Basic Features of a Cell Electroporation Model: Illustrative Behavior for Two Very Different Pulses
Open accessAbstract
Science increasingly involves complex modeling. Here we describe a model for cell electroporation in which membrane properties are dynamically modified by poration. Spatial scales range from cell membrane thickness (5 nm) to a typical mammalian cell radius (10 μm), and can be used with idealized and experimental pulse waveforms. The model consists of traditional passive components and additional active components representing nonequilibrium processes. Model responses include measurable quantities: transmembrane voltage, membrane electrical conductance, and solute transport rates and amounts for the representative "long" and "short" pulses. The long pulse--1.5 kV/cm, 100 μs--evolves two pore subpopulations with a valley at ~5 nm, which separates the subpopulations that have peaks at ~1.5 and ~12 nm radius. Such pulses are widely used in biological research, biotechnology, and medicine, including cancer therapy by drug delivery and nonthermal physical tumor ablation by causing necrosis. The short pulse--40 kV/cm, 10 ns--creates 80-fold more pores, all small (<3 nm; ~1 nm peak). These nanosecond pulses ablate tumors by apoptosis. We demonstrate the model's responses by illustrative electrical and poration behavior, and transport of calcein and propidium. We then identify extensions for expanding modeling capability. Structure-function results from MD can allow extrapolations that bring response specificity to cell membranes based on their lipid composition. After a pulse, changes in pore energy landscape can be included over seconds to minutes, by mechanisms such as cell swelling and pulse-induced chemical reactions that slowly alter pore behavior.
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Electroporation pulses can range from nanoseconds to milliseconds in duration and tend to form aqueous pores in the plasma membrane that are on the order of ~1 nm in radius.
“Electroporation pulses can range from nanoseconds to milliseconds in duration and tend to form aqueous pores in the plasma membrane that are on the order of ~1 nm in radius [60,62,63,64].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [60]
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Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.96 · Cited by 2,421 · see citing works
Atomic-level characterization of the structural dynamics of proteins
Shaw, D. E., Maragakis, P., Lindorff-Larsen, K., Piana, S., Dror, R. O., Eastwood, M. P., Bank, J. A., Jumper, J. M., Salmon, J. K., Shan, Y., et al. (2010) · Science · doi:10.1126/science.1187409 · Cited by 1,923 · see citing works
Theory of electroporation: A review
Weaver, J. C., & Chizmadzhev, Y. A. (1996) · Bioelectrochemistry and Bioenergetics · doi:10.1016/s0302-4598(96)05062-3 · Cited by 1,611 · see citing works
Self-citationTissue Ablation with Irreversible Electroporation
Davalos, R. V., Mir, L. M., & Rubinsky, B. (2005) · Annals of Biomedical Engineering · doi:10.1007/s10439-005-8981-8 · Cited by 1,296 · see citing works
PARSEGIAN, A. (1969) · Nature · doi:10.1038/221844a0 · Cited by 854 · see citing works
Reversible electrical breakdown of lipid bilayers: formation and evolution of pores
Glaser, R. W., Leikin, S., Chernomordik, L., Pastushenko, V. F., & Sokirko, A. V. (1988) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(88)90202-7 · Cited by 611 · see citing works
Gothelf, A., Mir, L. M., & Gehl, J. (2003) · Cancer Treatment Reviews · doi:10.1016/s0305-7372(03)00073-2 · Cited by 549 · see citing works
Intracellular effect of ultrashort electrical pulses
Schoenbach, K. H., Beebe, S. J., & Buescher, E. S. (2001) · Bioelectromagnetics · doi:10.1002/bem.71 · Cited by 548 · see citing works
Abiror, I. G., Arakelyan, V. B., Chernomordik, L. V., Chizmadzhev, Y. A., Pastushenko, V. F., & Tarasevich, M. R. (1979) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(79)85005-9 · Cited by 540 · see citing works
Membrane Electroporation: A Molecular Dynamics Simulation
Tarek, M. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.050617 · Cited by 516 · see citing works
Nanosecond pulsed electric fields cause melanomas to self-destruct
Nuccitelli, R., Pliquett, U. F., Chen, X., et al. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.02.181 · Cited by 513 · see citing works
Modeling Electroporation in a Single Cell
Krassowska, W., & Filev, P. D. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.094235 · Cited by 501 · see citing works
Nanosecond, high‐intensity pulsed electric fields induce apoptosis in human cells
Beebe, S. J., Fox, P. M., Rec, L. J., Willis, L. K., & Schoenbach, K. H. (2003) · The FASEB Journal · doi:10.1096/fj.02-0859fje · Cited by 465 · see citing works
Simulation of Pore Formation in Lipid Bilayers by Mechanical Stress and Electric Fields
Tieleman, D. P., Leontiadou, H., Mark, A. E., & Marrink, . J. (2003) · Journal of the American Chemical Society · doi:10.1021/ja029504i · Cited by 459 · see citing works
Modeling Electroporation in a Single Cell. I. Effects of Field Strength and Rest Potential
DeBruin, K. A., & Krassowska, W. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)76973-0 · Cited by 449 · see citing works
The molecular basis of electroporation
Tieleman, D. P. (2004) · BMC Biochemistry · doi:10.1186/1471-2091-5-10 · Cited by 440 · see citing works
Beebe, S. J., Fox, P. M., Rec, L. J., Somers, K. D., Stark, R. H., & Schoenbach, K. H. (2002) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2002.1003872 · Cited by 422 · see citing works
Über die Impedanz einer Suspension von kugelförmigen Teilchen mit einer Schale
Pauly, H., & Schwan, H. P. (1959) · Zeitschrift für Naturforschung B · doi:10.1515/znb-1959-0213 · Cited by 409 · see citing works
Reversible electrical breakdown of lipid bilayer membranes: A charge-pulse relaxation study
Benz, R., Beckers, F., & Zimmermann, U. S. (1979) · The Journal of Membrane Biology · doi:10.1007/bf01872858 · Cited by 365 · see citing works
Asymptotic model of electroporation
Neu, J. C., & Krassowska, W. (1999) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.59.3471 · Cited by 325 · see citing works
Böckmann, R. A., de Groot, B. L., Kakorin, S., et al. (2008) · Biophysical Journal · doi:10.1529/biophysj.108.129437 · Cited by 321 · see citing works
Nanoelectropulse-driven membrane perturbation and small molecule permeabilization
Vernier, P. T., Sun, Y. H., & Gundersen, M. A. (2006) · BMC Cell Biology · doi:10.1186/1471-2121-7-37 · Cited by 320 · see citing works
Self-citationKotnik, T., & Miklavčič, D. (2006) · Biophysical Journal · doi:10.1529/biophysj.105.070771 · Cited by 318 · cited 5× · see citing works
“Close examination reveals a much thinner green band near the membrane around the anodic pole, with two small green areas away from the anodic pole— these areas are transition regions that favor large pores (DeBruin and Krassowska 1999a; Krassowska and Filev 2007; Smith 2011).”
BackgroundMethodInfluentialCancer Cells Ablation with Irreversible Electroporation
Miller, L., Leor, J., & Rubinsky, B. (2005) · Technology in Cancer Research & Treatment · doi:10.1177/153303460500400615 · Cited by 298 · see citing works
Pakhomov, A. G., Kolb, J. F., White, J. A., Joshi, R. P., Xiao, S. H., & Schoenbach, K. H. (2007) · Bioelectromagnetics · doi:10.1002/bem.20354 · Cited by 294 · see citing works
(1982) · Current topics in membranes and transport · doi:10.1016/s0070-2161(08)x6032-0 · Cited by 291 · see citing works
Weaver, J. C., Smith, K. C., Esser, A. T., Son, R. S., & Gowrishankar, T. R. (2012) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2012.02.007 · Cited by 291 · see citing works
Self-citationOsmotic pressure-induced pores in phospholipid vesicles
Taupin, C., Dvolaitzky, M., & Sauterey, C. (1975) · Biochemistry · doi:10.1021/bi00692a032 · Cited by 290 · see citing works
Mir, L. M., Banoun, H., & Paoletti, C. (1988) · Experimental Cell Research · doi:10.1016/0014-4827(88)90251-0 · Cited by 283 · see citing works
Stability of lipid bilayers and red blood cell membranes
Litster, J. D. (1975) · Physics Letters A · doi:10.1016/0375-9601(75)90402-8 · Cited by 282 · see citing works
Electroporation of cell membrane visualized under a pulsed-laser fluorescence microscope
Kinosita, K., Ashikawa, I., Saita, N., Yoshimura, H., Itoh, H., Nagayama, K., & Ikegami, A. (1988) · Biophysical Journal · doi:10.1016/s0006-3495(88)83181-3 · Cited by 275 · see citing works
Melikov, K., Frolov, V. A., Shcherbakov, A., et al. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)76153-x · Cited by 268 · see citing works
Quantitative cell biology with the Virtual Cell☆
Slepchenko, B. M., Schaff, J. C., Macara, I. G., & Loew, L. M. (2003) · Trends in Cell Biology · doi:10.1016/j.tcb.2003.09.002 · Cited by 257 · see citing works
Quantitative Study of Electroporation-Mediated Molecular Uptake and Cell Viability
Canatella, P. J., Karr, J. F., Petros, J. A., & Prausnitz, M. R. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)76055-9 · Cited by 256 · see citing works
The electrical breakdown of cell and lipid membranes: the similarity of phenomenologies
Chernomordik, L., Sukharev, S., Popov, S. V., Pastushenko, V. F., Sokirko, A. V., Abidor, I. G., & Chizmadzhev, Y. A. (1987) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(87)90204-5 · Cited by 247 · see citing works
Plasma Membrane Voltage Changes during Nanosecond Pulsed Electric Field Exposure
Frey, W., White, J. A., Price, R. O., Blackmore, P. F., Joshi, R. P., Nuccitelli, R., Beebe, S. J., Schoenbach, K. H., & Kolb, J. F. (2006) · Biophysical Journal · doi:10.1529/biophysj.105.072777 · Cited by 242 · see citing works
Direct Therapeutic Applications of Calcium Electroporation to Effectively Induce Tumor Necrosis
Frandsen, S. K., Gissel, H., Højman, P., Tramm, T., Eriksen, J., & Gehl, J. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3782 · Cited by 240 · see citing works
Levine, Z. A., & Vernier, P. T. (2010) · The Journal of Membrane Biology · doi:10.1007/s00232-010-9277-y · Cited by 232 · see citing works
Self-citationVery high cytotoxicity of bleomycin introduced into the cytosol of cells in culture
Poddevin, B., Orlowski, S., Belehradek, J., et al. (1991) · Biochemical Pharmacology · doi:10.1016/0006-2952(91)90394-k · Cited by 228 · see citing works
Medical applications of electroporation
Dev, S. B., Rabussay, D., Widera, G., & Hofmann, G. (2000) · IEEE Transactions on Plasma Science · doi:10.1109/27.842905 · Cited by 225 · see citing works
Microsecond and nanosecond electric pulses in cancer treatments
Breton, M., & Mir, L. M. (2011) · Bioelectromagnetics · doi:10.1002/bem.20692 · Cited by 223 · see citing works
Howland, J. (1992) · Biochemical Education · doi:10.1016/0307-4412(92)90213-6 · Cited by 223 · see citing works
Barnett, A., & Weaver, J. C. (1991) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(91)87001-w · Cited by 210 · see citing works
Self-citationAn approach to electrical modeling of single and multiple cells
Gowrishankar, T. R., & Weaver, J. C. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0636434100 · Cited by 204 · see citing works
Thermal and nonthermal mechanisms of interaction of radio-frequency energy with biological systems
Foster, K. R. (2000) · IEEE Transactions on Plasma Science · doi:10.1109/27.842819 · Cited by 202 · see citing works
Nonthermal Irreversible Electroporation: Fundamentals, Applications, and Challenges
Golberg, A., & Yarmush, M. L. (2013) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2013.2238672 · Cited by 198 · see citing works
Microdosimetry for conventional and supra-electroporation in cells with organelles
Gowrishankar, T. R., Esser, A. T., Vasilkoski, Z., Smith, K. C., & Weaver, J. C. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.01.094 · Cited by 198 · see citing works
Self-citationMembrane permeabilization and cell damage by ultrashort electric field shocks
Pakhomov, A. G., Shevin, R. S., White, J. A., Kolb, J. F., Pakhomova, O. N., Joshi, R. P., & Schoenbach, K. H. (2007) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2007.05.003 · Cited by 197 · see citing works
Model of Creation and Evolution of Stable Electropores for DNA Delivery
Smith, K. C., Neu, J. C., & Krassowska, W. (2004) · Biophysical Journal · doi:10.1016/s0006-3495(04)74334-9 · Cited by 189 · see citing works
Self-citationMolecular Dynamics Simulations of Lipid Membrane Electroporation
Delemotte, L., & Tarek, M. (2012) · The Journal of Membrane Biology · doi:10.1007/s00232-012-9434-6 · Cited by 188 · see citing works
Atomistic Simulations of Pore Formation and Closure in Lipid Bilayers
Bennett, W. F., Sapay, N., & Tieleman, D. P. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2013.11.4486 · Cited by 182 · see citing works
Garon, E. B., Sawcer, D., Vernier, P. T., et al. (2007) · International Journal of Cancer · doi:10.1002/ijc.22723 · Cited by 176 · see citing works
Self-citationMembrane electroporation: The absolute rate equation and nanosecond time scale pore creation
Vasilkoski, Z., Esser, A. T., Gowrishankar, T. R., & Weaver, J. C. (2006) · Physical Review E · doi:10.1103/physreve.74.021904 · Cited by 172 · see citing works
Self-citationNanosecond electric pulses cause mitochondrial membrane permeabilization in Jurkat cells
Napotnik, T. B., Wu, Y., Gundersen, M. A., Damijan Miklavčič, A., & Vernier, P. T. (2011) · Bioelectromagnetics · doi:10.1002/bem.20707 · Cited by 171 · see citing works
Self-citationCell electrofusion using nanosecond electric pulses
Rems, L., Ušaj, M., Kandušer, M., Reberšek, M., Damijan Miklavčič, A., & Pucihar, G. (2013) · Scientific Reports · doi:10.1038/srep03382 · Cited by 152 · see citing works
Second-order model of membrane electric field induced by alternating external electric fields
Kotnik, T., & Miklavcic, D. (2000) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.855935 · Cited by 150 · cited 6× · see citing works
“explanations, here we present two versions of a basic passive cell model equation, often referred to as the Schwan equation in the spherical case (Pauly and Schwan 1959; Kotnik and Miklavčič 2000; Foster 2000; Kotnik and Miklavčič 2006).”
BackgroundMethodInfluentialVernier, P. T., Ziegler, M. J., Sun, Y. H., Chang, W. V., Gundersen, M. A., & Tieleman, D. P. (2006) · Journal of the American Chemical Society · doi:10.1021/ja0588306 · Cited by 147 · see citing works
Self-citationGarcia, P. A., Pancotto, T. E., Rossmeisl, J. H., et al. (2011) · Technology in Cancer Research & Treatment · doi:10.7785/tcrt.2012.500181 · Cited by 146 · see citing works
Bioelectric Effects of Intense Ultrashort Pulses
Schoenbach, K. H., & Joshi, R. P. (2010) · Critical Reviews in Biomedical Engineering · doi:10.1615/critrevbiomedeng.v38.i3.20 · Cited by 139 · see citing works
Quantitative model of small molecules uptake after in vitro cell electropermeabilization
Puc, M., Kotnik, T., Mir, L. M., et al. (2003) · Bioelectrochemistry · doi:10.1016/s1567-5394(03)00021-5 · Cited by 139 · see citing works
Damijan Miklavčič, A., Pucihar, G., Pavlovec, M., Ribarič, S., Mali, M., Maček-Lebar, A., Petkovšek, M., Nastran, J., Kranjc, S., Čemažar, M., et al. (2004) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2004.07.004 · Cited by 133 · see citing works
Optimal Parameters for the Destruction of Prostate Cancer Using Irreversible Electroporation
Rubinsky, J., Onik, G. M., Mikus, P., et al. (2008) · The Journal of Urology · doi:10.1016/j.juro.2008.08.003 · Cited by 130 · see citing works
Modeling Electroporation in a Single Cell. II. Effects of Ionic Concentrations
DeBruin, K. A., & Krassowska, W. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)76974-2 · Cited by 128 · see citing works
Gurtovenko, A. A., & Vattulainen, I. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.094797 · Cited by 123 · see citing works
Decreased bilayer stability due to transmembrane potentials
Weaver, J. C., & Mintzer, R. A. (1981) · Physics Letters A · doi:10.1016/0375-9601(81)90688-5 · Cited by 121 · see citing works
Self-citationGowrishankar, T. R., & Weaver, J. C. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.08.097 · Cited by 121 · see citing works
Self-citationION‐MEMBRANE INTERACTIONS AS STRUCTURAL FORCES
Parsegian, V. A. (1975) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1975.tb31481.x · Cited by 118 · see citing works
Transport Lattice Approach to Describing Cell Electroporation: Use of a Local Asymptotic Model
Stewart, D. A., Gowrishankar, T. R., & Weaver, J. C. (2004) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2004.832639 · Cited by 117 · see citing works
Self-citationFirst‐in‐human trial of nanoelectroablation therapy for basal cell carcinoma: proof of method
Nuccitelli, R., Wood, R., Kreis, M., et al. (2013) · Experimental Dermatology · doi:10.1111/exd.12303 · Cited by 116 · see citing works
Müller, K. J., Sukhorukov, V. L., & Zimmermann, U. S. (2001) · The Journal of Membrane Biology · doi:10.1007/s00232-001-0084-3 · Cited by 114 · see citing works
Atomic-level simulation of current–voltage relationships in single-file ion channels
Jensen, M. Ø., Jogini, V., Eastwood, M. P., et al. (2013) · The Journal of General Physiology · doi:10.1085/jgp.201210820 · Cited by 111 · see citing works
Electrical Impedance Tomography for Imaging Tissue Electroporation
Davalos, R. V., Otten, D. M., Mir, L. M., et al. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2004.824148 · Cited by 109 · see citing works
Mechanisms for the Intracellular Manipulation of Organelles by Conventional Electroporation
Esser, A. T., Smith, K. C., Gowrishankar, T. R., Vasilkoski, Z., & Weaver, J. C. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.02.035 · Cited by 105 · see citing works
Self-citationNumerical simulation of molecular uptake via electroporation
Li, J., & Lin, H. (2011) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2011.04.006 · Cited by 103 · see citing works
Esser, A. T., Smith, K. C., Gowrishankar, T. R., & Weaver, J. C. (2007) · Technology in Cancer Research & Treatment · doi:10.1177/153303460700600402 · Cited by 100 · see citing works
Self-citationSmith, K. C., & Weaver, J. C. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.121921 · Cited by 94 · see citing works
Self-citationNanosecond Field Alignment of Head Group and Water Dipoles in Electroporating Phospholipid Bilayers
Vernier, P. T., & Ziegler, M. J. (2007) · The Journal of Physical Chemistry B · doi:10.1021/jp077148q · Cited by 92 · see citing works
Self-citationNagaoka, T., Kunieda, E., & Watanabe, S. (2008) · Physics in Medicine and Biology · doi:10.1088/0031-9155/53/23/004 · Cited by 88 · see citing works
Silve, A., Leray, I., & Mir, L. M. (2011) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2011.10.002 · Cited by 80 · see citing works
Pauly, H., & Hp, S. (1959) · PubMed · Cited by 77 · see citing works
Water influx and cell swelling after nanosecond electropermeabilization
Romeo, S., Wu, Y., Levine, Z. A., et al. (2013) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2013.03.007 · Cited by 69 · see citing works
Size-controlled nanopores in lipid membranes with stabilizing electric fields
Fernández, M. L., Risk, M. R., Reigada, R., et al. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.05.122 · Cited by 68 · see citing works
Electroporation of Intracellular Liposomes Using Nanosecond Electric Pulses—A Theoretical Study
Rems, L., Pucihar, G., & Damijan Miklavčič, A. (2013) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2013.2262177 · Cited by 68 · see citing works
Novel Passive Element Circuits for Microdosimetry of Nanosecond Pulsed Electric Fields
Merla, C., Denzi, A., Paffi, A., Casciola, M., d'Inzeo, G., Apollonio, F., & Liberti, M. (2012) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2012.2203133 · Cited by 66 · see citing works
Towards Solid Tumor Treatment by Nanosecond Pulsed Electric Fields
Esser, A. T., Smith, K. C., Gowrishankar, T. R., & Weaver, J. C. (2009) · Technology in Cancer Research & Treatment · doi:10.1177/153303460900800406 · Cited by 57 · see citing works
Self-citationMerla, C., Paffi, A., Apollonio, F., Lévêque, P., d'Inzeo, G., & Liberti, M. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2010.2104150 · Cited by 55 · see citing works
Modulation of intracellular Ca2+ levels in chromaffin cells by nanoelectropulses
Craviso, G. L., Choe, S., Chatterjee, I., & Vernier, P. T. (2011) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2011.11.016 · Cited by 52 · see citing works
Self-citationPliquett, U. F., Gift, E. A., & Weaver, J. C. (1996) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(95)05031-0 · Cited by 52 · see citing works
Self-citationEmergence of a large pore subpopulation during electroporating pulses
Smith, K. C., Son, R. S., Gowrishankar, T. R., et al. (2013) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2013.10.009 · Cited by 50 · see citing works
Self-citationModelling single cell electroporation with bipolar pulse parameters and dynamic pore radii
Talele, S., Gaynor, P. T., Cree, M. J., & van Ekeren, J. (2010) · Journal of Electrostatics · doi:10.1016/j.elstat.2010.02.001 · Cited by 40 · see citing works
Quantification of propidium iodide delivery using millisecond electric pulses: Experiments
Sadik, M., Li, J., Shan, J. W., et al. (2013) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2013.01.002 · Cited by 38 · see citing works
Transmembrane potential measurements on plant cells using the voltage-sensitive dye ANNINE-6
Flickinger, B., Berghöfer, T., Hohenberger, P., et al. (2010) · PROTOPLASMA · doi:10.1007/s00709-010-0131-y · Cited by 38 · see citing works
Ionic conductivity of electroporated lipid bilayer membranes
Kakorin, S., & Neumann, E. (2002) · Bioelectrochemistry · doi:10.1016/s1567-5394(02)00040-3 · Cited by 37 · see citing works
Transmembrane molecular transport during versus after extremely large, nanosecond electric pulses
Smith, K. C., & Weaver, J. C. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.06.171 · Cited by 34 · see citing works
Self-citationPastushenko, V. F., Arakelyan, V. B., & Chizmadzhev, Y. A. (1979) · Bioelectrochemistry and Bioenergetics · doi:10.1016/0302-4598(79)85010-2 · Cited by 31 · see citing works
Theoretical and Experimental Analysis of Electroporated Membrane Conductance in Cell Suspension
Suzuki, D. O. H., Ramos, A., Ribeiro, M. F. S. F. C., et al. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2010.2103074 · Cited by 31 · see citing works
Mastering Conformal Meshing for Complex CAD-Based C-FDTD Simulations
Benkler, S., Chavannes, N., & Kuster, N. (2008) · IEEE Antennas and Propagation Magazine · doi:10.1109/map.2008.4562256 · Cited by 27 · see citing works
A unified model of electroporation and molecular transport
Smith, K. C. (2011) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 25 · see citing works
Self-citationThe effects of external fields on the structure of lipid bilayers.
Sugár, I. P. (1981) · PubMed · Cited by 25 · see citing works
Elia, S., Lamberti, P., & Tucci, V. (2010) · IEEE Transactions on NanoBioscience · doi:10.1109/tnb.2010.2050599 · Cited by 18 · see citing works
Cationic Peptide Exposure Enhances Pulsed-Electric-Field-Mediated Membrane Disruption
Kennedy, S. M., Aiken, E. J., Beres, K. A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092528 · Cited by 15 · see citing works
Smith, K. C., & Weaver, J. C. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2011.2180378 · Cited by 15 · see citing works
Self-citationModel of pore formation in a single cell in a flow-through channel with micro-electrodes
Kaner, A., Braslavsky, I., & Rubinsky, B. (2013) · Biomedical Microdevices · doi:10.1007/s10544-013-9820-6 · Cited by 10 · see citing works
Gowrishankar, T. R., Esser, A. T., Smith, K. C., et al. (2011) · doi:10.1109/iembs.2011.6090166 · Cited by 9 · see citing works
Self-citationYao, C., Li, C., Mi, Y., et al. (2005) · doi:10.1109/iembs.2005.1615401 · Cited by 5 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Rubinsky B Irreversible electroporation 2010 Berlin Springer
Cited by
Sorted by citations
Membrane Electroporation and Electropermeabilization: Mechanisms and Models
Kotnik, T., Rems, L., Tarek, M., & Miklavčič, D. (2019) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-052118-115451 · Cited by 813 · see citing works
Permeabilizing Cell Membranes with Electric Fields
Aguilar, A. A., Ho, M. C., Chang, E., Carlson, K. W., Natarajan, A., Marciano, T., Bomzon, Z., & Patel, C. B. (2021) · Cancers · doi:10.3390/cancers13092283 · Cited by 76 · see citing works
Burke, R. C., Bardet, S. M., Carr, L., Romanenko, S., Arnaud-Cormos, D., Leveque, P., & O'Connor, R. P. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.07.004 · Cited by 58 · see citing works
- Authors
- Son, R. S., Smith, K. C., Gowrishankar, T. R., Vernier, P. T., & Weaver, J. C.
- Affiliations
- Harvard–MIT Division of Health Sciences and Technology (US)
- Massachusetts General Hospital (US)
- Old Dominion University (US)
- Corresponding author
- Weaver, James C.
- Venue
- The Journal of Membrane Biology
- Published
- 2014-07-22
- Volume
- 247
- Issue
- 12
- Pages
- 1209-1228
- ISSN
- 0022-2631 (ISSN-L)
- 1432-1424
- PMC
- PMC4224743
- OpenAlex
- W1849302557
- Cited by
- 99
- References
- 105
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 9 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 10 · 2019: 7 · 2018: 8 · 2017: 20 · 2016: 9 · 2015: 9 · 2014: 1
- FWCI
- 11.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- The Journal of Membrane Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- ODU Digital Commons (Old Dominion University) (submittedVersion, cc-by)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation
- University of Southern California
- National Institutes of Health
- National Institute of General Medical Sciences (GM063857, R01GM063857)
- Air Force Office of Scientific Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Plasma Applications and Diagnostics
- Physical Sciences › Engineering › Control and Systems Engineering › Pulsed Power Technology Applications
- Keywords
- cell electroporation, membrane poration, nanosecond pulses, long pulses, transmembrane voltage, solute transport, calcein, propidium, membrane lipid composition, tumor ablation, apoptosis, drug delivery
- MeSH terms
- Animals, Biological Transport, Cell Membrane, Electric Conductivity, Fluoresceins, Mammals, Models, Biological, Propidium, Porosity, Electroporation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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