Abstract
Irreversible electroporation (IRE) is a technique for the disruption of localized cells or vesicles by a series of short and high−frequency electric pulses which has been used for tissue ablation and treatment in certain diseases. It is well reported that IRE induces lateral tension in the membranes of giant unilamellar vesicles (GUVs). The GUVs are prepared by a mixture of anionic lipid dioleoylphosphatidylglycerol (DOPG) and neutral lipid dioleoylphosphatidylcholine (DOPC) using the natural swelling method. Here the influence of DOPG mole fraction, XDOPG, on the critical tension of electroporation in GUVs has been investigated in sodium chloride-containing PIPES buffer. The critical tension decreases from 9.0 ± 0.3 to 6.0 ± 0.2 mN/m with the increase of XDOPG from 0.0 to 0.60 in the membranes of GUVs. Hence an increase in XDOPG greatly decreases the mechanical stability of membranes. We develop a theoretical equation that fits the XDOPG dependent normalized critical tension, and obtain a binding constant for the lipid-ion interaction of 0.75 M−1. The decrease in the energy barrier for formation of the nano−size nascent or prepore state, due to the increase in XDOPG, is the main factor explaining the decrease in critical tension of electroporation in vesicles.
References
Abidor IG, Arakelyan VB, Chernomordik LV, Chizmadzhev YA, Pastushenko VF, Tarasevich MR (1979) Electric breakdown of bilayer lipid membranes: I. The main experimental facts and their qualitative discussion. J Electroanal Chem Interfacial Electrochem 104:37–52. https://doi.org/10.1016/S0022-0728(79)81006-2
Ahamed MK, Karal MAS, Ahmed M, Ahammed S (2020) Kinetics of irreversible pore formation under constant electrical tension in giant unilamellar vesicles. Eur Biophys 49:371–381. https://doi.org/10.1007/s00249-020-01440-1
Akimov SA, Volynsky PE, Galimzyanov TR, Kuzmin PI, Pavlov KV, Batishchev OV (2017) Pore formation in lipid membrane II: Energy landscape under external stress. Sci Rep 7:12509. https://doi.org/10.1038/s41598-017-12749-x
Al-Sakere B, André F, Bernat C, Connault E, Opolon P, Davalos RV, Rubinsky B, Mir LM (2007) Tumor ablation with irreversible electroporation. PLoS ONE 2:e1135. https://doi.org/10.1371/journal.pone.0001135
Betterton MD, Brenner MP (1999) Electrostatic edge instability of lipid membranes. Phys Rev Lett 82:1598–1601. https://doi.org/10.1103/PhysRevLett.82.1598
Böckmann RA, de Groot BL, Kakorin S, Neumann E, Grubmuller H (2008) Kinetics, statistics, and energetics of lipid membrane electroporation studied by molecular dynamics simulations. Biophys J 95:1837–1850. https://doi.org/10.1529/biophysj.108.129437
Cevc G (1987) Phospholipid bilayers : Physical principles and models. Wiley, New York
Cevc G (1990) Membrane electrostatics. Biochim Biophys Acta (BBA) Rev Biomem 1031:311–382. https://doi.org/10.1016/0304-4157(90)90015-5
Dev SB, Rabussay DP, Widera G, Hofmann GA (2000) Medical applications of electroporation. IEEE Trans Plasma Sci 28:206–223. https://doi.org/10.1109/27.842905
Diederich A, Bähr G, Winterhalter M (1998) Influence of surface charges on the rupture of black lipid membranes. Phys Rev E 58:4883–4889. https://doi.org/10.1103/PhysRevE.58.4883
Dimova R, Riske KA, Aranda S, Bezlyepkina N, Knorr RL, Lipowsky R (2007) Giant vesicles in electric fields. Soft Matter 3:817. https://doi.org/10.1039/b703580b
Dimova R, Bezlyepkina N, Jordö MD, 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. https://doi.org/10.1039/b901963d
Evans E, Smith BA (2011) Kinetics of hole nucleation in biomembrane rupture. New J Phys 13:095010. https://doi.org/10.1088/1367-2630/13/9/095010
Evans E, Heinrich V, Ludwig F, Rawicz W (2003) Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85:2342–2350. https://doi.org/10.1016/S0006-3495(03)74658-X
Israelachvili JN (2011) Intermolecular and surface forces, 3rd edn. London, UK, Academic Press
Karal MAS, Levadnyy V, Tsuboi T-A, Belaya M, Yamazaki M (2015) Electrostatic interaction effects on tension-induced pore formation in lipid membranes. Phys Rev E 92:012708. https://doi.org/10.1103/PhysRevE.92.012708
Karal MAS, Levadnyy V, Yamazaki M (2016) Analysis of constant tension-induced rupture of lipid membranes using activation energy. Phys Chem Chem Phys 18:13487–13495. https://doi.org/10.1039/C6CP01184E
Karal MAS, Ahamed MK, Rahman M, Ahmed M, Shakil MM, Rabbani KS (2019) Effects of electrically-induced constant tension on giant unilamellar vesicles using irreversible electroporation. Eur Biophys J 48:731–741. https://doi.org/10.1007/s00249-019-01398-9
Karal MAS, Rahman M, Ahamed MK, Shibly SUA, Ahmed M, Shakil MM (2019) Low cost non-electromechanical technique for the purification of giant unilamellar vesicles. Eur Biophys J 48:349–359. https://doi.org/10.1007/s00249-019-01363-6
Karal MAS, Ahamed MK, Ahmed M, Ahamed S, Mahbub ZB (2020) Location of peptide-induced submicron discontinuities in the membranes of vesicles using ImageJ. J Fluoresc 30:735–740. https://doi.org/10.1007/s10895-020-02560-9
Karal MAS, Ahamed MK, Mokta NA, Ahmed M, Ahammed S (2020) Influence of cholesterol on electroporation in lipid membranes of giant vesicles. Eur Biophys J 49:361–370. https://doi.org/10.1007/s00249-020-01443-y
Karal MAS, Ahammed S, Levadny V, Levadny V, Belaya M, Ahamed MK, Ahmed M, Mahbub ZB, Ullah AKMA (2020) Deformation and poration of giant unilamellar vesicles induced by anionic nanoparticles. Chem Phys Lipids. https://doi.org/10.1016/j.chemphyslip.2020.104916
Karal MAS, Islam MK, Mahbub ZB (2020) Study of molecular transport through a single nanopore in the membrane of a giant unilamellar vesicle using COMSOL simulation. Eur Biophys J 49:59–69. https://doi.org/10.1007/s00249-019-01412-0
Karal MAS, Orchi US, Towhiduzzaman M, Ahamed MK, Ahmed M, Ahammed S, Mokta NA, Sharmin S, Sarkar MK (2020) Electrostatic effects on the electrical tension-induced irreversible pore formation in giant unilamellar vesicles. Chem Phys Lipids 231:104935. https://doi.org/10.1016/j.chemphyslip.2020.104935
Karatekin E, Sandre O, Guitouni H et al (2003) Cascades of transient pores in giant vesicles: line tension and transport. Biophys J 84:1734–1749. https://doi.org/10.1016/S0006-3495(03)74981-9
Kraayenhof R, Sterk GJ, Sang HWWF, Krab K, Epand RM (1996) Monovalent cations differentially affect membrane surface properties and membrane curvature, as revealed by fluorescent probes and dynamic light scattering. Biochim Biophys Acta (BBA) Biomem 1282:293–302. https://doi.org/10.1016/0005-2736(96)00069-7
Langner M, Kubica K (1999) The electrostatics of lipid surfaces. Chem Phys Lipids 101:3–35. https://doi.org/10.1016/S0009-3084(99)00052-3
Lekkerkerker HNW (1989) Contribution of the electric double layer to the curvature elasticity of charged amphiphilic monolayers. Physica A 159:319–328. https://doi.org/10.1016/0378-4371(89)90400-7
Levadny V, Tsuboi T, Belaya M, Yamazaki M (2013) Rate constant of tension-induced pore formation in lipid membranes. Langmuir 29:3848–3852. https://doi.org/10.1021/la304662p
Levine ZA, Vernier PT (2010) Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation. J Membrane Biol 236:27–36. https://doi.org/10.1007/s00232-010-9277-y
Lisin R, Zion Ginzburg B, Schlesinger M, Feldman Y (1996) Time domain dielectric spectroscopy study of human cells. I. Erythrocytes and ghosts. Biochim Biophys Acta (BBA) Biomem 1280:34–40. https://doi.org/10.1016/0005-2736(95)00266-9
May S (1996) Curvature elasticity and thermodynamic stability of electrically charged membranes. J Chem Phys 105:8314–8323. https://doi.org/10.1063/1.472686
Meier W, Graff A, Diederich A, Winterhalter M (2000) Stabilization of planar lipid membranes: A stratified layer approach. Phys Chem Chem Phys 2:4559–4562. https://doi.org/10.1039/b004073h
Miklavcic D (2017) Handbook of Electroporation. Springer International Publishing, Switzerland. https://doi.org/10.1007/978-3-319-26779-1
Miller L, Leor J, Rubinsky B (2005) Cancer cells ablation with irreversible electroporation. Technol Cancer Res Treat 4:699–705. https://doi.org/10.1177/153303460500400615
Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta (BBA) Rev Biomem 1469:159–195. https://doi.org/10.1016/S0304-4157(00)00016-2
Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328–339
Reeves JP, Dowben RM (1969) Formation and properties of thin-walled phospholipid vesicles. J Cell Physiol 73:49–60. https://doi.org/10.1002/jcp.1040730108
Riske KA, Dimova R (2005) Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys J 88:1143–1155. https://doi.org/10.1529/biophysj.104.050310
Rowan NJ, MacGregor SJ, Anderson JG, Fouracre RA, Farish O (2000) Pulsed electric field inactivation of diarrhoeagenic Bacillus cereus through irreversible electroporation. Lett Appl Microbiol 31:110–114. https://doi.org/10.1046/j.1365-2672.2000.00772.x
Sandre O, Moreaux L, Brochard-Wyart F (1999) Dynamics of transient pores in stretched vesicles. Proc Natl Acad Sci USA 96:10591–10596. https://doi.org/10.1073/pnas.96.19.10591
Shoemaker SD, Vanderlick TK (2002) Intramembrane electrostatic interactions destabilize lipid vesicles. Biophys J 83:2007–2014. https://doi.org/10.1016/S0006-3495(02)73962-3
Simon SA, McIntosh TJ (1986) Depth of water penetration into lipid bilayers. I Method Enzymol 127:511–521. https://doi.org/10.1016/0076-6879(86)27041-X
Tamba Y, Terashima H, Yamazaki M (2011) A membrane filtering method for the purification of giant unilamellar vesicles. Chem Phys Lipids 164:351–358. https://doi.org/10.1016/j.chemphyslip.2011.04.003
Tanizaki S, Feig M (2005) A generalized Born formalism for heterogeneous dielectric environments: Application to the implicit modeling of biological membranes. J Chem Phys 122:124706. https://doi.org/10.1063/1.1865992
Teissié J, Eynard N, Vernhes MC, Bénichoua A, Ganeva V, Galutzov B, Cabanes PA (2002) Recent biotechnological developments of electropulsation. A prospective review Bioelectrochemistry 55:107–112. https://doi.org/10.1016/s1567-5394(01)00138-4
Yeagle P (1992) The structure of biological membranes. CRC Press, BocaRaton, FL
Acknowledgements
This work was supported partly by the Grants from Ministry of Science and Technology, ICT Division (Ministry of Posts, Telecommunications and Information Technology), Ministry of Education and CASR-BUET of Bangladesh to Mohammad Abu Sayem Karal.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Karal, M.A.S., Ahamed, M.K., Orchi, U.S. et al. An investigation into the critical tension of electroporation in anionic lipid vesicles. Eur Biophys J 50, 99–106 (2021). https://doi.org/10.1007/s00249-020-01477-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00249-020-01477-2