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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.”
From An Overview of Sub-Cellular Mechanisms Involved in the Action of TTFields (2016) · cites this paper as [31]
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“The two values that were tested (0.1 and 0.5 S/m) were chosen because they fall in the range of conductivities for intracellular organelles reported in the literature (Kotnik and Miklavčič 2006).”
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BackgroundReview of Developments in Bioelectrics as an Application of Pulsed Power Technology
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“In [19], in fact, through a frequency-domain analysis, the authors highlight the dependence on the voltage induced on both plasma and nuclear membranes due to variations of the electromagnetic properties characterizing the membranes assumed as linear media: their nonlinear behavior with respect to EP is not accounted…”
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Nonlinear dispersive cell model for microdosimetry of nanosecond pulsed electric fields
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“8 h 5 nm Membrane thickness[39] εe 70 Relative permittivity of the extracellular medium [40] εi 70 Relative permittivity of the intracellular medium [40] εm 5 Relative permittivity of the membrane [40]”
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Alshahat, M. A., Elgenedy, M. A., Aboushady, A. A., & Williams, M. T. S. (2023) · Applied Sciences · doi:10.3390/app131810029 · Cited by 15
Shock waves associated with electric pulses affect cell electro-permeabilization
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“Previous studies have reported that the high-frequency components of PEF could interact with intermembrane organelles, such as mitochondria and nucleus, when PEF passes through cytomembrane [35, 36].”
BackgroundApplication of electric field treatment (EFT) for microbial control in water and liquid food
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Finite Element Evaluation of the Electric Field Distribution in a Non-Homogeneous Environment
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BackgroundMembrane Heating in Living Tissues Exposed to Nonthermal Pulsed EM Fields
Pierro, V. C., Vita, A. D., Croce, R. P., & Pinto, I. M. (2014) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2014.2342492 · Cited by 11
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MethodNon-thermal Processing By Radio Frequency Electric Fields
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Beyond Electroporation Pulse Parameters: From Application to Evaluation
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Transmembrane Voltage Induced by Applied Electric Fields
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Nonthermal Processing By Radio Frequency Electric Fields
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Extending membrane pore lifetime with AC fields: A modeling study
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Probing Lipid Bilayers under Ionic Imbalance
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“Temporally, the TMP gradually increases to its steady-state value over the course of tens of microseconds when an external electric field is turned on (5,22).”
BackgroundSelective Electroporation of Organelles Under an Intense Picosecond Pulsed Electric Field
Mao, Z., Liu, L., Zhang, Y., Zhang, J.-H., Liu, N., & Liu, Q. H. (2018) · IEEE journal on multiscale and multiphysics computational techniques · doi:10.1109/jmmct.2018.2887000 · Cited by 9
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MethodResultDistinct Kinetics in Electrophoretic Extraction of Cytoplasmic RNA from Single Cells
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INFLUENCE OF CELLULAR PROPERTIES ON THE ELECTRIC FIELD DISTRIBUTION AROUND A SINGLE CELL
Ye, H., Cotic, M., Fehlings, M. G., & Carlen, P. L. (2012) · Progress In Electromagnetics Research B · doi:10.2528/pierb11122705 · Cited by 8
“Finally, the electric field that penetrates into the cytoplasmic space (intracellular field) is likely important in polarizing internal organelles such as mitochondria [14] and in facilitating polynucleotide uptake and migration within the cell [27].”
Dawson, J. E., Lee, P. S., van Rienen, U., & Appali, R. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.557447 · Cited by 8
Mechanisms of Electrically Mediated Cytosolic Ca2+ Transients in Aequorin-Transformed Tobacco Cells
Sukhorukov, V. L., Endter, J. M., Zimmermann, D., Shirakashi, R., Fehrmann, S., Kiesel, M., REUSS, R., Becker, D., Hedrich, R., Bamberg, E., et al. (2007) · Biophysical Journal · doi:10.1529/biophysj.107.110783 · Cited by 8
“The electrostatic interaction of the induced dipole m with the applied field results in a variety of electrokinetic phenomena (13,25,43,50,51).”
BackgroundMethodModel Analysis of Electric Fields Induced by High-Voltage Pulsing in Cylindrical Nerves
Joshi, R. P., & Song, J. (2010) · IEEE Transactions on Plasma Science · doi:10.1109/tps.2010.2063717 · Cited by 8
“Furthermore, appreciable electric fields within the organelle interior can be created if their electrical conductivities are higher than that of the cytosol or if the organelle membrane had lower dielectric permittivities than the cellular membrane [ 36 ].”
BackgroundPerez, B., Weber, N., Haberkorn, I., & Mathys, A. (2025) · Algal Research · doi:10.1016/j.algal.2025.104125 · Cited by 7
Sabri, E., & Brosseau, C. (2023) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2023.108583 · Cited by 7
Single Cell Microdosimetric Studies Comparing Ideal and Measured Nanosecond Pulsed Electric Fields
Denzi, A., Merla, C., Palego, C., Apollonio, F., Hwang, J. C. M., & Liberti, M. (2013) · IEEE MTT-S International Microwave Symposium digest · doi:10.1109/mwsym.2013.6697655 · Cited by 7
“In [6], it is shown that the best pulse shape for attaining efficient poration is the trapezoidal one.”
BackgroundYe, H., & Ng, J. (2018) · PeerJ · doi:10.7717/peerj.6020 · Cited by 7
Analysis of Electrical Analogue of a Biological Cell and Its Response to External Electric Field
Ravikumar, K., Basu, B., & Dubey, A. K. (2018) · Regenerative Engineering and Translational Medicine · doi:10.1007/s40883-018-0073-z · Cited by 7
Modulating Ca2+ influx into adrenal chromaffin cells with short-duration nanosecond electric pulses
Yun, S. H., Mansurov, V., Yang, L., Yoon, J., Leblanc, N., Craviso, G. L., & Zaklit, J. (2024) · Biophysical Journal · doi:10.1016/j.bpj.2024.06.021 · Cited by 6
Pulse Power Ablation of Melanoma with Nanosecond Pulsed Electric Fields
Stephen, J., Wentia, E., Ren, W., & Che, X. (2011) · InTech eBooks · doi:10.5772/22850 · Cited by 6
Electric pulse shape impact on biological effects: A modeling study
Garner, A. L., Maciejewski, J. J., Vadlamani, A., & Byer, R. J. (2015) · IEEE Conference on Electrical Insulation and Dielectric Phenomena (CEIDP) · doi:10.1109/ceidp.2015.7352148 · Cited by 6
“Multiple modeling studies have investigated the impact of EPs on various components of the cell [9-13].”
BackgroundTheoretical analysis of transmembrane potential of cells exposed to nanosecond pulsed electric field
Lu, W., Wu, K., Hu, X., Xie, X.-D., Ning, J., Wang, C., Zhou, H., & Yang, G. (2016) · International Journal of Radiation Biology · doi:10.1080/09553002.2017.1230244 · Cited by 6
“DUo is not able to exceed DUc in some given electric and geometrical parameters (Kotnik and Miklavcic 2006).”
BackgroundMethodTissue Ablation Using Nanosecond Electric Pulses
Nuccitelli, R. (2016) · Springer eBooks · doi:10.1007/978-3-319-26779-1_93-1 · Cited by 6
Angelis, A. D., Denzi, A., Merla, C., André, F. M., García-Sánchez, T., Mir, L. M., Apollonio, F., & Liberti, M. (2019) · European Microwave Conference (EuMC) · doi:10.23919/eumc.2019.8910909 · Cited by 6
“Many works exist on radiofrequency electric field effects, both theoretical [17-19] and experimental [20-24].”
BackgroundEffect of nanosecond pulsed electric fields (nsPEFs) on coronavirus survival
Cantu, J. C., Barnes, R. A., Gamboa, B. M., Keister, A. S., Echchgadda, I., & Ibey, B. L. (2023) · AMB Express · doi:10.1186/s13568-023-01601-3 · Cited by 6
“For the membrane charging dynamics a single shell capacitive model and general parameters (membrane permittivity and conductivity, inside permittivity and conductivity) were taken from Kotnik and Miklavčič (2006).”
MethodElectrotherapy on Cancer: Experiment and Mathematical Modeling
Pupo, A. E. B., Jiménez, R. P., & Cabrales, L. E. B. (2011) · InTech eBooks · doi:10.5772/25765 · Cited by 6
“On the other hand, the mathematical modeling has been used to understand alterations on cellular membrane [Kotnik & Miklavčič, 2006], the role of pH in electrotherapy [Turjanski et al., 2009], the possible physicochemical reactions induced into the tumor during direct current application [Nilsson &…”
Electric Pulse Pretreatment for Enhanced Lipid Recovery from Chlorella protothecoides
Geissler, C. H., Mulligan, M. L., Zmola, Z. E., Ray, S., Morgan, J. A., & Garner, A. L. (2019) · BioEnergy Research · doi:10.1007/s12155-019-10064-z · Cited by 6
Electrochemical Treatment of Tumours: Brief Considerations
Sequeira, C. A. C. (2022) · American Journal of Biomedical Science & Research · doi:10.34297/ajbsr.2022.17.002317 · Cited by 5
A Simplified Electrical-Based Model for Electroporation Dynamics
Loveless, A. M., Wyss, S. J., Milestone, W., Joshi, R. P., & Garner, A. L. (2024) · IEEE Access · doi:10.1109/access.2024.3351715 · Cited by 5
Linghu, L., Tan, Y., Lou, Y., Hu, L., Yang, H., & Yu, T. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.11.089 · Cited by 5
Gomonov, S. V., & Efanov, V. M. (2008) · IEEE International Power Modulator Symposium and High-Voltage Workshop (IPMHVC) · doi:10.1109/ipmc.2008.4743650 · Cited by 5
“Therefore we considered the alternating (oscillating) external field with amplitude E. In order to obtain the transmembrane potential induced on the organelle membrane we used the spherical cell model given in [ 5 ].”
BackgroundMethodHu, Q., & Joshi, R. P. (2010) · IEEE Transactions on Dielectrics and Electrical Insulation · doi:10.1109/tdei.2010.5658243 · Cited by 5
“In fact, theoretical reports in the literature have clearly shown such a possibility [44] in cases when the organelle interior was electrically more conductive than the cytosol, or if the organelle membrane had a lower dielectric permittivity than the cell membrane, As before our results with inner membrane poration s…”
Result
Metadata
- 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 › Engineering › Electrical and Electronic Engineering › 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
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.
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