Membrane Electroporation and Electropermeabilization: Mechanisms and Models

Kotnik, Tadej; Rems, Lea; Tarek, Mounir; Miklavčič, Damijan

doi:10.1146/annurev-biophys-052118-115451

Cited by 813Microbial Inactivation MethodsLipid Membrane Structure and BehaviorPlasma Applications and Diagnostics

Membrane Electroporation and Electropermeabilization: Mechanisms and Models

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Kotnik, Tadej, Rems, Lea, Tarek, Mounir, Miklavčič, Damijan·2019·Annual Review of Biophysics

DOI 10.1146/annurev-biophys-052118-115451

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Abstract

Exposure of biological cells to high-voltage, short-duration electric pulses causes a transient increase in their plasma membrane permeability, allowing transmembrane transport of otherwise impermeant molecules. In recent years, large steps were made in the understanding of underlying events. Formation of aqueous pores in the lipid bilayer is now a widely recognized mechanism, but evidence is growing that changes to individual membrane lipids and proteins also contribute, substantiating the need for terminological distinction between electroporation and electropermeabilization. We first revisit experimental evidence for electrically induced membrane permeability, its correlation with transmembrane voltage, and continuum models of electropermeabilization that disregard the molecular-level structure and events. We then present insights from molecular-level modeling, particularly atomistic simulations that enhance understanding of pore formation, and evidence of chemical modifications of membrane lipids and functional modulation of membrane proteins affecting membrane permeability. Finally, we discuss the remaining challenges to our full understanding of electroporation and electropermeabilization.

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Electropores may form under external electric fields and can also arise spontaneously in naturally occurring systems due to transient transmembrane potentials arising from bilayer-surface charge fluctuations.
“Electropores may form under external electric fields 9 and can also arise spontaneously in naturallyoccuring (particularly biological) systems due to transient transmembrane potentials arising from bilayer-surface charge flucuations 8,12,[22][23][24][25][26][27][28][29][30] .”
From Fusion of lipid membranes: an alternative pathway (2026) · cites this paper as [25]
Section 3.2 states that an electric field can initiate pores in lipid bilayers. Neither that section nor the passages on spontaneous pore formation in Section 6 support the proposed mechanism of bilayer-surface charge fluctuations producing transient transmembrane potentials in naturally occurring systems; Section 6 instead discusses possible pores in oxidized membrane lesions. Page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured
After the first threshold is surpassed, the Vm depolarizes the membrane sufficiently to trigger the formation of aqueous pores and stimulate other voltage-dependent processes such as ion channel activation and cytoskeletal disruption.
“After the first threshold is surpassed, it is thought that the Vm depolarizes the membrane sufficiently to trigger the formation of aqueous pores and stimulate other voltage-dependent processes such as ion channel activation and cytoskeletal disruption [62,65].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [62]
Recent studies suggest that chemical and structural changes in the lipids and proteins (such as ion channels) of the membrane itself also contribute to the mechanism of action of electroporation.
“While it has been recognized for some time now that aqueous pore formation allows for increased permeability across the plasma membrane, recent studies suggest that chemical and structural changes in the lipids and proteins (such as ion channels) of the membrane itself also contribute to the mechanism of action [62].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [62]
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 [62]
There are two thresholds for electroporation that are not universal but particular to the parameters being used (cell type/size, membrane curvature, exposure time, temperature, transported molecule, and osmotic pressure): the induced transmembrane potential needed to cause a detectable increase in membrane permeability, and the critical Vm at which reversible electroporation becomes irreversible.
“An important component of this proposed mechanism, by which altering the plasma membrane through electric pulses leads to increased permeability, is that there are two “thresholds” which are not universal but rather particular to the parameters being used (i.e., cell type/size, membrane curvature, exposure time, temperature, transported molecule, and osmotic pressure) [62]. The first threshold is”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [62]

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Authors: Kotnik, T., Rems, L., Tarek, M., & Miklavčič, D.
Affiliations: University of Ljubljana (SI)
Science for Life Laboratory (SE)
Centre National de la Recherche Scientifique (FR)
Faculty of Electrical Engineering, University of Ljubljana, SI-1000 Ljubljana, Slovenia;,
ORCID: Kotnik, Tadej
Rems, Lea
Tarek, Mounir
Venue: Annual Review of Biophysics
Publisher: Annual Reviews
Published: 2019-05-06
Volume: 48
Issue: 1
Pages: 63-91
ISSN: 1936-122X (ISSN-L)
1936-1238
DOI: 10.1146/annurev-biophys-052118-115451
OpenAlex: W2917550741
Cited by: 813
References: 216
Citations by year: 2026: 129 · 2025: 138 · 2024: 141 · 2023: 122 · 2022: 97 · 2021: 102 · 2020: 66 · 2019: 18
FWCI: 6.75
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Annual Review of Biophysics (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: Javna Agencija za Raziskovalno Dejavnost RS
Centre National de la Recherche Scientifique
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Plasma Applications and Diagnostics
Keywords: electroporation, plasma membrane permeability, lipid bilayers, transmembrane voltage, continuum model, atomistic simulation, electric pulses
MeSH terms: Cell Membrane, Cell Membrane Permeability, Humans, Lipid Bilayers, Membrane Lipids, Electroporation

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Membrane Electroporation and Electropermeabilization: Mechanisms and Models

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