Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields
Open accessAbstract
Several reports have recently been published on effects of very short and intense electric pulses on cellular organelles; in a number of cases, the cell plasma membrane appeared to be affected less than certain organelle membranes, whereas with longer and less intense pulses the opposite is the case. The effects are the consequence of the voltages induced on the membranes, and in this article we investigate the conditions under which the induced voltage on an organelle membrane could exceed its counterpart on the cell membrane. This would provide a possible explanation of the observed effects of very short pulses. Frequency-domain analysis yields an insight into the dependence of the voltage inducement on the electric and geometric parameters characterizing the cell and its vicinity. We show that at sufficiently high field frequencies, for a range of parameter values the voltage induced on the organelle membrane can indeed exceed the voltage induced on the cell membrane. Particularly, this can occur if the organelle interior is electrically more conductive than the cytosol, or if the organelle membrane has a lower dielectric permittivity than the cell membrane, and we discuss the plausibility of these conditions. Time-domain analysis is then used to determine the courses of the voltage induced on the membranes by pulses with risetimes and durations in the nanosecond range. The particularly high resting voltage in mitochondria, to which the induced voltage superimposes, could contribute to the explanation why these organelles are the primary target of many observed effects.
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As the frequency of the field increases, the high membrane field gain diminishes, allowing for higher field intensities to penetrate into the cell.
“as the frequency of the field increases, the high membrane field gain diminishes, allowing for higher field intensities to penetrate into the cell.”
From An Overview of Sub-Cellular Mechanisms Involved in the Action of TTFields (2016) · cites this paper as [31]
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“However, other dielectric properties of the nucleus may affect the membrane charging time [35,61].”
BackgroundMethodRen, W., & Beebe, S. J. (2011) · APOPTOSIS · doi:10.1007/s10495-010-0572-y · Cited by 122 · see citing works
“Nevertheless, modeling evidence suggests that under certain circumstances it is possible to have effects on intracellular membranes without effects on the plasma membrane [18].”
BackgroundHaandbæk, N., Bürgel, S. C., Heer, F., & Hierlemann, A. R. (2013) · Lab on a Chip · doi:10.1039/c3lc50866h · Cited by 116 · see citing works
Recruitment of the intracellular Ca2+ by ultrashort electric stimuli: The impact of pulse duration
Semenov, I., Xiao, S. H., Pakhomova, O. N., & Pakhomov, A. G. (2013) · Cell Calcium · doi:10.1016/j.ceca.2013.05.008 · Cited by 116 · see citing works
“The formation of small membrane pores (“nanopores”), concurrently in both PM and intracellular membranes was supported by advanced numerical models [15, 16].”
Ibey, B. L., Cantu, J. C., Pakhomova, O. N., Roth, C. C., Semenov, I., Beier, H. T., Tarango, M., Xiao, S. H., Schoenbach, K. H., & Pakhomov, A. G. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.12.004 · Cited by 112 · see citing works
“While the high-frequency components present with short-duration pulses are believed to be less effective at PM permeabilization they are hypothesized to cause intracellular membrane permeabilization [14, 21, 22].”
Ye, H., & Steiger, A. (2015) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-015-0061-1 · Cited by 107 · see citing works
“Kotnik T, Miklavcic D. Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields.”
BackgroundInfluentialRecent Advances in Microscale Electroporation
Choi, S., Khoo, H., & Hur, S. C. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00677 · Cited by 108 · see citing works
Modulation of cell function by electric field: a high-resolution analysis
Taghian, T., Narmoneva, D. A., & Kogan, A. B. (2015) · Journal of The Royal Society Interface · doi:10.1098/rsif.2015.0153 · Cited by 105 · see citing works
“Several studies have modelled the cell as multiple concentric shells to determine the induced EF in the internal membranes [55,56].”
BackgroundCell membrane electroporation-Part 3: the equipment
Reberšek, M., Damijan Miklavčič, A., Bertacchini, C., & Sack, M. (2014) · IEEE Electrical Insulation Magazine · doi:10.1109/mei.2014.6804737 · Cited by 102 · see citing works
“An electroporator generates short HV pulses of specific shape, amplitude, duration, number, and repetition frequency [4], and the pulses are applied to the target cells or load through the electrodes [5].”
BackgroundBeebe, S. J., Chen, Y.-J., Sain, N. M., Schoenbach, K. H., & Xiao, S. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051349 · Cited by 100 · see citing works
“outer membranes [9], possibly making poration pervasive across whole cells.”
Basic Features of a Cell Electroporation Model: Illustrative Behavior for Two Very Different Pulses
Son, R. S., Smith, K. C., Gowrishankar, T. R., Vernier, P. T., & Weaver, J. C. (2014) · The Journal of Membrane Biology · doi:10.1007/s00232-014-9699-z · Cited by 99 · 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).”
BackgroundMethodInfluentialTargeted cellular ablation based on the morphology of malignant cells
Ivey, J. W., Latouche, E. L., Sano, M. B., Rossmeisl, J. H., Davalos, R. V., & Verbridge, S. S. (2015) · Scientific Reports · doi:10.1038/srep17157 · Cited by 97 · see citing works
An Overview of Sub-Cellular Mechanisms Involved in the Action of TTFields
Tuszynski, J., Wenger, C., Friesen, D., & Preto, J. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph13111128 · Cited by 95 · see citing works
Effect of electromagnetic waves on human reproduction
Wdowiak, A., Mazurek, P. A., Wdowiak, A., & Bojar, I. (2017) · Annals of Agricultural and Environmental Medicine · doi:10.5604/12321966.1228394 · Cited by 95 · see citing works
A scaling law for membrane permeabilization with nanopulses
Schoenbach, K. H., Joshi, R. P., Beebe, S. J., & Baum, C. E. (2009) · IEEE Transactions on Dielectrics and Electrical Insulation · doi:10.1109/tdei.2009.5293932 · Cited by 95 · see citing works
“Modeling results using molecular dynamics [26-28] and continuum models [29-32] have provided insight into the mechanism of permeabilization of membranes with a single pulse.”
BackgroundRegulation of intracellular calcium concentration by nanosecond pulsed electric fields
Scarlett, S. S., White, J. A., Blackmore, P. F., Schoenbach, K. H., & Kolb, J. F. (2009) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2009.02.006 · Cited by 94 · see citing works
“Since the pulse duration is much shorter than the charging time of the cell, the interior of the cell is not yet shielded from the external field and organelle membranes are charged in a manner similar to the outer membrane [41,42].”
BackgroundSmith, K. C., & Weaver, J. C. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.121921 · Cited by 94 · see citing works
Subnanosecond Electric Pulses Cause Membrane Permeabilization and Cell Death
Xiao, S. H., Guo, S., Nesin, V., Heller, R. F., & Schoenbach, K. H. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2011.2112360 · Cited by 91 · see citing works
“For subnanosecond pulses, the probability of penetrating into the interior of the cell is even higher than for nanosecond pulses [19].”
BackgroundAdvantages and Disadvantages of Different Concepts of Electroporation Pulse Generation
Reberšek, M., & Damijan Miklavčič, A. (2011) · Automatika · doi:10.1080/00051144.2011.11828399 · Cited by 91 · see citing works
“Elektroporator je generator impulsa koji se koristi za permeabilizaciju stanica.”
BackgroundElectrochemical Control of Cell and Tissue Polarity
Chang, F., & Minc, N. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013357 · Cited by 87 · see citing works
Perspective on Pulsed Electric Field Treatment in the Bio-based Industry
Buchmann, L., & Mathys, A. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00265 · Cited by 82 · see citing works
Ibey, B. L., Roth, C. C., Pakhomov, A. G., Bernhard, J. A., Wilmink, G. J., & Pakhomova, O. N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015642 · Cited by 80 · see citing works
“apt to form pores than a larger cell due to a smaller induced transmembrane potential [2,3,45,46,47,48].”
BackgroundZhao, H.-P., Steiger, A., Nohner, M., & Ye, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129625 · Cited by 75 · see citing works
“Although little is known about the effects of the DC electric field on internal organelles such as mitochondria, theoretical works have shown that the cytoplasmic membrane could provide “shielding effects” against the DC electric field, and prevent the electric field from penetrating into the cell [49].”
BackgroundPerrier, D. L., Rems, L., & Boukany, P. E. (2017) · Advances in Colloid and Interface Science · doi:10.1016/j.cis.2017.04.016 · Cited by 76 · see citing works
Nanosecond Pulsed Electric Field (nsPEF): Opening the Biotechnological Pandora’s Box
Ruiz-Fernández, A. R., Campos, L., Gutiérrez-Maldonado, S. E., Núñez, G., Villanelo, F., & Pérez‐Acle, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116158 · Cited by 74 · see citing works
Nesin, V., Bowman, A. M., Xiao, S. H., & Pakhomov, A. G. (2011) · Bioelectromagnetics · doi:10.1002/bem.21696 · Cited by 72 · see citing works
“Indeed, the conditions for selective intracellular electroporation appear somewhat exotic and it is not clear if they exist in living cells [Kotnik and Miklavcic, 2006].”
Sano, M. B., Fan, R. E., & Xing, L. (2017) · Scientific Reports · doi:10.1038/srep40747 · Cited by 69 · see citing works
Vižintin, A., Marković, S., Ščančar, J., & Damijan Miklavčič, A. (2021) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2021.107798 · 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
Nanosecond electric pulses: A mini-review of the present state of the art
Chopinet, L., & Rols, M. (2014) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2014.07.008 · Cited by 67 · see citing works
Electropermeabilization of endocytotic vesicles in B16 F1 mouse melanoma cells
Napotnik, T. B., Reberšek, M., Kotnik, T., Lebrasseur, É., Cabodevila, G., & Damijan Miklavčič, A. (2010) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-010-0599-9 · Cited by 67 · see citing works
“Although the nsEP have strong effects on cell interior, theoretical models and simulations [21, 32, 55] point out that generally, the plasma membrane is also affected.”
BackgroundNovel 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
Reberšek, M., Kranjc, M., Pavliha, D., Napotnik, T. B., Vrtačnik, D., Amon, S., & Damijan Miklavčič, A. (2009) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2009.2027422 · Cited by 64 · see citing works
Effect of nanosecond pulsed electric field treatment on cell proliferation of microalgae
Buchmann, L., Frey, W., Gusbeth, C., Ravaynia, P. S., & Mathys, A. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.09.124 · Cited by 60 · see citing works
“Based on mathematical models an increased electropermeabilization effect on intracellular structures compared to the cell membrane was observed for angular frequencies ω (rad s−1) above 107 (Kotnik and Miklavčič, 2006; Vernier et al., 2006).”
Xu, S., Du, C., Zhang, M., Wang, R., Feng, W., Wang, C., Liu, Q., & Zhao, W. (2023) · Nano Research · doi:10.1007/s12274-023-5527-z · Cited by 59 · see citing works
Teissié, J., Escoffre, J., Rols, M., & Golzio, M. (2008) · Radiology and Oncology · doi:10.2478/v10019-008-0016-2 · Cited by 59 · see citing works
Pulse Electric Field Technology for Wastewater and Biomass Residues’ Improved Valorization
Capodaglio, A. G. (2021) · Processes · doi:10.3390/pr9050736 · Cited by 58 · see citing works
“In conventional PEF processing the electric field is applied in intervals in the range of micro- to milliseconds; in nanosecond PEF (nsPEF) processing, much higher electric fields (10–100 kV/cm) are applied for intervals of 1–300 ns, inducing distinct intracellular effects from those of conventional PEF [8].”
BackgroundVariability of the Minimal Transmembrane Voltage Resulting in Detectable Membrane Electroporation
Towhidi, L., Kotnik, T., Pucihar, G., Firoozabadi, M., Mozdarani, H., & Damijan Miklavčič, A. (2008) · Electromagnetic Biology and Medicine · doi:10.1080/15368370802394644 · Cited by 58 · see citing works
“The conductivities of the cytoplasm and the (non porated) membrane were set at 3 10 1 S/m and 5 10 7 Sm 1, respectively, and the membrane thickness at 5 nm (Kotnik et al., 1997; Kotnik and Miklavčič, 2006).”
BackgroundMechanisms and immunogenicity of nsPEF-induced cell death in B16F10 melanoma tumors
Rossi, A., Pakhomova, O. N., Pakhomov, A. G., Weygandt, S., Bulysheva, A. A., Murray, L., Mollica, P. A., & Muratori, C. (2019) · Scientific Reports · doi:10.1038/s41598-018-36527-5 · Cited by 56 · see citing works
Merla, 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
Advantages and Disadvantages of Different Concepts of Electroporation Pulse Generation
Reberšek, M., & Damijan Miklavčič, A. (2011) · doi:10.7305/automatika.52-1.79 · Cited by 55 · see citing works
Miklovic, T., Latouche, E. L., DeWitt, M. R., Davalos, R. V., & Sano, M. B. (2017) · Annals of Biomedical Engineering · doi:10.1007/s10439-017-1889-2 · Cited by 54 · see citing works
Assessment of Cytoplasm Conductivity by Nanosecond Pulsed Electric Fields
Denzi, A., Merla, C., Palego, C., Paffi, A., Ning, Y., Multari, C. R., Cheng, X., Apollonio, F., Hwang, J. C. M., & Liberti, M. (2015) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2015.2399250 · Cited by 53 · see citing works
“result, three-layer microdosimetry models often resorted to the conductivity of simple phosphate buffer saline solution (PBS) [15], [19], [30], or water with a certain fraction of dissolved”
BackgroundEffects of Oscillatory Electric Fields on Internal Membranes: An Analytical Model
Vajrala, V., Claycomb, J. R., Sanabria, H., & Miller, J. H. (2007) · Biophysical Journal · doi:10.1529/biophysj.107.114611 · Cited by 51 · see citing works
“More recently, Kotnik and Miklavčič calculated the ac transmembrane voltage induced on spheroidal cells (26) and across internal membranes, using a double-shell model for application to cells exposed to nanosecond-duration pulsed electric fields (27).”
MethodHuang, K., Yu, L., Wang, W., Gai, L., & Wang, J. (2013) · Food Control · doi:10.1016/j.foodcont.2013.07.011 · Cited by 48 · see citing works
Controlling properties of human neural progenitor cells using 2D and 3D conductive polymer scaffolds
Song, S., Amores, D., Chen, C., McConnell, K. W., Oh, B., Poon, A. S. Y., & George, P. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-56021-w · Cited by 48 · see citing works
Ye, H., Cotic, M., Kang, E. E., Fehlings, M. G., & Carlen, P. L. (2010) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/1743-0003-7-12 · Cited by 47 · see citing works
“Another study [41] has modeled the internal membrane response to the time-varying electric field, and has investigated the condition under which ψorg can temporarily exceed ψcell under nanosecond duration pulsed electric fields.”
InfluentialSong, J., Joshi, R. P., & Schoenbach, K. H. (2011) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-011-0745-z · Cited by 46 · see citing works
Histopathology of normal skin and melanomas after nanosecond pulsed electric field treatment
Chen, X., Swanson, R. J., Kolb, J. F., Nuccitelli, R., & Schoenbach, K. H. (2009) · Melanoma Research · doi:10.1097/cmr.0b013e32832f1558 · Cited by 46 · see citing works
From the basic science of biological effects of ultrashort electrical pulses to medical therapies
Schoenbach, K. H. (2018) · Bioelectromagnetics · doi:10.1002/bem.22117 · Cited by 44 · see citing works
“This simple, analytical model, which served as the basis for the understanding of intracellular effects caused by ultrashort pulses, has been refined and expanded [Foster, 2000; Kotnik and Miklavcic, 2006].”
MethodMicrodosimetric Study for Nanosecond Pulsed Electric Fields on a Cell Circuit Model with Nucleus
Denzi, A., Merla, C., Camilleri, P., Paffi, A., d'Inzeo, G., Apollonio, F., & Liberti, M. (2013) · The Journal of Membrane Biology · doi:10.1007/s00232-013-9546-7 · Cited by 44 · see citing works
“The analytical models rely on the solution of the quasi-static Laplace equation on a spherical cell (Kotnik and Miklavcic 2006; Kotnik et al. 2010; Merla et al. 2011); the numerical ones are based on a distributed circuit representation (Joshi et al.”
BackgroundMethodInfluentialYe, H., Hendee, J., Ruan, J., Zhirova, A., Ye, J., & Dima, M. (2022) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-022-01094-4 · Cited by 46 · see citing works
“Computational work revealed that larger cell bodies are associated with greater transmembrane potentials under electrical [56] and magnetic [13] stimulation.”
BackgroundŽgalin, M. K., Hodžić, D., Reberšek, M., & Kandušer, M. (2012) · The Journal of Membrane Biology · doi:10.1007/s00232-012-9481-z · Cited by 43 · see citing works
Nanosecond Electric Pulse Effects on Gene Expression
Chopinet, L., Napotnik, T. B., Montigny, A., Reberšek, M., Teissié, J., Rols, M., & Damijan Miklavčič, A. (2013) · The Journal of Membrane Biology · doi:10.1007/s00232-013-9579-y · Cited by 43 · see citing works
“Numerical simulations (Joshi et al. 2004; Kotnik and Miklavcic 2006; Retelj et al. 2013) predict that the electric parameters of cells Fig.”
BackgroundWindow effect of pulsed electric field on biological cells
Yao, C., Hu, X., Mi, Y., Li, C., & Sun, C. (2009) · IEEE Transactions on Dielectrics and Electrical Insulation · doi:10.1109/tdei.2009.5293936 · Cited by 40 · see citing works
“Kontik and Damijan [17-19] extended the Schwan theory, introducing a general analytical method.”
BackgroundKranjc, M., Kranjc, S., Bajd, F., Serša, G., Serša, I., & Miklavčič, D. (2017) · Scientific Reports · doi:10.1038/s41598-017-10846-5 · Cited by 42 · see citing works
Cell membrane thermal gradients induced by electromagnetic fields
Garner, A. L., Deminsky, M., Neculaes, V. B., Chashihin, V., Knizhnik, A. A., & Potapkin, B. V. (2013) · Journal of Applied Physics · doi:10.1063/1.4809642 · Cited by 39 · see citing works
Membrane dielectric dispersion in nanosecond pulsed electroporation of biological cells
Salimi, E., Thomson, D. J., & Bridges, G. E. (2013) · IEEE Transactions on Dielectrics and Electrical Insulation · doi:10.1109/tdei.2013.6571442 · Cited by 39 · see citing works
“There is evidence that by applying megavolt-per-meter, nanosecond duration electric pulses, such that the pulse duration is less than the charging time of the cell membrane, the electric field can penetrate inside the cell and electroporate internal membranes [9-11].”
BackgroundHaberkorn, I., Buchmann, L., Hiestand, M., & Mathys, A. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.122029 · Cited by 40 · see citing works
Mercadal, B., Vernier, P. T., & Ivorra, A. (2016) · The Journal of Membrane Biology · doi:10.1007/s00232-016-9907-0 · Cited by 38 · see citing works
“, 1988) εe 70 Relative permittivity of the extracellular medium (Kotnik and Miklavčič, 2006) εi 70 Relative permittivity of the intracellular medium (Kotnik and Miklavčič, 2006) εm 5 Relative permittivity of the membrane (Kotnik and Miklavčič, 2006) w 10 × R Dimensions of the simulated space (10 times cell radius) σp…”
BackgroundTemperature Dependence of High Frequency Irreversible Electroporation Evaluated in a 3D Tumor Model
Fesmire, C. C., Petrella, R. A., FOGLE, C. A., Gerber, D. A., Xing, L., & Sano, M. B. (2020) · Annals of Biomedical Engineering · doi:10.1007/s10439-019-02423-w · Cited by 38 · see citing works
Evaluation of the Electroporation Efficiency of a Grid Electrode for Electrochemotherapy
Ongaro, A., Campana, L. G., Mattei, M. D., Dughiero, F., Forzan, M., Pellati, A., Rossi, C. R., & Sieni, E. (2015) · Technology in Cancer Research & Treatment · doi:10.1177/1533034615582350 · Cited by 37 · see citing works
“A simple model of needles inserted in homogeneous tissue was proposed previously.(2,18,27-29,31-35) Figure 2 shows the model geometry, a parallelepiped (eg, sizes 5 3.”
MethodField distribution and DNA transport in solid tumors during electric field-mediated gene delivery.
Henshaw, J., & Yuan, F. (2008) · Journal of Pharmacy and Science · doi:10.1002/jps.21000 · Cited by 40 · see citing works
Assessing how electroporation affects the effective conductivity tensor of biological tissues
Mezeme, M. E., Kranjc, M., Bajd, F., Serša, I., Brosseau, C., & Damijan Miklavčič, A. (2012) · Applied Physics Letters · doi:10.1063/1.4767450 · Cited by 37 · see citing works
Transmembrane potential induced in a spherical cell model under low-frequency magnetic stimulation
Ye, H., Cotic, M., & Carlen, P. L. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/3/014 · Cited by 36 · see citing works
Ye, H., Cotic, M., Fehlings, M. G., & Carlen, P. L. (2010) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-010-0704-0 · Cited by 36 · see citing works
“The choice of values and their ranges for the electric parameters was based on reports in the literature [23, 24].”
MethodSteuer, A., Schmidt, A., Labohá, P., Babica, P., & Kolb, J. F. (2016) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2016.07.003 · Cited by 36 · see citing works
Huang, K., Jiang, T., Wang, W., Gai, L., & Wang, J. (2014) · Food and Bioprocess Technology · doi:10.1007/s11947-014-1272-3 · Cited by 35 · see citing works
The Phenomenon of Electroporation
Mahnič-Kalamiza, S., & Damijan Miklavčič, A. (2022) · Food engineering series · doi:10.1007/978-3-030-70586-2_3 · Cited by 33 · see citing works
“This is followed, within a microsecond, by the transmembrane field being amplified by polarization (positive and negative charge carriers accumulating either side of the membrane), resulting in the buildup of an induced transmembrane voltage (Kotnik and Miklavčič 2006).”
BackgroundGarcía-Sánchez, T., Merla, C., Fontaine, J., Muscat, A., & Mir, L. M. (2018) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2018.01.018 · Cited by 32 · see citing works
“Considering our results as a reflect of electropermeabilization of the internal membranes, the observed low pass filter frequency response is not in agreement with the theoretical predictions where a band pass filter behavior is usually assigned for the intracellular membranes [23,24].”
BackgroundMethodResultInfluentialNatural Fluctuations of an Electropore Show Fractional Lévy Stable Motion
Kotulska, M. (2006) · Biophysical Journal · doi:10.1529/biophysj.106.091363 · Cited by 32 · see citing works
Merla, C., Pakhomov, A. G., Semenov, I., & Vernier, P. T. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.04.014 · Cited by 31 · see citing works
Buchmann, L., Böcker, L., Frey, W., Haberkorn, I., Nyffeler, M., & Mathys, A. (2018) · Innovative Food Science & Emerging Technologies · doi:10.1016/j.ifset.2018.04.013 · Cited by 31 · see citing works
Electrolytic ablation enables cancer cell targeting through pH modulation
Perkons, N. R., Stein, E. J., Nwaezeapu, C., Wildenberg, J. C., Saleh, K. S., Itkin-Ofer, R., Ackerman, D., Soulen, M. C., Hunt, S. J., Nadolski, G., et al. (2018) · Communications Biology · doi:10.1038/s42003-018-0047-1 · Cited by 31 · see citing works
- Authors
- Kotnik, T., & Miklavčič, D.
- Affiliations
- University of Ljubljana (SI)
- Corresponding author
- Kotnik, Tadej
- ORCID
- Kotnik, Tadej
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2006-01
- Volume
- 90
- Issue
- 2
- Pages
- 480-491
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1367054
- OpenAlex
- W2106955112
- Cited by
- 318
- References
- 68
- Citations by year
- 2026: 13 · 2025: 11 · 2024: 15 · 2023: 22 · 2022: 12 · 2021: 12 · 2020: 17 · 2019: 20 · 2018: 19 · 2017: 26 · 2016: 19 · 2015: 12 · 2014: 19 · 2013: 17 · 2012: 17
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electromagnetic Fields and Biological Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Electrical and Electromagnetic Research
- Keywords
- electric field effects on cells, organelle membranes, nanosecond pulses, frequency domain analysis, time-domain analysis, membrane conductivity
- MeSH terms
- Animals, Biological Transport, Active, Biophysics, Cell Membrane, Cell Membrane Permeability, Cytosol, Electric Conductivity, Electromagnetic Fields, Intracellular Membranes, Membrane Fluidity, Membrane Lipids, Membrane Potentials, Models, Theoretical, Time Factors
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