Abstract
The first sign of cell exposure to electrical pulses (strength in Kilovolts per Centimeter and duration in microseconds to milliseconds) is loss of the membrane permeation barrier against ions and small molecules. These permeability changes may be rapidly reversible or irreversible depending on the intensity and the width of the electrical pulses, as well as the composition of the suspending medium. After the rapid increase of the membrane permeability, many delayed effects of the electrical stimulation are observed. These slower secondary effects include membrane fusions, membrane bleb formation, endocytotic reactions, reorganization of the cytoskeletal network, and, in severe cases, lysis of the cells. Global membrane rupture and cell death are mainly due to these secondary effects. Cell death may be prevented by following certain protocols, the most crucial of which is to balance the osmotic pressure of the cytoplasmic fluid and the extracellular medium. Experiments show that electrical stimulation introduces pores of limited sizes in the plasma membrane. These pores can be resealed without losing the cytoplasmic macromolecular contents, and most cells will survive after pore resealing. Electroporation has found many applications in molecular biology, genetic engineering, agricultural research, and biotechnology.
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References
Benz, R., and Zimmermann, U. (1979). Reversible electric breakdown of lipid bilayer membranes: A charge-pulse relaxation study. J. Membrane Biol. 48: 181–204.
Blank, M., and Findl, E. (1987). Mechanistic approaches to interactions of electrical fields with living systems. Plenum Press. New York.
Caffrey, M. (1989). The study of lipid phase transition kinetics by time-resolved x-ray diffraction. Ann. Rev. Biophys. Chem. 18: 159–186.
Chang, D. C., and Reese, T. S. (1990). Changes of membrane structure induced by electroporation as revealed by rapid-freezing electron microscopy. Biophys. J. 58: 1–12.
Chernomordik, L. A., Sokolov, A. V., and Budker, V. G. (1990). Electrostimulated uptake of DNA by liposomes. Biochim. Biophys. Acta. 1024:179–183.
Cole, K. S. (1972). Membrane, ions and impulses. University of California Press, Berkeley.
Coster, H. G. L. and Zimmermann, U. (1975). The mechanism of electrical breakdown in the membranes of Valonia utricularis. J. Membrane Biol. 22: 73–90.
Ehrenberg, B., Farkas, D. L., Fluhler, E. N., Lojewska, Z., and Loew, L. M. (1987). Membrane potential induced by external electrical field pulses can be followed with a potentiometric dye. Biophys. J. 51: 833–837.
El-Mashak, E. M., and Tsong, T. Y. (1985). Ion selectivity of temperature-induced and electric field induced pores in dipalmitoylphosphatidylcholine vesicles. Biochemistry 24: 2884–2888.
Gass, G. V., and Chernomordik, L. V. (1990). Reversible large-scale deformations in the membrane of electrically-treated cells: Electroinduced bleb formation. Biochim. Biophys. Acta 1023: 1–11.
Genz, A., Holzwarth, J. F., and Tsong, T. Y. (1986). The influence of cholesterol on the main phase transition of unilamellar dipalmitoylphosphatidylcholine vesicles. Biophys. J. 50: 1043–1051.
Glaser, R. W., Leikin, S. L., Chernomordik, L. V., Pastushenko, V. F., and Sokirko, A. I., (1988). Reversible electric breakdown of lipid bilayers: Formation and evolution of pores. Biochim. Biophys. Acta 940: 275–287.
Goldman, D. E. (1943). Potential impedance and rectification in membranes. J. Gen Physiol. 27: 37–50.
Gross, D., Loew, L. M. and Webb, W. W. (1986). Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys. J. 50: 339–348.
Gruenewald, B., Frisch, W. and Holzwarth, J. F. (1981). The kinetics of the formation of rotational isomers in the hydrophobic tail region of phospholipid bilayers. Biochim. Biophys. Acta 641: 311–319.
Hibino, M., Shigemori, M., Itoh, H., Nagayama, K., and Kinosita, K. (1991). Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential. Biophys. J. 59: 209–220.
Huang, C.-H., Wheeldon, L., and Thompson, T. E. (1964). The properties of lipid bilayer membranes separating two aqueous phases: Formation of a membrane of simple composition. J. Mol. Biol. 8: 148–160.
Ipsen, J. H., Jorgensen, K., and Mouristen, O. G. (1990). Density fluctuations in saturated phospholipid bilayers increase as the acyl-chain length increases. Biophys. J. 58: 1099–1107.
Jain, M. K., and Wagner, R. C. (1980). Introduction to Biological Membranes. John Wiley and Sons, New York.
Kanehisa, M. I., and Tsong, T. Y. (1978). Cluster model of lipid phase transitions with application to passive permeation of molecules and structure relaxations in lipid bilayers. J. Am. Chem. Soc. 100: 424–432.
Kim, P. S., and Baldwin, R. L. (1990). Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem 159: 631–660.
Kinosita, K., Ashikava, I., Saita, N., Yosimura, H., Itoh, H., Nagayama, K., and Ikegami, A. (1988). Electroporation of cell membranes visualized under pulsed laser fluorescence microscope. Biophys. J. 53: 1015–1019.
Kinosita, K., and Tsong, T. Y. (1977a). Hemolysis of human erythrocytes by a transient electric field. Proc. Natl. Acad. Sci. USA. 74: 1923–1927.
Kinosita, K., and Tsong, T. Y. (1977b). Formation and resealing of pores of controlled sizes in human erythrocyte membrane. Nature 268: 438–441.
Kinosita, K., and Tsong, T. Y. (1977c). Voltage induced pore formation and hemolysis of human erythrocyte membranes. Biochim. Biophys. Acta 471: 227–242.
Kinosita, K., and Tsong, T. Y. (1978), Survival of sucrose-loaded erythrocytes in circulation. Nature 272: 258–260.
Kinosita, K., and Tsong, T. Y. (1979). Voltage-induced conductance in human erythrocyte membranes. Biochim. Biophys. Acta 554: 479–497.
Kuffler, S. W., and Nicholls, J. G. (1976). From Neuron to Brain. Sinauer Associates, Inc., Sunderland, Massachusetts.
Lee, R. C. (1990). Biophysical injury mechanisms in electrical shock victims. Proc. IEEE Eng. Med. Biol. Soc. Philadelphia. 12: 1502–1504.
Liu, D.-S., Astumian, R. D., and Tsong, T. Y. (1990). Activation of Na+ and K+ pumping modes of Na,K-ATPase by an oscillating electric field. J. Biol. Chem. 265: 7260–7267.
Marszalek, P., Liu, D.-S., and Tsong, T. Y. (1990). Schwan equation and transmembrane potential induced by alternating electric field. Biophys. J. 58: 1053–1058.
Mouneimne, Y., Tosi, R.-F., Barhoumi, R., and Nicolau, C. (1990). Electroinsertion of full length recombinant CD4 into red cell membrane. Biochim. Biophys. Acta. 1027: 53–58.
Neumann, E., Schaefer-Ridder, M., Wang, Y., and Hofschneider, P. H. (1982). Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1: 841–845.
Neumann, E., Sowers, A. E., and Jordan, C. A., eds. (1989) Electroporation and electrofusion in cell biology. Plenum Press, New York.
O’Neill, R. J., and Tung, L. (1991). A cell-attached patch clamp study of the electropermeabilization of amphibian cardiac cells. Biophys. J.
Pliquett, V. F. (1968). Das Verhalten von oxytrichiden unter einfluss des elektrischen, felds. Z. Biologie 116: 10–22.
Powell, K. T., Derrik, E. G., and Weaver, J. C. (1986). A quantitative theory of reversible electrical breakdown. Bioelectrochem. Bioenerg. 15: 243–255.
Rols, M.-P. and Teissie, J. (1990). Electropermeabilization of mammalian cells. Quantitative analysis of phenomenon. Biophys. J. 58 1089–1098.
Sale, A. J. H., and Hamilton, W. A. (1968). Effects of high electric fields in microorganisms. III. Lysis of erythrocytes and protoplasts. Biochim. Biophys. Acta. 163: 37–43.
Schwan, H. P. (1983). Biophysics of the interaction of electromagnetic energy with cells and membranes. Pages 213–231. In Biological Effects and Dosimetry of Nonionizing Radiation. Grandolfo, M., Michaelson, S. M., and Rindi, A. eds., Plenum Press, New York.
Serpersu, E. H., Kinosita, K. and Tsong, T. Y. (1985). Reversible and irreversible modification of membrane permeability by electric field. Biochim. Biophys. Acta. 812: 779–785.
Serpersu, E. H., and Tsong, T. Y. (1983). Stimulation of Rb+ pumping activity of Na, K-ATPase in human erythrocytes with an external electric field. J. Membrane Biol. 74: 191–201.
Sowers, A. E. (1986). A long-lived fusogenic state is induced in erythrocyte ghosts by electric pulses. J. Cell Biol. 102: 1358–1362.
Sowers, A. E. (1988). Fusion events and nonfusion content mixing events induced in erythrocyte ghosts by an electric pulse. Biophys. J. 54: 619–626.
Sowers, A. E., and Lieber, M. L. (1986). Electropores in individual erythrocyte ghost: Diameter, lifetimes, numbers, and locations. FEBS Lett. 205: 179–184.
Teissie, J., and Tsong, T. Y. (1980). Evidence of voltage induced channel opening in Na, K-ATPapse of human erythrocyte membranes. J. Membrane Biol. 55: 133–140.
Teissie, J. and Tsong, T. Y. (1981). Electric field-induced transient pores in phospholipid bilayer vesicles. Biochemistry 20: 1548–1554.
Tien, H. T. (1974). Bilayer Lipid Membranes (BLM): Theory and Practice. Marcel Dekker, New York.
Tsien, R. W., Hess, P., McClesky, E. W., and Rosenberg, R. L. (1987). Calcium channels: Mechanisms of selectivity, permeation, and block. Ann. Rev. Biophys. Biophys. Chem. 16: 265–290.
Tsong, T. Y. (1974a). Temperature jump relaxation kinetics of aqueous suspensions of phospholipids and B. subtlis membranes. Federation Proceedings 33: 1342.
Tsong, T. Y. (1974b). Kinetics of the crystalline-liquid phase transition of dimyristoyl L-α-lecithin bilayers. Proc. Natl. Acad. Sci. USA 71: 2684–2688.
Tsong, T. Y. (1983). Voltage modulation of membrane permeability and energy utilization in cells. Bioscience Reports 3: 487–505.
Tsong, T. Y. (1987). Electric modification of membrane permeability for drug loading into living cells. Methods in Enzymol. 149: 248–259.
Tsong, T. Y. (1990a). On electroporation of cell membranes and some related phenomena. Bioelectrochem. Bioenerg. 24: 271–295.
Tsong, T. Y. (1990b). Electrical modulation of membrane proteins: Enforced conformational oscillations and biological energy and signal transductions. Ann. Rev. Biophys. Biophys. Chem. 19: 83–106.
Tsong, T. Y., Greenberg, M., and Kanehisa, M. I. (1977a). Anesthetic action on membrane lipids. Biochemistry 16: 3115–3121.
Tsong, T. Y., and Kanehisa, M. I. (1977b). Relaxation phenomena in aqueous dispersions of synthetic lecithins. Biochemistry 16: 2674–2680.
Tsong, T. Y., and Kingsley, E. (1975). Hemolysis of human erythrocyte induced by a rapid temperature jump. J. Biol. Chem. 250: 786–789.
Wong, T.-K., and Neumann, E. (1982). Electric field mediated gene transfer. Biochem. Biophys. Res. Commun. 107: 584–587.
Xie, T.-D., Sun, L. and Tsong, T. Y. (1990), Study of mechanisms of electric field-induced DNA transfection I. DNA entry by surface binding and diffusion through membrane pores. Biophys. J. 58: 13–19.
Zimmermann, U. (1982). Electric field-mediated fusion and related electrical phenomena. Biochim. Biophys. Acta. 694: 227–277.
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Tsong, T.Y. (1996). Electrically Stimulated Membrane Breakdown. In: Lynch, P.T., Davey, M.R. (eds) Electrical Manipulation of Cells. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-1159-1_2
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DOI: https://doi.org/10.1007/978-1-4613-1159-1_2
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