Actin networks regulate the cell membrane permeability during electroporation

• Published in: Biochimica et biophysica acta. Biomembranes Vol. 1863; no. 1; p. 183468
• Main Authors: Muralidharan, Aswin, Rems, Lea, Kreutzer, Michiel T., Boukany, Pouyan E.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.01.2021
• Subjects: Actin Cytoskeleton - chemistry; Actin Cytoskeleton - metabolism; Actin networks; Animals; Cell Membrane - chemistry; Cell Membrane - metabolism; Cell Membrane Permeability; CHO Cells; Cricetulus; Electropermeabilization; Electroporation; Energy barrier; Kinetics; Propidium - chemistry; Temperature dependent kinetics of electroporation; Actin networks; Electroporation; Temperature dependent kinetics of electroporation; Energy barrier; Electropermeabilization
• ISSN: 0005-2736; 1879-2642; 1879-2642
• DOI: 10.1016/j.bbamem.2020.183468

Transient physical disruption of cell membranes by electric pulses (or electroporation) has significance in biomedical and biological applications requiring the delivery of exogenous (bio)molecules to living cells. We demonstrate that actin networks regulate the cell membrane permeability during electroporation. Disruption of actin networks increases the uptake of membrane-impermeable molecules such as propidium iodide during electroporation. Our experiments at different temperatures ranging from 11 °C to 37 °C show that molecular uptake during electroporation increases with temperature. Furthermore, by examining the temperature-dependent kinetics of propidium iodide uptake, we infer that the activation energy barrier of electroporation is lowered when the actin networks are disrupted. Our numerical calculations of transmembrane voltage show that the reduced activation energy barrier for the cells with disrupted actin is not a consequence of the changes in transmembrane voltage associated with changes in the cell shape due to the disruption of actin, indicating that this could be due to changes in membrane mechanical properties. Our results suggest that the current theoretical models of electroporation should be advanced further by including the contributions of the cytoskeletal networks on the cell membrane permeability during the delivery of exogenous materials. [Display omitted] •Electroporative uptake of propidium iodide increases when actin networks are chemically disrupted.•Electroporative uptake of propidium iodide is a temperature dependent process.•Activation energy barrier of electroporation is reduced when the actin networks are disrupted.•The observed reduction in activation energy barrier is possibly due to altered cell membrane mechanical properties.