Assessing membrane material properties from the response of giant unilamellar vesicles to electric fields

References

• Lee AG. Biological membranes: the importance of molecular detail. Trends Biochem Sci. 2011;36:493–27.
   PubMed Web of Science ®Google Scholar
• Basquin C, Trichet M, Vihinen H, et al. Membrane protrusion powers clathrin-independent endocytosis of interleukin-2 receptor. EMBO J. 2015;34:2147–2161.
   PubMed Web of Science ®Google Scholar
• Lee E, Knecht DA. Visualization of actin dynamics during macropinocytosis and exocytosis. Traffic. 2002;3:186–192.
   PubMed Web of Science ®Google Scholar
• Schmidtke DW, Diamond SL. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J Cell Biol. 2000;149:719–730.
   PubMed Web of Science ®Google Scholar
• Caballero D, Pinto IM, Rubinstein BY, et al. Protrusion membrane pearling emerges during 3D cell division. Phys Biol. 2019;16:066009.
   PubMed Web of Science ®Google Scholar
• Davis DM, Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol. 2008;9:431–436.
   PubMed Web of Science ®Google Scholar
• Chauveau A, Aucher A, Eissmann P, et al. Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc Natl Acad Sci U S A. 2010;107:5545–5550.
   PubMed Web of Science ®Google Scholar
• Kandušer M, Ušaj M. Cell electrofusion: past and future perspectives for antibody production and cancer cell vaccines. Expert Opin Drug Deliv. 2014;11:1885–1898.
   PubMed Web of Science ®Google Scholar
• Guo-Parke H, McCluskey JT, Kelly C, et al. Configuration of electrofusion-derived human insulin-secreting cell line as pseudoislets enhances functionality and therapeutic utility. J Endocrinol. 2012;214:257–265.
   PubMed Web of Science ®Google Scholar
• Davalos RV, Mir LM, Rubinsky B. Tissue Ablation with Irreversible Electroporation. Ann Biomed Eng. 2005;33:223.
   PubMed Web of Science ®Google Scholar
• Gothelf A, Mir LM, Gehl J. Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation. Cancer Treat Rev. 2003;29:371–387.
   PubMed Web of Science ®Google Scholar
• Probst U, Fuhrmann I, Beyer L, et al. Electrochemotherapy as a new modality in interventional oncology: a Review. Technol Cancer Res Treat. 2018;17:1–12.
   Web of Science ®Google Scholar
• Chang TT, Zhou VX, Rubinsky B. Using non-thermal irreversible electroporation to create an in vivo niche for exogenous cell engraftment. BioTechniques. 2017;62:229–231.
   PubMed Web of Science ®Google Scholar
• André F, Mir LM. DNA electrotransfer: its principles and an updated review of its therapeutic applications. Gene Ther. 2004;11:S33–S42.
   PubMed Web of Science ®Google Scholar
• Kim TK, Eberwine JH. Mammalian cell transfection: the present and the future. Anal Bioanal Chem. 2010;397:3173–3178.
   PubMed Web of Science ®Google Scholar
• Mahnič-Kalamiza S, Vorobiev E, Miklavčič D. Electroporation in food processing and biorefinery. J Membr Biol. 2014;247:1279–1304.
   PubMed Web of Science ®Google Scholar
• Dimova R. Giant vesicles and their use in assays for assessing membrane phase state, curvature, mechanics, and electrical properties. Annu Rev Biophys. 2019;48:93–119.
   PubMed Web of Science ®Google Scholar
• Dimova R, Marques C. The Giant Vesicle Book. Boca Raton: Taylor & Francis Group, LLC; 2019.
   Google Scholar
• Dimova R, Aranda S, Bezlyepkina N, et al. A practical guide to giant vesicles. Probing the membrane nanoregime via optical microscopy. J Phys. 2006;18:S1151–S1176.
   Google Scholar
• Walde P, Cosentino K, Engel H, et al. Giant vesicles: preparations and applications. ChemBioChem. 2010;11:848–865.
   PubMed Web of Science ®Google Scholar
• Fenz SF, Sengupta K. Giant vesicles as cell models. Integr Biol. 2012;4:982–995.
   Google Scholar
• Perrier DL, Rems L, Boukany PE. Lipid vesicles in pulsed electric fields: fundamental principles of the membrane response and its biomedical applications. Adv Colloid Interface Sci. 2017;249:248–271.
   PubMed Web of Science ®Google Scholar
• Dimova R, Riske KA, Aranda S, et al. Giant vesicles in electric fields. Soft Matter. 2007;3:817–827.
   PubMed Web of Science ®Google Scholar
• Dimova R, Bezlyepkina N, Jordö MD, et al. Vesicles in electric fields: some novel aspects of membrane behavior. Soft Matter. 2009;5:3201–3212.
   Web of Science ®Google Scholar
• Portet T, Mauroy C, Démery V, et al. Destabilizing giant vesicles with electric fields: an overview of current applications. J Membr Biol. 2012;245:555–564.
   PubMed Web of Science ®Google Scholar
• Rawicz W, Olbrich KC, McIntosh T, et al. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J. 2000;79:328–339.
   PubMed Web of Science ®Google Scholar
• Tian AW, Capraro BR, Esposito C, et al. Bending stiffness depends on curvature of ternary lipid mixture tubular membranes. Biophys J. 2009;97:1636–1646.
   PubMed Web of Science ®Google Scholar
• Sorre B, Callan-Jones A, Manneville J-B, et al. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc Nat Acad Sci. 2009;106:5622–5626.
   PubMed Web of Science ®Google Scholar
• Dimova R, Pouligny B, Dietrich C. Pretransitional effects in dimyristoylphosphatidylcholine vesicle membranes: optical dynamometry study. Biophys J. 2000;79:340–356.
   PubMed Web of Science ®Google Scholar
• Meleard P, Gerbeaud C, Pott T, et al. Bending elasticities of model membranes: influences of temperature and sterol content. Biophys J. 1997;72:2616–2629.
   PubMed Web of Science ®Google Scholar
• Evans E, Needham D. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion and colloidal interactions. J Phys Chem. 1987;91:4219–4228.
   Web of Science ®Google Scholar
• Needham D, Evans E. Structure and mechanical properties of giant lipid (DMPC) vesicle bilayers from 20.degree.C below to 10.degree.C above the liquid crystal-crystalline phase transition at 24.degree.C. Biochemistry. 1988;27:8261–8269.
   PubMed Web of Science ®Google Scholar
• Aranda-Espinoza H, Bermudez H, Bates FS, et al. Electromechanical Limits of Polymersomes. Physical Review Letters. 2001; 87: 208301.
   PubMed Web of Science ®Google Scholar
• Dimova R, Riske KA. Electrodeformation, electroporation, and electrofusion of giant unilamellar vesicles. In: Miklavcic D, editor. Handbook of electroporation. Cham: Springer International Publishing; 2016. p. 1–18.
   Google Scholar
• Faizi HA, Tsui A, Dimova R, et al. Bending rigidity, capacitance, and shear viscosity of giant vesicle membranes prepared by spontaneous swelling, electroformation, gel-assisted, and phase transfer methods: a comparative study. Langmuir. 2022;38:10548–10557.
   PubMed Web of Science ®Google Scholar
• Salipante PF, Vlahovska PM. Vesicle deformation in DC electric pulses. Soft Matter. 2014;10:3386–3393.
   PubMed Web of Science ®Google Scholar
• Dimova R, Seifert U, Pouligny B, et al. Hyperviscous diblock copolymer vesicles. Eur Phys J E. 2002;7:241–250.
   Web of Science ®Google Scholar
• Dimova R, Dietrich C, Hadjiisky A, et al. Falling ball viscosimetry of giant vesicle membranes: finite-size effects. Eur Phys J B. 1999; 12: 589–598.
   Web of Science ®Google Scholar
• Heimburg T. The capacitance and electromechanical coupling of lipid membranes close to transitions: the effect of electrostriction. Biophys J. 2012;103:918–929.
   PubMed Web of Science ®Google Scholar
• Gracià RS, Bezlyepkina N, Knorr RL, et al. Effect of cholesterol on the rigidity of saturated and unsaturated membranes: fluctuation and electrodeformation analysis of giant vesicles. Soft Matter. 2010;6:1472–1482.
   Web of Science ®Google Scholar
• Brochard F, Lennon JF. Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys. 1975;36:1035–1047.
   Google Scholar
• Faizi HA, Reeves CJ, Georgiev VN, et al. Fluctuation spectroscopy of giant unilamellar vesicles using confocal and phase contrast microscopy. Soft Matter. 2020;16:8996–9001.
   Web of Science ®Google Scholar
• Pecreaux J, Döbereiner H-G, Prost J, et al. Refined contour analysis of giant unilamellar vesicles. Eur Phys J E. 2004;13:277–290.
   PubMed Web of Science ®Google Scholar
• Dimova R. Recent developments in the field of bending rigidity measurements on membranes. Adv Colloid Interface Sci. 2014;208:225–234.
   PubMed Web of Science ®Google Scholar
• Faizi HA, Dimova R, Vlahovska PM. Electromechanical characterization of biomimetic membranes using electrodeformation of vesicles. ELECTROPHORESIS. 2021;42:2027–2032.
   PubMed Web of Science ®Google Scholar
• Kummrow M, Helfrich W. Deformation of giant lipid vesicles by electric fields. Phys Rev A. 1991;44:8356–8360.
   PubMed Web of Science ®Google Scholar
• Yamamoto T, Aranda-Espinoza S, Dimova R, et al. Stability of spherical vesicles in electric fields. Langmuir. 2010;26:12390–12407.
   PubMed Web of Science ®Google Scholar
• Aranda S, Riske KA, Lipowsky R, et al. Morphological transitions of vesicles induced by alternating electric fields. Biophys J. 2008;95:L19–L21.
   PubMed Web of Science ®Google Scholar
• Harbich W, Helfrich W. Alignment and opening of giant lecithin vesicles by electric fields. Z Naturforschung A. 1979;34:1063–1065.
   Google Scholar
• Niggemann G, Kummrow M, Helfrich W. The bending rigidity of phosphatidylcholine bilayers: dependences on experimental method, sample cell sealing and temperature. Journal de Physique II. 1995;5:413–425.
   Google Scholar
• Fricke N, Dimova R. GM1 Softens POPC membranes and induces the formation of micron-sized domains. Biophys J. 2016;111:1935–1945.
   PubMed Web of Science ®Google Scholar
• Vlahovska PM, Gracià RS, Aranda-Espinoza S, et al. Electrohydrodynamic model of vesicle deformation in alternating electric fields. Biophys J. 2009;96:4789–4803.
   PubMed Web of Science ®Google Scholar
• Hu Y, Vlahovska PM, Miksis MJ. Electrohydrodynamic assembly of colloidal particles on a drop interface. Math Biosci Eng. 2021;18:2357–2371.
   PubMed Web of Science ®Google Scholar
• Vlahovska PM. Electrohydrodynamics of Drops and Vesicles. Annu Rev Fluid Mech. 2019;51:305–330.
   Web of Science ®Google Scholar
• Vlahovska PM. Electrohydrodynamics of soft particles: role of the interface. in AIChE Annual Meeting, Conference Proceedings, Philadelphia (PA, USA). 2008.
   Google Scholar
• Karimi M, Steinkühler J, Roy D, et al. Asymmetric ionic conditions generate large membrane curvatures. Nano Lett. 2018;18:7816–7821.
   PubMed Web of Science ®Google Scholar
• Steinkühler J, De Tillieux P, Knorr RL, et al. Charged giant unilamellar vesicles prepared by electroformation exhibit nanotubes and transbilayer lipid asymmetry. Sci Rep. 2018;8:11838.
   PubMed Web of Science ®Google Scholar
• Yu M, Lira RB, Riske KA, et al. Ellipsoidal Relaxation of Deformed Vesicles. Phys Rev Lett. 2015;115:128303.
   PubMed Web of Science ®Google Scholar
• Portet T, Dimova R. A new method for measuring edge tensions and stability of lipid bilayers: effect of membrane composition. Biophys J. 2010;99:3264–3273.
   PubMed Web of Science ®Google Scholar
• Lira RB, Leomil FSC, Melo RJ, et al. To close or to collapse: the role of charges on membrane stability upon pore formation. Adv Sci. 2021;8:2004068.
   Web of Science ®Google Scholar
• Leomil FSC, Zoccoler M, Dimova R, et al. PoET: automated approach for measuring pore edge tension in giant unilamellar vesicles. Bioinf Adv, 2021. 1: p. vbab.;:037.
   Google Scholar
• Brochard-Wyart F, Gennes PG, Sandre O. Transient pores in stretched vesicles: role of leak-out. Phys A Stat Mech Appli. 2000;278:32–51.
   Google Scholar
• Sandre O, Moreaux L, Brochard-Wyart F. Dynamics of transient pores in stretched vesicles. Proc Nat Acad Sci. 1999;96:10591.
   PubMed Web of Science ®Google Scholar
• Karatekin E, Sandre O, Guitouni H, et al. Cascades of transient pores in giant vesicles: line tension and transport. Biophys J. 2003;84:1734–1749.
   PubMed Web of Science ®Google Scholar
• Sabri E, Aleksanyan, M, Brosseau, C, Dimova, R . Effects of solution conductivity on macropore size dynamics in electroporated lipid vesicle membranes. Bioelectrochemistry. 2022;147:108222.
   Google Scholar
• Aleksanyan M, Lira RB, Steinkühler J, et al. GM1 asymmetry in the membrane stabilizes pores. Biophys J. 2022;121:3295–3302.
   PubMed Web of Science ®Google Scholar
• Riske KA, Dimova R. Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys J. 2005;88:1143–1155.
   PubMed Web of Science ®Google Scholar
• Garten M, Mosgaard LD, Bornschlögl T, et al. Whole-GUV patch-clamping. Proc Natl Acad Sci U S A. 2017;114:328–333.
   PubMed Web of Science ®Google Scholar
• Henslee EA. Review: dielectrophoresis in cell characterization. Electrophoresis. 2020;41:1915–1930.
   PubMed Web of Science ®Google Scholar
• Gentet LJ, Stuart GJ, Clements JD. Direct measurement of specific membrane capacitance in neurons. Biophys J. 2000;79:314–320.
   PubMed Web of Science ®Google Scholar
• Liu P, Zabala-Ferrera O, Beltramo PJ. Fabrication and electromechanical characterization of freestanding asymmetric membranes. Biophys J. 2021;120:1755–1764.
   PubMed Web of Science ®Google Scholar
• Salipante PF, Knorr RL, Dimova R, et al. Electrodeformation method for measuring the capacitance of bilayer membranes. Soft Matter. 2012;8:3810–3816.
   Web of Science ®Google Scholar
• Vitkova V, Mitkova D, Antonova K, et al. Sucrose solutions alter the electric capacitance and dielectric permittivity of lipid bilayers. Colloids and Surfaces A. Colloids Surf A Physicochem Eng Asp. 2018;557:51–57.
   Web of Science ®Google Scholar
• Vitkova V, Yordanova V, Staneva G, et al. Dielectric properties of phosphatidylcholine membranes and the effect of sugars. Membranes. 2021;11:847.
   PubMed Web of Science ®Google Scholar
• Faizi HA, Dimova R, Vlahovska PM. A vesicle microrheometer for high-throughput viscosity measurements of lipid and polymer membranes. Biophys J. 2022;121:910–918.
   PubMed Web of Science ®Google Scholar
• Adrien, V., G. Rayan, K. Astafyeva, I. Broutin, M. Picard, P. Fuchs, W. Urbach, and N. Taulier. 2022.How to best estimate the viscosity of lipid bilayers. Biophysical Chemistry. 281:106732.
   Google Scholar
• Cicuta P, Keller SL, Veatch SL. Diffusion of liquid domains in lipid bilayer membranes. J Phys Chem A. 2007;111:3328–3331.
   PubMed Web of Science ®Google Scholar
• Sakuma Y, Kawakatsu T, Taniguchi T, et al. Viscosity landscape of phase-separated lipid membrane estimated from fluid velocity field. Biophys J. 2020;118:1576–1587.
   PubMed Web of Science ®Google Scholar
• Jahl PE, Parthasarathy R. Assessing the use of ellipsoidal microparticles for determining lipid membrane viscosity. Biophys J. 2021;120:5513–5520.
   PubMed Web of Science ®Google Scholar
• Dobereiner H-G, Evans E, Kraus M, et al. Mapping vesicle shapes into the phase diagram: a comparison of experiment and theory. Phys Rev E. 1997;55:4458–4474.
   Web of Science ®Google Scholar
• Lipowsky R. Understanding giant vesicles: a theoretical perspective. In: Dimova R, Marques C, editors. The giant vesicle book. Boca Raton: Taylor & Francis Group, LLC; 2019. p. 73–168.
   Google Scholar
• Micheletto, Y., N. Silveira, A. Dal-Bó, F. Giacomelli, N. Filho, T. Frizon, C. Marques, and A. Schroder. 2017. Study on the Application of Electric Field to Giant Vesicles Comprised of 1,2-Dilauroyl-Sn-Glycero-3-Phosphatidylcholine Using Optical Fluorescence Microscopy. Materials Research. 20. doi: 10.1590/1980-5373-mr-2016-0700
   Google Scholar
• Georgiev VN, Grafmüller A, Bléger D, et al. Area increase and budding in giant vesicles triggered by light: behind the scene. Adv Sci. 2018;5:1800432.
   Web of Science ®Google Scholar
• Aleksanyan, M., F. Crea, V. Georgiev, A. Grafmueller, J. Heberle, and R. Dimova (2021). Modulating membrane shape and mechanics by light. EUROPEAN BIOPHYSICS JOURNAL WITH BIOPHYSICS LETTERS. SPRINGER ONE NEW YORK PLAZA, SUITE 4600, 139. NEW YORK, NY, UNITED STATES.
   Google Scholar
• Mertins O, Bacellar IL, Thalmann F, et al. Physical damage on giant vesicles membrane as a result of methylene blue photoirradiation. Biophys J. 2014;106:162–171.
   PubMed Web of Science ®Google Scholar
• Mattei B, França ADC, Riske KA. Solubilization of binary lipid mixtures by the detergent triton X-100: the role of cholesterol. Langmuir. 2015;31:378–386.
   PubMed Web of Science ®Google Scholar
• Lira RB, Robinson T, Dimova R, et al. Highly efficient protein-free membrane fusion: a giant vesicle study. Biophys J. 2019;116:79–91.
   PubMedGoogle Scholar
• Steinkühler J, Agudo-Canalejo J, Lipowsky R, et al. Modulating vesicle adhesion by electric fields. Biophys J. 2016;111:1454–1464.
   PubMed Web of Science ®Google Scholar
• Riske KA, Sudbrack TP, Archilha NL, et al. Giant vesicles under oxidative stress induced by a membrane-anchored photosensitizer. Biophys J. 2009;97:1362–1370.
   PubMed Web of Science ®Google Scholar
• Erkan-Candag H, Krivic D, Gsell MAF, et al. Characterization of DAG binding to TRPC channels by target-dependent cis–trans isomerization of OptoDArG. Biomolecules. 2022;12:799.
   PubMed Web of Science ®Google Scholar
• Bhatia T, Robinson T, Dimova R. Membrane permeability to water measured by microfluidic trapping of giant vesicles. Soft Matter. 2020;16:7359–7369.
   PubMed Web of Science ®Google Scholar
• Yarmush ML, Golberg A, Serša G, et al. Electroporation-based technologies for medicine: principles, applications, and challenges. Annu Rev Biomed Eng. 2014;16:295–320.
   PubMed Web of Science ®Google Scholar
• Dev SB, Rabussay DP, Widera G, et al. Medical applications of electroporation. IEEE Trans Plasma Sci. 2000;28:206–223.
   Web of Science ®Google Scholar
• Riske KA, Knorr RL, Dimova R. Bursting of charged multicomponent vesicles subjected to electric pulses, Soft Matter. 2009;5:1983–1986.
   Google Scholar
• Kotnik T, Rems, L, Tarek, M, Miklavčič, D. Membrane electroporation and electropermeabilization: mechanisms and models. Annu Rev Biophys. 2019;48(1):63–91.
   PubMed Web of Science ®Google Scholar
• Rols M-P. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim Biophys Acta - Biomembr. 2006;1758:423–428.
   PubMed Web of Science ®Google Scholar
• Olbrich K, Rawicz W, Needham D, et al. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys J. 2000;79:321–327.
   PubMed Web of Science ®Google Scholar
• Salipante PF, Shapiro ML, Vlahovska PM. Electric field induced deformations of biomimetic fluid membranes. Vol. 16. Compiègne, France: Procedia IUTAM; 2015. p. 60–69.
   Google Scholar
• Lipowsky R. Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discussions. 2013;161:305–331.
   Google Scholar
• Lira RB, Steinkühler J, Knorr RL, et al. Posing for a picture: vesicle immobilization in agarose gel. Sci Rep. 2016;6:25254.
   PubMed Web of Science ®Google Scholar
• van Uitert I, Le Gac S, van den Berg A. The influence of different membrane components on the electrical stability of bilayer lipid membranes. Biochim Biophys Acta - Biomembr. 2010;1798:21–31.
   Web of Science ®Google Scholar
• Dasgupta R, Miettinen MS, Fricke N, et al. The glycolipid GM1 reshapes asymmetric biomembranes and giant vesicles by curvature generation. Proc Natl Acad Sci U S A. 2018;115:5756–5761.
   PubMed Web of Science ®Google Scholar
• Chen S, Yang D, Wen Y, et al. Dysregulated hemolysin liberates bacterial outer membrane vesicles for cytosolic lipopolysaccharide sensing. PLoS Pathog. 2018;14:e1007240–e1007240.
   PubMed Web of Science ®Google Scholar
• Perrier DL, Vahid A, Kathavi V, et al. Response of an actin network in vesicles under electric pulses. Sci Rep. 2019;9:8151.
   PubMed Web of Science ®Google Scholar
• Muralidharan A, Rems L, Kreutzer MT, et al. Actin networks regulate the cell membrane permeability during electroporation. Biochim Biophys Acta Biomembr. 2021;1863:183468.
   PubMed Web of Science ®Google Scholar
• Lira RB, Dimova R, Riske KA. Giant unilamellar vesicles formed by hybrid films of agarose and lipids display altered mechanical properties. Biophys J. 2014;107:1609–1619.
   PubMed Web of Science ®Google Scholar
• Knorr RL, Staykova M, Gracià RS, et al. Wrinkling and electroporation of giant vesicles in the gel phase. Soft Matter. 2010;6:1990–1996.
   Web of Science ®Google Scholar
• Perrier DL, Rems L, Kreutzer MT, et al. The role of gel-phase domains in electroporation of vesicles. Sci Rep. 2018;8:4758.
   PubMed Web of Science ®Google Scholar
• Portet T, Camps I Febrer F, Escoffre J-M, et al. Visualization of membrane loss during the shrinkage of giant vesicles under electropulsation. Biophys J. 2009;96:4109–4121.
   PubMed Web of Science ®Google Scholar
• Portet T, Favard C, Teissié J, et al. Insights into the mechanisms of electromediated gene delivery and application to the loading of giant vesicles with negatively charged macromolecules. Soft Matter. 2011;7:3872–3881.
   Web of Science ®Google Scholar
• Rems L, Tang, X, Zhao, F, Pérez-Conesa, S, Testa, I, Delemotte, L . Identification of electroporation sites in the complex lipid organization of the plasma membrane. eLife. 2022;11:e74773.
   Google Scholar
• Breton M, Amirkavei M, Mir LM. Optimization of the electroformation of giant unilamellar vesicles (GUVs) with unsaturated phospholipids. J Membr Biol. 2015;248:827–835.
   PubMed Web of Science ®Google Scholar
• Gabriel B, Teissié J. Generation of reactive-oxygen species induced by electropermeabilization of Chinese hamster ovary cells and their consequence on cell viability. Eur J Biochem. 1994;223:25–33.
   PubMedGoogle Scholar
• Wiczew D, Szulc N, Tarek M. Molecular dynamics simulations of the effects of lipid oxidation on the permeability of cell membranes. Bioelectrochemistry; 2021;141:107869.
   Google Scholar
• Sözer EB, Levine ZA, Vernier PT. Quantitative limits on small molecule transport via the electropermeome — measuring and modeling single nanosecond perturbations. Sci Rep. 2017;7:57.
   PubMed Web of Science ®Google Scholar
• Sözer EB, Pocetti CF, Vernier PT. Transport of charged small molecules after electropermeabilization — drift and diffusion. BMC Biophys. 2018;11:4.
   PubMed Web of Science ®Google Scholar
• Sözer EB, Pocetti CF, Vernier PT. Asymmetric patterns of small molecule transport after nanosecond and microsecond electropermeabilization. J Membr Biol. 2018;251:197–210.
   PubMed Web of Science ®Google Scholar
• Messina P, Lemaître F, Huet F, et al. Monitoring and quantifying the passive transport of molecules through patch-clamp suspended real and model cell membranes. Angew Chem Int Ed Engl. 2014;53:3192–3196.
   PubMed Web of Science ®Google Scholar
• Mosharov EV, Sulzer D. Analysis of exocytotic events recorded by amperometry. Nat Methods. 2005;2:651–658.
   PubMed Web of Science ®Google Scholar
• Ben Trad F, Wieczny V, Delacotte J, et al. Dynamic electrochemiluminescence imaging of single giant liposome opening at polarized electrodes. Anal Chem. 2022;94:1686–1696.
   PubMed Web of Science ®Google Scholar
• Mauroy C, Portet, T, Winterhalder, M, Bellard, E, Blache, MC, Teissié, J, Zumbusch, A, Rols, MP Giant lipid vesicles under electric field pulses assessed by non invasive imaging. Bioelectrochemistry. 2012;87:253–259.
   Google Scholar
• Akashi K, Miyata H, Itoh H, et al. Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. Biophys J. 1996;71:3242–3250.
   PubMed Web of Science ®Google Scholar
• Dos Santos Cabrera MP, Alvares DS, Leite NB, et al. New insight into the mechanism of action of wasp mastoparan peptides: lytic activity and clustering observed with giant vesicles. Langmuir. 2011;27:10805–10813.
   PubMed Web of Science ®Google Scholar
• Ewins E, Lira RB, Zhang W, et al. Poly(Ionic Liquid) nanoparticles selectively disrupt biomembranes. Adv Sci. 2019;6:1801602.
   Web of Science ®Google Scholar
• Lira RB, Steinkühler J, Knorr RL, et al. Posing for a picture: vesicle immobilization in agarose gel. Sci Rep. 2016;6:25254.
   PubMed Web of Science ®Google Scholar
• Golzio M, Teissié J, Rols M-P. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci U S A. 2002;99:1292–1297.
   PubMed Web of Science ®Google Scholar
• Sözer EB, Haldar S, Blank PS, et al. Dye transport through bilayers agrees with lipid electropore molecular dynamics. Biophys J. 2020;119:1724–1734.
   PubMed Web of Science ®Google Scholar
• Young JL, Dean DA. Electroporation-mediated gene delivery. Adv Genet. 2015;89:49–88.
   PubMed Web of Science ®Google Scholar
• Broderick KE, Humeau LM. Electroporation-enhanced delivery of nucleic acid vaccines. Expert Rev Vaccines. 2015;14:195–204.
   PubMed Web of Science ®Google Scholar
• Rosazza C, Deschout H, Buntz A, et al. Endocytosis and endosomal trafficking of DNA after gene electrotransfer in vitro. Mol Ther Nucleic Acids. 2016;5:e286.
   PubMedGoogle Scholar
• Escoffre J-M, Mauroy C, Portet T, et al. Gene electrotransfer: from biophysical mechanisms to in vivo applications: part 2 - In vivo developments and present clinical applications. Biophys Rev. 2009;1:185.
   PubMedGoogle Scholar
• Venslauskas MS, Šatkauskas S. Mechanisms of transfer of bioactive molecules through the cell membrane by electroporation. Eur Biophys J. 2015;44:277–289.
   PubMed Web of Science ®Google Scholar
• Breton M, Delemotte L, Silve A, et al. Transport of siRNA through lipid membranes driven by nanosecond electric pulses: an experimental and computational study. J Am Chem Soc. 2012;134:13938–13941.
   PubMed Web of Science ®Google Scholar
• Yu M, Tan W, Lin H. A stochastic model for DNA translocation through an electropore. Biochim Biophys Acta - Biomembr. 2012;1818:2494–2501.
   Web of Science ®Google Scholar
• Sachdev S, Muralidharan A, Choudhary DK, et al. DNA translocation to giant unilamellar vesicles during electroporation is independent of DNA size. Soft Matter. 2019;15:9187–9194.
   PubMed Web of Science ®Google Scholar
• Barlow ST, Figueroa B, Fu D, et al. Membrane tension modifies redox loading and release in single liposome electroanalysis. Anal Chem. 2021;93:3876–3882.
   PubMed Web of Science ®Google Scholar
• Choi Y, Park C, Kang Y, et al. Temporally resolved electrochemical interrogation for stochastic collision dynamics of electrogenerated single polybromide droplets. Anal Chem. 2021;93:8336–8344.
   PubMed Web of Science ®Google Scholar
• Winterhalder MJ, Zumbusch A. Beyond the borders — biomedical applications of non-linear Raman microscopy. Adv Drug Deliv Rev. 2015;89:135–144.
   PubMed Web of Science ®Google Scholar
• Zumbusch A, Langbein W, Borri P. Nonlinear vibrational microscopy applied to lipid biology. Prog Lipid Res. 2013;52:615–632.
   PubMed Web of Science ®Google Scholar
• Riske KA, Dimova R. Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. Biophys J. 2006;91:1778–1786.
   PubMed Web of Science ®Google Scholar
• Vlahovska PM. Voltage-morphology coupling in biomimetic membranes: dynamics of giant vesicles in applied electric fields. Soft Matter. 2015;11:7232–7236.
   PubMed Web of Science ®Google Scholar
• Faizi HA, Frey SL, Steinkühler J, et al. Bending rigidity of charged lipid bilayer membranes. Soft Matter. 2019;15:6006–6013.
   PubMed Web of Science ®Google Scholar
• Winterhalter M, Helfrich W. Effect of surface charge on the curvature elasticity of membranes. J Phys Chem. 1988;92:6865–6867.
   Web of Science ®Google Scholar
• Lekkerkerker HNW. Contribution of the electric double layer to the curvature elasticity of charged amphiphilic monolayers. Physica A. Phys A Stat Mech Appli. 1989;159:319–328.
   Web of Science ®Google Scholar
• Lacoste D, Menon GI, Bazant MZ, et al. Electrostatic and electrokinetic contributions to the elastic moduli of a driven membrane. Eur Phys J E. 2009;28:243–264.
   PubMed Web of Science ®Google Scholar
• Loubet B, Hansen PL, Lomholt MA. Electromechanics of a membrane with spatially distributed fixed charges: flexoelectricity and elastic parameters. Phys Rev E. 2013;88:062715.
   Web of Science ®Google Scholar