Stoylov SP, editors. Colloid and molecular electro-optics. Bristol: IOP publishing LTD; 1992. p. 197-206.Search in Google Scholar

Rols MP, Coulet D, Teissie J. Highly efficient transfection of mammalian cells by electric field pulses. Application to large volumes of cell culture by using a flow system. Eur J Biochem 1992; 206: 115-21.10.1111/j.1432-1033.1992.tb16908.x1316837Search in Google Scholar

Kubiniec RT, Liang H, Hui SW. Effects of pulse length and pulse strength on transfection by electroporation. Biotechniques 1990; 8: 16-20.Search in Google Scholar

Ferreira E, Potier E, Logeart-Avramoglou D, Salomskaite-Davalgiene S, Mir LM, Petite H. Optimization of a gene electrotransfer method for mesenchymal stem cell transfection. Gene Ther 2008; 15: 537-44.10.1038/gt.2008.918256695Search in Google Scholar

Frey W, White JA, Price RO, Blackmore PF, Joshi RP, Nuccitelli R, et al. Plasma membrane voltage changes during nanosecond pulsed electric field exposure. Biophys J 2006; 90: 3608-15.10.1529/biophysj.105.072777144074116513782Search in Google Scholar

Kotnik T, Miklavcic D. Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. Biophys J 2006; 90: 480-91.10.1529/biophysj.105.070771136705416239325Search in Google Scholar

Tekle E, Oubrahim H, Dzekunov SM, Kolb JF, Schoenbach KH, Chock PB. Selective field effects on intracellular vacuoles and vesicle membranes with nanosecond electric pulses. Biophys J 2005; 89: 274-84.10.1529/biophysj.104.054494136652515821165Search in Google Scholar

Muller KJ, Sukhorukov VL, Zimmermann U. Reversible electropermeabilization of mammalian cells by high-intensity, ultra-short pulses of submicrosecond duration. J Membr Biol 2001; 184: 161-70.10.1007/s00232-001-0084-311719852Search in Google Scholar

Sukhorukov VL, Mussauer H, Zimmermann U. The effect of electrical deformation forces on the electropermeabilization of erythrocyte membranes in low- and high-conductivity media. J Membr Biol 1998; 163: 235-45.10.1007/s0023299003879625780Search in Google Scholar

Beebe SJ, Fox PM, Rec LJ, Willis LK, Schoenbach KH. Nanosecond high intensity pulsed electric fields induce apoptosis in human cells. FASEB J 2003; 30: 286-292.10.1096/fj.02-0859fje12824299Search in Google Scholar

Vernier TP, Sun YH, Marcu L, Craft CM, Gundersen MA. Nanoelectropore-induced phosphatidylserine translocation. Biophys J 2004; 86: 4040-8.10.1529/biophysj.103.037945130430415189899Search in Google Scholar

Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG. Phosphatidylinositol 4,5-bisphosphate and Arf-regulated membrane traffic. J Biol Chem 2001; 154: 1007-17.Search in Google Scholar

White JA, Blackmore PF, Schoenbach KH, Beebe SJ. Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields. J Biol Chem 2004; 279: 22964-72.10.1074/jbc.M31113520015026420Search in Google Scholar

Nuccitelli R, Pliquet U, Chen X, Ford W, James Swanson R, Beebe SJ, et al. Nanosecond pulsed electric fields cause melanomas to self-destruct. Biochem Biophys Res Commun 2006; 343: 351-60.10.1016/j.bbrc.2006.02.181151354616545779Search in Google Scholar

Garon EB, Sawcer D, Vernier PT, Tang T, Sun Y, Marcu L, et al. In vitro and in vivo evaluation and a case report of intense nanosecond pulsed electric field as a local therapy for human malignancies. Int J Cancer 2007; 121: 675-82.10.1002/ijc.2272317417774Search in Google Scholar

Beebe SJ, White J, Blackmore PF, Deng Y, Somers K, Schoenbach KH. Diverse effects of nanosecond pulsed electric fields on cells and tissues. DNA Cell Biol 2003; 22: 785-96.10.1089/10445490332262499314683589Search in Google Scholar

Tarek M. Membrane electroporation: a molecular dynamics simulation. Biophys J 2005; 88: 4045-53.10.1529/biophysj.104.050617130563515764667Search in Google Scholar

Eynard N, Sixou S, Duran N, Teissie J. Fast kinetics studies of Escherichia coli electrotransformation. Eur J Biochem 1992; 209: 431-6.10.1111/j.1432-1033.1992.tb17306.x1396716Search in Google Scholar

Ganeva V, Galutzov B, Teissie J. Fast kinetic studies of plasmid DNA transfer in intact yeast cells mediated by electropulsation. Biochem Biophys Res Commun 1995; 214: 825-32.10.1006/bbrc.1995.23617575551Search in Google Scholar

Lebar AM, Sersa G, Kranjc S, Groselj A, Miklavcic D. Optimisation of pulse parameters in vitro for in vivo electrochemotherapy. Anticancer Res 2002; 22: 1731-6.Search in Google Scholar

Phez E, Faurie C, Golzio M, Teissié J, Rols MP. New insights in the visualization of membrane permeabilization and DNA/membrane interaction of cells submitted to electric pulses. Biochim Biophys Acta 2005; 1724: 248-54.10.1016/j.bbagen.2005.04.00515878640Search in Google Scholar