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Destabilizing Giant Vesicles with Electric Fields: An Overview of Current Applications

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Abstract

This review presents an overview of the effects of electric fields on giant unilamellar vesicles. The application of electrical fields leads to three basic phenomena: shape changes, membrane breakdown, and uptake of molecules. We describe how some of these observations can be used to measure a variety of physical properties of lipid membranes or to advance our understanding of the phenomena of electropermeabilization. We also present results on how electropermeabilization and other liposome responses to applied fields are affected by lipid composition and by the presence of molecules of therapeutic interest in the surrounding solution.

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References

  • Angelova MI, Dimitrov DS (1986) Liposome electroformation. Biophys J 81:303–311

    CAS  Google Scholar 

  • Aranda S, Riske KA, Lipowsky R, Dimova R (2008) Morphological transitions of vesicles induced by alternating electric fields. Biophys J 95:L19–L21

    Article  PubMed  CAS  Google Scholar 

  • Belehradek M, Domenge C, Luboinski B, Orlowski S, Belehradek J Jr, Mir LM (1993) Electrochemotherapy, a new antitumor treatment. First clinical phase I–II trial. Cancer 72:3694–3700

    Article  PubMed  CAS  Google Scholar 

  • Brochard-Wyart F, de Gennes PG, Sandre O (2000) Transient pores in stretched vesicles: role of leak-out. Phys A 278:32–51

    Article  CAS  Google Scholar 

  • Carr CM, Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823–832

    Article  PubMed  CAS  Google Scholar 

  • Chernomordik LV, Kozlov MM (2003) Protein-lipid interplay in fusion and fission of biological membranes. Annu Rev Biochem 72:175–207

    Article  PubMed  CAS  Google Scholar 

  • Chernomordik LV, Sokolov AV, Budker VG (1990) Electrostimulated uptake of DNA by liposomes. Biochim Biophys Acta 1024:179–183

    Article  PubMed  CAS  Google Scholar 

  • Chiu DT, Wilson CF, Ryttsen F, Stromberg A, Farre C, Karlsson A, Nordholm S, Gaggar A, Modi BP, Moscho A, Garza-Lopez RA, Orwar O, Zare RN (1999) Chemical transformations in individual ultrasmall biomimetic containers. Science 283:1892–1895

    Article  PubMed  CAS  Google Scholar 

  • Dimova R, Aranda S, Bezlyepkina N, Nikolov V, Riske KA, Lipowsky R (2006) A practical guide to giant vesicles. Probing the membrane nanoregime via optical microscopy. J Phys Condens Matter 18:S1151–S1176

    Article  PubMed  CAS  Google Scholar 

  • Dimova R, Riske KA, Aranda S, Bezlyepkina N, Knorr RL, Lipowsky R (2007) Giant vesicles in electric fields. Soft Matter 3:817–827

    Article  CAS  Google Scholar 

  • Dimova R, Bezlyepkina N, Domange Jordo M, Knorr RL, Riske KA, Staykova M, Vlahovska PM, Yamamoto T, Yang P, Lipowsky R (2009) Vesicles in electric fields: some novel aspects of membrane behavior. Soft Matter 5:3201–3212

    Article  CAS  Google Scholar 

  • Eitzen G (2003) Actin remodeling to facilitate membrane fusion. Biochim Biophys Acta 1641:175–181

    Article  PubMed  CAS  Google Scholar 

  • Escoffre JM, Portet T, Wasungu L, Teissie J, Dean D, Rols MP (2009) What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues. Mol Biotechnol 41:286–295

    Article  PubMed  CAS  Google Scholar 

  • Estes DJ, Mayer M (2005) Giant liposomes in physiological buffer using electroformation in a flow chamber. Biochim Biophys Acta 1712:152–160

    Article  PubMed  CAS  Google Scholar 

  • Faucon JF, Mitov MD, Méléard P, Bivas I, Bothorel P (1989) Bending elasticity and thermal fluctuations of lipid membranes. Theoretical and experimental requirements. J Phys 50:2389–2414

    Article  Google Scholar 

  • Fromherz P, Röcker C, Rüppel D (1986) From discoid micelles to spherical vesicles. The concept of edge activity. Faraday Discuss Chem Soc 81:39–48

    Article  CAS  Google Scholar 

  • Golzio M, Teissie J, Rols MP (2002) Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci U S A 99:1292–1297

    Article  PubMed  CAS  Google Scholar 

  • Gracia RS, Bezlyepkina N, Knorr RL, Lipowsky R, Dimova R (2010) Effect of cholesterol on the rigidity of saturated and unsaturated membranes: fluctuation and electrodeformation analysis of giant vesicles. Soft Matter 6:1472–1482

    Article  CAS  Google Scholar 

  • Haluska CK, Riske KA, Marchi-Artzner V, Lehn JM, Lipowsky R, Dimova R (2006) Time scales of membrane fusion revealed by direct imaging of vesicle fusion with high temporal resolution. Proc Natl Acad Sci U S A 103:15841–15846

    Article  PubMed  CAS  Google Scholar 

  • Harbich W, Helfrich W (1979) Alignment and opening of giant lecithin vesicles by electric fields. Z Naturforsch 34:1063–1065

    Google Scholar 

  • Hay JC (2007) Calcium: a fundamental regulator of intracellular membrane fusion? EMBO Rep 8:236–240

    Article  PubMed  CAS  Google Scholar 

  • Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28:693–703

    PubMed  CAS  Google Scholar 

  • Helm CA, Israelachvili JN, McGuiggan PM (1992) Role of hydrophobic forces in bilayer adhesion and fusion. Biochemistry 31:1794–1805

    Article  PubMed  CAS  Google Scholar 

  • Horger KS, Estes DJ, Capone R, Mayer M (2009) Films of agarose enable rapid formation of giant liposomes in solutions of physiologic ionic strength. J Am Chem Soc 131:1810–1819

    Article  PubMed  CAS  Google Scholar 

  • Jeremic A, Kelly M, Cho JA, Cho SJ, Horber JK, Jena BP (2004) Calcium drives fusion of SNARE-apposed bilayers. Cell Biol Int 28:19–31

    Article  PubMed  CAS  Google Scholar 

  • Jorgacevski J, Fosnaric M, Vardjan N, Stenovec M, Potokar M, Kreft M, Kralj-Iglic V, Iglic A, Zorec R (2010) Fusion pore stability of peptidergic vesicles. Mol Membr Biol 27:65–80

    Article  PubMed  CAS  Google Scholar 

  • Karatekin E, Sandre O, Guitouni H, Borghi N, Puech PH, Brochard-Wyart F (2003) Cascades of transient pores in giant vesicles: line tension and transport. Biophys J 84:1734–1749

    Article  PubMed  CAS  Google Scholar 

  • Kielian M, Rey FA (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4:67–76

    Article  PubMed  CAS  Google Scholar 

  • Knorr RL, Staykova M, Gracia RS, Dimova R (2010) Wrinkling and electroporation of giant vesicles in the gel phase. Soft Matter 6:1990–1996

    Article  CAS  Google Scholar 

  • Kozlovsky Y, Kozlov MM (2002) Stalk model of membrane fusion: solution of energy crisis. Biophys J 82:882–895

    Article  PubMed  CAS  Google Scholar 

  • Kummrow M, Helfrich W (1991) Deformation of giant lipid vesicles by electric fields. Phys Rev A 44:8356–8360

    Article  PubMed  CAS  Google Scholar 

  • Lentz BR (1994) Polymer-induced membrane fusion: potential mechanism and relation to cell fusion events. Chem Phys Lipids 73:91–106

    Article  PubMed  CAS  Google Scholar 

  • Lentz BR, Malinin V, Haque ME, Evans K (2000) Protein machines and lipid assemblies: current views of cell membrane fusion. Curr Opin Struct Biol 10:607–615

    Article  PubMed  CAS  Google Scholar 

  • Lopez A, Rols MP, Teissie J (1988) 31P NMR analysis of membrane phospholipid organization in viable, reversibly electropermeabilized Chinese hamster ovary cells. Biochemistry 27:1222–1228

    Article  PubMed  CAS  Google Scholar 

  • Lurquin PF, Athanasiou K (2000) Electric field-mediated DNA encapsulation into large liposomes. Biochem Biophys Res Commun 267:838–841

    Article  PubMed  CAS  Google Scholar 

  • Marsh D (2006) Elastic curvature constants of lipid monolayers and bilayers. Chem Phys Lipids 144:146–159

    Article  PubMed  CAS  Google Scholar 

  • Mathivet L, Cribier S, Devaux PF (1996) Shape change and physical properties of giant phospholipid vesicles prepared in the presence of an AC electric field. Biophys J 70:1112–1121

    Article  PubMed  CAS  Google Scholar 

  • McLaughlin S (1989) The electrostatic properties of membranes. Annu Rev Biophys Biophys Chem 18:113–136

    Article  PubMed  CAS  Google Scholar 

  • Milner ST, Safran SA (1987) Dynamical fluctuations of droplet microemulsions and vesicles. Phys Rev A 36:4371–4379

    Article  PubMed  CAS  Google Scholar 

  • Mitov MD, Meleard P, Winterhalter M, Angelova MI, Bothorel P (1993) Electric-field-dependent thermal fluctuations of giant vesicles. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 48:628–631

    Article  PubMed  CAS  Google Scholar 

  • Montes LR, Alonso A, Goni FM, Bagatolli LA (2007) Giant unilamellar vesicles electroformed from native membranes and organic lipid mixtures under physiological conditions. Biophys J 93:3548–3554

    Article  PubMed  CAS  Google Scholar 

  • Needham D, Hochmuth RM (1989) Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. Biophys J 55:1001–1009

    Article  PubMed  CAS  Google Scholar 

  • Neumann E, Sowers A, Jordan C (1989) Electroporation and electrofusion in cell biology. Plenum, New York

    Google Scholar 

  • Portet T, Dimova R (2010) A new method for measuring edge tensions and stability of lipid bilayers: effect of membrane composition. Biophys J 99:3264–3273

    Article  PubMed  CAS  Google Scholar 

  • Portet T, Camps i Febrer F, Escoffre JM, Favard C, Rols MP, Dean DS (2009) Visualization of membrane loss during the shrinkage of giant vesicles under electropulsation. Biophys J 96:4109–4121

    Article  PubMed  CAS  Google Scholar 

  • Portet T, Favard C, Teissie J, Dean DS, Rols MP (2011) Insights into the mechanisms of electromediated gene delivery and application to the loading of giant vesicles with negatively charged macromolecules. Soft Matter 7:3872–3881

    Article  CAS  Google Scholar 

  • Pott T, Bouvrais H, Meleard P (2008) Giant unilamellar vesicle formation under physiologically relevant conditions. Chem Phys Lipids 154:115–119

    Article  PubMed  CAS  Google Scholar 

  • Riske KA, Dimova R (2005) Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys J 88:1143–1155

    Article  PubMed  CAS  Google Scholar 

  • Riske KA, Dimova R (2006) Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. Biophys J 91:1778–1786

    Article  PubMed  CAS  Google Scholar 

  • Riske KA, Bezlyepkina N, Lipowsky R, Dimova R (2006) Electrofusion of model lipid membranes viewed with high temporal resolution. Biophys Rev Lett 1:387–400

    Article  CAS  Google Scholar 

  • Riske KA, Knorr RL, Dimova R (2009) Bursting of charged multicomponent vesicles subjected to electric pulses. Soft Matter 5:1983–1986

    Article  CAS  Google Scholar 

  • Rodriguez N, Pincet F, Cribier S (2005) Giant vesicles formed by gentle hydration and electroformation: a comparison by fluorescence microscopy. Colloids Surf B Biointerfaces 42:125–130

    Article  PubMed  CAS  Google Scholar 

  • Rols MP, Teissie J (1989) Ionic-strength modulation of electrically induced permeabilization and associated fusion of mammalian cells. Eur J Biochem 179:109–115

    Article  PubMed  CAS  Google Scholar 

  • Sandre O, Moreaux L, Brochard-Wyart F (1999) Dynamics of transient pores in stretched vesicles. Proc Natl Acad Sci U S A 96:10591–10596

    Article  PubMed  CAS  Google Scholar 

  • Schneider MB, Jenkins JT, Webb WW (1984) Thermal fluctuations of large cylindrical phospholipid vesicles. Biophys J 45:891–899

    Article  PubMed  CAS  Google Scholar 

  • Sharma V, Stebe K, Murphy JC, Tung L (1996) Poloxamer 188 decreases susceptibility of artificial lipid membranes to electroporation. Biophys J 71:3229–3241

    Article  PubMed  CAS  Google Scholar 

  • Sowers AE (1986) A long-lived fusogenic state is induced in erythrocyte ghosts by electric pulses. J Cell Biol 102:1358–1362

    Article  PubMed  CAS  Google Scholar 

  • Staykova M, Lipowsky R, Dimova R (2008) Membrane flow patterns in multicomponent giant vesicles induced by alternating electric fields. Soft Matter 4:2168–2171

    Article  PubMed  CAS  Google Scholar 

  • Tamm LK, Crane J, Kiessling V (2003) Membrane fusion: a structural perspective on the interplay of lipids and proteins. Curr Opin Struct Biol 13:453–466

    Article  PubMed  CAS  Google Scholar 

  • Teissie J, Rols MP (1986) Fusion of mammalian cells in culture is obtained by creating the contact between cells after their electropermeabilization. Biochem Biophys Res Commun 140:258–266

    Article  PubMed  CAS  Google Scholar 

  • Teissie J, Rols MP (1993) An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization. Biophys J 65:409–413

    Article  PubMed  CAS  Google Scholar 

  • Tekle E, Astumian RD, Friauf WA, Chock PB (2001) Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. Biophys J 81:960–968

    Article  PubMed  CAS  Google Scholar 

  • Vlahovska PM, Gracia RS, Aranda-Espinoza S, Dimova R (2009) Electrohydrodynamic model of vesicle deformation in alternating electric fields. Biophys J 96:4789–4803

    Article  PubMed  CAS  Google Scholar 

  • Weissenhorn W, Hinz A, Gaudin Y (2007) Virus membrane fusion. FEBS Lett 581:2150–2155

    Article  PubMed  CAS  Google Scholar 

  • Winterhalter M, Helfrich W (1988) Deformation of spherical vesicles by electric fields. J Colloid Interface Sci 122:583–586

    Article  CAS  Google Scholar 

  • Yamamoto T, Aranda-Espinoza S, Dimova R, Lipowsky R (2010) Stability of spherical vesicles in electric fields. Langmuir 26:12390–12407

    Article  PubMed  CAS  Google Scholar 

  • Yang P, Lipowsky R, Dimova R (2009) Nanoparticle formation in giant vesicles: synthesis in biomimetic compartments. Small 5:2033–2037

    Article  PubMed  CAS  Google Scholar 

  • Yu YG, King DS, Shin YK (1994) Insertion of a coiled-coil peptide from influenza virus hemagglutinin into membranes. Science 266:274–276

    Article  PubMed  CAS  Google Scholar 

  • Zhelev DV, Needham D (1993) Tension-stabilized pores in giant vesicles: determination of pore size and pore line tension. Biochim Biophys Acta 1147:89–104

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann U (1982) Electric field-mediated fusion and related electrical phenomena. Biochim Biophys Acta 694:227–277

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge financial support from the Institut Universitaire de France, ANR-PCV (project CMIDT-139888), and the Association Française contre les Myopathies. We thank our colleagues C. Favard, J. Tessié, L. Wasungu, N. Mignet, M. Bureau, and D. Scherman for many useful discussions and interactions on the subjects discussed in this review.

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Correspondence to Marie-Pierre Rols.

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Thomas Portet and Chloé Mauroy contributed equally to this review.

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Portet, T., Mauroy, C., Démery, V. et al. Destabilizing Giant Vesicles with Electric Fields: An Overview of Current Applications. J Membrane Biol 245, 555–564 (2012). https://doi.org/10.1007/s00232-012-9467-x

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