The Mechanism of Erythrocyte Ghost Fusion by Electric Field Pulses

  • Arthur E. Sowers
  • Veena Kapoor

Abstract

The electric field method of fusing membranes is significant for the general study of membrane fusion mechanisms because of the following unique possibilities
  1. i)

    the condition which triggers fusion can be presented and withdrawn within a millisecond or less,

     
  2. ii)

    the effects of membrane-membrane contact can be separated from fusion-inducing stimulus,

     
  3. iii)

    the effects of chemical conditions can be separated from the fusion-inducing stimulus,

     
  4. iv)

    fusion can be induced simultaneously in many membranes,

     
  5. v)

    very high fusion yields are possible,

     
  6. vi)

    there is preliminary evidence that at least two mechanisms may be involved.

     

Keywords

Permeability Migration Sucrose Glycerol Platinum 

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References

  1. Bates, G., Saunders, J., and Sowers, A.E., 1987, Electrofusion: principles and applications, in: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York.Google Scholar
  2. Berg, H., Bauer, E., Berg, D., Forster, W., Hamann, M., Jacob, H.-E., Kurischko, A., Muhlig, P., and Weber, H., 1983, Cell fusion by electric fields, Studia Biophys., 94:93.Google Scholar
  3. Berg, H., 1982, Molecular biological implications of electric-field effects, Studia Biophys., 90:169.Google Scholar
  4. Blangero, C, and Teissie, J., 1985, Ionic modulation of electrically induced fusion of mammalian cells, J. Memb. Biol., 86:247.CrossRefGoogle Scholar
  5. Buschle, R., Ringsdorf, H., and Zimmermann, U., 1982, Electric fieldinduced fusion of large liposomes from natural and polymerizable lipids, FEBS Let., 150:38.CrossRefGoogle Scholar
  6. Chan, L.-N., 1977, Changes in the composition of plasma membrane proteins during differentiation of embryonic chick erythroid cell, Proc. Nat’1. Acad. Sci. USA, 74:1062.CrossRefGoogle Scholar
  7. Chernomordik, L.V., Sukharev, I.G., Abidor, I.G., 1985, Long-living defects in BLM after reversible electrical breakdown, Biologicheskie Membrany, 2:87.Google Scholar
  8. Conrad, M.K., Lo, M.M.S., Tsong, T.Y., and Snyder, S.H., 1987, Bioselective cell-cell fusion for antibody production, in: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York.Google Scholar
  9. Diacumakos, E.G., 1973, Microsurgically fused human somatic cell hybrids: analysis and cloning, Proc. Nat11. Acad. Sci., USA, 69:2959.CrossRefGoogle Scholar
  10. Dimitrov, D.S., and Jain, R.K., 1984, Membrane stability, Biochim. Biophys. Acta, 779:437.Google Scholar
  11. Düzgüneş, N., Hong, K., Baldwin, P. A., Bentz, J., Nir, Shlomo, and Papahadjopoulos, D., 1987, Fusion of phospholipid vesicles induced by divalent cations and protons: modulation by phase transitions, free fatty acids, monovalent cations, and polyamines, in.: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York.Google Scholar
  12. Fricke, H., 1953, The electric permittivity of a dilute suspension of membrane covered ellipsoids, J. Appl. Phys., 24:644.CrossRefGoogle Scholar
  13. Goodby, J.W., 1986, Optical activity and ferroelectricity in liquid crystals, Science, 231:350.PubMedCrossRefGoogle Scholar
  14. Gross, D., Loew, L.M., and Webb, W., 1986, Optical imaging of cell membrane potential changes by applied electric fields, Biophys. J., 50:339.PubMedCrossRefGoogle Scholar
  15. Hofmann, G.A., and Evans, G.A., 1986, Electronic genetic-physical and biological aspects of cellular electromanipulation, IEEE Eng. Med. Biol. Mag., 5:6.PubMedCrossRefGoogle Scholar
  16. Hofmann, G.A., 1988, Physical and Electronic Aspects of Electro Cell Manipulation, in: “Electroporation and Electrofusion in Cell Biology,” E. Neumann, A.E. Sowers, and C. A. Jordan, eds., Plenum Press, New York.Google Scholar
  17. Knight, D.E., and Scrutton, M. C., 1986, Gaining access to the cytosol: The technique and some applications of electropermeabiliziation, Biochem. J., 234:497.PubMedGoogle Scholar
  18. Lieber, M.R., and Steck, T.L., 1982a, A description of the holes in human erythroctye membrane ghosts, J. Biol. Chem., 257:11651.Google Scholar
  19. Lieber, M.R., and Steck, T.L., 1982b, Dynamics of the holes in human erythroctye membrane ghosts, J. Biol. Chem., 257:11660.Google Scholar
  20. Lo, M.M.S., Tsong, T.Y., Conrad, M.K., Strittmatter, S.M., Hester, L.D., and Snyder, S.H., 1984, Monoclonal antibody production by receptor-mediated electrically-induced cell fusion, Nature (London), 310:792.CrossRefGoogle Scholar
  21. Lovinger, A.J., 1983, Ferroelectric polymers, Science, 220:1115.PubMedCrossRefGoogle Scholar
  22. Malmstadt, H.V., Enke, C.G., and Toren, E.C., 1963, “Electronics for scientists,” W. A. Benjamin, New YorkGoogle Scholar
  23. Malmstadt, H.V., Enke, C.G., and Crouch, S.R., 1981, “Electronics and Instrumentation for Scientists,” Benjamin/Cummings, Menlo Park.Google Scholar
  24. Melikyan, G.B., Abidor, I.G., Chernomordik, L.V., and Chailakhyan, L.M., 1983, Electrostimulated fusion and fission of bilayer lipid membranes, Biochim. Biophys. Acta, 730:395.CrossRefGoogle Scholar
  25. Miles, D.M., and Hochmuth, R.M., 1987, Micromanipulation and elastic response of electrically fused red cells, in: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York.Google Scholar
  26. Mischke, S., Saunders, J.A., and Owens, L., 1986, A versatile low-cost apparatus for cell electrofusion and other physiological treatments, J. Biochem. Biophys. Meth., 13:65.PubMedCrossRefGoogle Scholar
  27. Moore, J.H., Davis, C. C., and Coplan, M.A., 1983, “Building Scientific Apparatus,” Addison-Wesley, London.Google Scholar
  28. Neumann, E., 1984, Electric gene transfer into culture cells, Bioelectrochem. Bioenerget., 13:219.CrossRefGoogle Scholar
  29. Neumann, E., Sowers, A.E., and Jordan, C.A., 1988, “Electroporation and Electrofusion in Cell Biology,” Plenum Press, New York.Google Scholar
  30. 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.PubMedGoogle Scholar
  31. Pilwat, G., Richter, H.-P., and Zimmermann, U., 1981, Giant culture cells by electric field-induced fusion, FEBS Let, 133:169.CrossRefGoogle Scholar
  32. Pohl, H.A., 1978, “Dielectrophoresis,” Cambridge Univ. Press, London.Google Scholar
  33. Pohl, H.A., Pollock, K., and Rivera, H., 1984, The electrofusion of cells, Int. J. Quant. Chem: Quant. Biol. Symp., 11:327.CrossRefGoogle Scholar
  34. Porschke, D., 1985, Effects of electric fields on biopolymers, Ann. Rev. Phys. Chem., 36:159.CrossRefGoogle Scholar
  35. Rand, R.P., and Parsegian, V.A., 1986, Mimicry and mechanism in phospholipid models of membrane fusion, Ann. Rev. Physiol., 48:201.CrossRefGoogle Scholar
  36. Rosenberg, B., Van Camp, L., and Krigas, T., 1965, Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode, Nature (London), 205:698.CrossRefGoogle Scholar
  37. Sauer, F.A., 1983, Forces on suspended particles in the electromagnetic field, in: “Coherent Excitations in Biological Systems,” H. Frohlich, and F. Kremer, eds., Springer Verlag, New York.Google Scholar
  38. Schierenberg, E., 1987, Laser-induced cell fusion, in: “Cell Fusion,” A.E. Sowers, Ed., Plenum Press, New York.Google Scholar
  39. Schwister, K., and Deuticke, B., 1985, Formation and properties of aqueous leaks induced in human erythrocytes by electrical breakdown, Biochim. Biophys. Acta, 816:332.PubMedCrossRefGoogle Scholar
  40. Serpersu, E.H., Kinosita Jr., K., and Tsong, T.Y., 1985, Reversible and irreversible modification of erythrocyte membrane permeability by electric field, Biochim. Biophys. Acta, 812:779.PubMedCrossRefGoogle Scholar
  41. Siegel, D.P., 1987, Membrane-membrane interactions via intermediates in lamellar-to-inverted hexagonal phase transitions, in: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York.Google Scholar
  42. Sowers, A.E., 1986a, A long-lived fusogenic state is induced in erythrocyte ghosts by electric pulses, J. Cell Biol., 102:1358.CrossRefGoogle Scholar
  43. Sowers, A.E., 1986b, Long-lived fusogenic membrane sites induced by electric field pulses are not free to diffuse laterally in the plane of the membrane, Biophys. J., 49:132a.Google Scholar
  44. Sowers, A.E., 1985a, Movement of a fluorescent lipid label from a labeled erythrocyte membrane to an unlabeled erythrocyte membrane following electric field-induced fusion, Biophys. J., 47:519.CrossRefGoogle Scholar
  45. Sowers, A.E., 1985b, Electric field-induced membrane fusion in erythrocyte ghosts: evidence that pulses induce a long-lived fusogenic state and that fusion may not involve pore formation. Biophys. J., 47:171a.CrossRefGoogle Scholar
  46. Sowers, A.E., 1984, Characterization of electric field-induced fusion in erythrocyte ghost membranes, J. Cell Biol., 99:1989.PubMedCrossRefGoogle Scholar
  47. Sowers, A.E., 1983a, Fusion of mitochondrial inner membranes by electric fields produces inside out vesicles: visualization by freeze-fracture electron microscopy, Biochim. Biophys. Acta, 735:426.CrossRefGoogle Scholar
  48. Sowers, A.E., 1983b, Red cell and red cell ghost membrane shape changes accompanying the application of electric fields for inducing fusion, J. Cell Biol., 97:179a.Google Scholar
  49. Sowers, A.E., and Hackenbrock, C. R., 1981, Rates of lateral diffusion of intramembrane particles: Measurements by electrophoretic displacement and rerandomization, Proc. Natl. Acad. Sci., USA 78:6246.PubMedCrossRefGoogle Scholar
  50. Sowers, A.E., and Kapoor, V., 1987a, The electrofusion mechanism in erythrocyte ghosts, in: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York..Google Scholar
  51. Sowers, A.E., and Kapoor, V., 1987b, Fusogenic membrane alterations induced by electric field pulses, in: “Mechanistic Approaches to Interactions of Electromagnetc Fields with Living Systems,” M. Blank and E. Findl, eds., Plenum Press, New York.Google Scholar
  52. Sowers, A.E., and Kapoor, V., 1988, The Mechanism of electrically-induced fusion in erythrocyte membranes, in: “Electroporation and Electrofusion in Cell Biology,” E. Neumann, A.E. Sowers, and C. A. Jordan, eds., Plenum Press, New York.Google Scholar
  53. Sowers, A.E., and Lieber, M.L., 1986, Electropores in individual erythrocyte ghosts: diameters, lifetimes, numbers, and locations, FEBS Let., 205:179.CrossRefGoogle Scholar
  54. Stenger, D.A., and Hui, S.W., 1986, Kinetics of ultrastructural changes during electrically induced fusion of human erythrocytes, J. Memb. Biol., 93:43.CrossRefGoogle Scholar
  55. Stenger, D.A., and Hui, S.W., 1988, Electron microscopy of electrofusion, in: “Electroporation and Electrofusion in Cell Biology,” E. Neumann, A.E. Sowers, and C. A. Jordan, eds., Plenum Press, New York.Google Scholar
  56. Stulen, G., 1981, Electric field effects on lipid membrane structure, Biochim. Biophys. Acta, 640:621.PubMedCrossRefGoogle Scholar
  57. Sukharev, S.I., Popov, S.V., Chernomordik, L.V., and Abidor, I.G., 1985, A patch-clamp study of electrical breakdown of cell membranes, Biologicheskie Membrany, 2:77.Google Scholar
  58. Szoka, F. C., 1987, Lipid vesicles: model systems to study membrane-membrane destabilization and fusion, in: “Cell Fusion,” A.E. Sowers, ed., Plenum Press, New York.Google Scholar
  59. Tanaka, T., Nishio, I., Sun, S.-T., and Ueno-Nishio, S., 1982, Collapse of gels in an electric field, Science, 218:467.PubMedCrossRefGoogle Scholar
  60. Tsong, T.Y., 1983, Voltage modulation of membrane permeability and energy utilization in cells, Bioscience Reports, 3:487.PubMedCrossRefGoogle Scholar
  61. Von Hippel, A., 1958, Dielectrics, in: “Handbook of Physics,” E.U. Condon and H. Odishaw, eds., McGraw-Hill, New York.Google Scholar
  62. Zachrisson, A., and Bornman, C. H., 1984, Application of electric field fusion in plant tissue cutlure, Physiol. Plant., 61:314.CrossRefGoogle Scholar
  63. Zimmermann, U., 1982, Electric field-mediated fusion and related electrical phenomena, Biochim. Biophys. Acta, 694:227.PubMedGoogle Scholar
  64. Zimmermann, U., 1986, Electrical breakdown, electropermeabilization and electro fusion, Rev. Physiol. Biochem. Pharmacol., 105:176.PubMedGoogle Scholar
  65. Zimmermann, U., Buchner, K.-H., and Arnold, W.M., 1984, Electrofusion of cells: recent developments and relevance for evolution, in: “Charge and Field Effects in Biosystems,” M.J. Allen and P.N.R. Usherwood, eds., Abacus Press, McComb.Google Scholar
  66. Zimmermann, U., Vienken, J., Halfmann, J., and Emeis, C. C., 1985, Electrofusion: A novel hybridization technique, in: “Advances in Biotechnological Processes,” vol. 4, A. Mizrahi and A.L. van Wezel, eds., Alan R. Liss, New York.Google Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Arthur E. Sowers
    • 1
  • Veena Kapoor
    • 1
  1. 1.Biomedical Research and DevelopmentAmerican Red CrossRockvilleUSA

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