Cell Fusion pp 367-395 | Cite as


Principles and Applications
  • George W. Bates
  • James A. Saunders
  • Arthur E. Sowers


Electric field-induced cell fusion (electrofusion) is emerging as a promising new tool in cell biology and somatic cell genetics. Compared with other cell-fusion techniques, electrofusion is rapid, simple, and highly efficient. What makes electrofusion truly unique, however, is its unusual physical basis. As a consequence, electrofusion creates some novel experimental opportunities. Although electrofusion has been the subject of several recent reviews (Pohl et al., 1984; Zimmermann et al., 1984a, b), these reviews have focused on the results of just a few laboratories; a wider review of the field may, therefore, be beneficial. This chapter has two components: (1) a discussion of the underlying physical principles of electrical fusion to elucidate the inherent strengths and limitations of the technique, and (2) a broad-based, critical account of progress in applying electrofusion to cell biology and somatic cell genetics. Wherever possible we have stressed the need for quantitative as opposed to qualitative observations and have tried to indicate important areas requiring further research. Our goal is to provide both a theoretical and a practical basis from which workers interested in pursuing this technique, or those with a general interest in cell and membrane fusion, can compare electrofusion with other fusion methods.


Alternate Current Somatic Hybrid Cell Fusion Fusion Product Plant Protoplast 


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  1. Abidor, I. G., Arakelyan, V. G., Chernomordik, L. V., Chizmadzhev, Yu. A., Pastushenko, V. F., and Tarasevich, M. R., 1979, Electric breakdown of bilayer lipid membranes, Bioelectrochem. Bioenerg. 6:37–52.CrossRefGoogle Scholar
  2. Adams, R. J., 1982, Organelle movement in axons depends on ATP, Nature (Lond.) 297:327–329.CrossRefGoogle Scholar
  3. Asano, A., and Asano, K., 1982, Mechanism of HVJ-induced cell fusion, in: Structure, Dynamics, and Biogenesis of Biomembranes (R. Sato and S. Ohinishi, eds.), pp. 57–77, Japan Scientific Societies Press, Tokyo, and Plenum Press, New York.CrossRefGoogle Scholar
  4. Baker, P. F., and Knight, D. E., 1978, Calcium dependent exocytosis in bovine adrenal medullary cells with leaky plasma membranes, Nature (Lond.) 276:620–622.CrossRefGoogle Scholar
  5. Bates, G. W., 1985, Electrical fusion for the optimal formation of protoplast heterokaryons in Nicotiana, Planta 165:217–224.CrossRefGoogle Scholar
  6. Bates, G. W., and Hasenkampf, C. A., 1985, Culture of plant somatic hybrids following electrical fusion, Theor. Appl. Genet. 70:227–233.CrossRefGoogle Scholar
  7. Bates, G. W., Gaynor, J. J., and Shekhawat, N. S., 1983, The fusion of plant protoplasts by electric fields, Plant Physiol. 72:1110–1113.PubMedCrossRefGoogle Scholar
  8. Benz, R., and Zimmermann, U., 1981, High electric field effects on the cell membranes of Halicystis parvula. A charge pulse study., Planta 152:314–318.CrossRefGoogle Scholar
  9. Benz, R., Beckers, F., and Zimmermann, U., 1979, Reversible electrical breakdown of lipid bilayer membranes: A charge-pulse relaxation study, J. Membrane Biol. 48:181–204.CrossRefGoogle Scholar
  10. Berg, H., 1982, Biological implications of electric field effects. Part V. Fusion of blastomeres and blastocysts of mouse embryos, Bioelectrochem. Bioenerg. 9:223–228.CrossRefGoogle Scholar
  11. Berg, H., Augsten, K., Bauer, E., Forster, W., Jacob, H. E., Muhlig, P., and Weber, H., 1984, Possibilities of cell fusion and transformation by electrostimulation, Bioelectrochem. Bioenerget. 12:119–133.CrossRefGoogle Scholar
  12. Bischoff, R., Eisert, R. M., Schedel, I., Vienken, J., and Zimmermann, U., 1982, Human hy-bridoma cells produced by electro-fusion, FEBS Lett. 147:64–68.PubMedCrossRefGoogle Scholar
  13. Blangero, C., and Teissie, J., 1983, Homokaryon production by electro fusion: A convenient way to produce a large number of viable mammalian fused cells, Biochem. Biophys. Res. Commun. 114:663–669.CrossRefGoogle Scholar
  14. Blangero, C., and Teissie, J., 1985, Ionic modulation of electrically induced fusion of mammalian cells, J. Membrane Biol. 86:247–253.CrossRefGoogle Scholar
  15. Büschl, R., Ringsdorf, H., and Zimmermann, U., 1982, Electric field-induced fusion of large liposomes from natural and polymerizable lipids, FEBS Lett. 150:38–42.CrossRefGoogle Scholar
  16. Chandler, D. E., Heuser, J. E., 1980, Arrest of membrane fusion events in mast cells by quickfreezing, J. Cell Biol 86:666–674.PubMedCrossRefGoogle Scholar
  17. Chapel, M., Teissie, J., and Alibert, G., 1984, Electrofusion of spermine-treated plant protoplasts, FEBS Lett. 173:331–336.CrossRefGoogle Scholar
  18. Cole, K. S., 1968, Membranes, Ions and Impulses. A Chapter of Classical Biophysics, University of California Press, Berkeley.Google Scholar
  19. Coster, H. G. L., and Zimmermann, U., 1975, Dielectric breakdown in the membranes of Valonia utricularis, Biochim. Biophys. Acta 382:410–418.PubMedCrossRefGoogle Scholar
  20. Crowley, J. M., 1973, Electrical breakdown of bimolecular lipid membranes as an electromechanical instability, Biophys. J. 13:711–724.PubMedCrossRefGoogle Scholar
  21. de Kruijff, B., Cullis, P. R., Verkleij, A. J., Hope, M. J., van Echteld, C. J. A., and Taraschi, T. F., 1985, Lipid polymorphism and membrane function, in: The Enzymes of Biological Membranes, Vol. 1: Membrane Structure and Dynamics (A. N. Martonosi, ed.), pp. 131–204, Plenum Press, New York.CrossRefGoogle Scholar
  22. Dimitrov, D. S., and Jain, R. K., 1984, Membrane stability, Biochim. Biophys. Acta 779:437–468.PubMedCrossRefGoogle Scholar
  23. Finaz, C., Lefevre, A., and Teissie, J., 1984, A new, highly efficient technique for generating somatic cell hybrids, Exp. Cell Res. 150:477–482.PubMedCrossRefGoogle Scholar
  24. Gauger, B., and Bentrup, F. W., 1979, A study of dielectric membrane breakdown in the Fucus egg, J. Membrane Biol. 48:249–264.CrossRefGoogle Scholar
  25. Gingell, D., and Ginsberg, L., 1978, Problems in the physical interpretation of membrane interaction and fusion, in: Membrane Fusion (G. Poste and G. L. Nicolson, eds.), pp. 792–833, North-Holland, Amsterdam.Google Scholar
  26. Gleba, Y. Y, and Sytnik, K M., 1984, Protoplast Fusion. Genetic Engineering in Higher Plants, in: Monographs on Theoretical and Applied Genetics, Vol. 8 (R. Frankel, ed.), Springer-Verlag, Berlin.Google Scholar
  27. Halfmann, H. J., Rocken, W., Emeis, C. C., and Zimmermann, U., 1982, Transfer of mitochondrial function into a cytoplasmic respiratory-deficient mutant of Saccharomyces yeast by electro-fusion, Curr. Genet. 6:25–28.CrossRefGoogle Scholar
  28. Halfmann, H. J., Emeis, C. C., and Zimmermann, U., 1983, Electro-fusion of haploid Saccharomyces yeast cells of identical mating type, Arch. Microbiol. 134:1–4.CrossRefGoogle Scholar
  29. Hui, S. W., Isac, T., Boni, L. T., and Sen, A., 1985, Action of polyethylene glycol on the fusion of human erythrocyte membranes, J. Membrane Biol. 84:137–146.CrossRefGoogle Scholar
  30. Jacob, H. E., Siegemund, F., and Bauer, E., 1984, Fusion von pflanzlichen Protoplasten durch elektrischen Feldimpuls nach Dielectrophorese, Biol. Zentralbl. 103:77–82.Google Scholar
  31. Kao, K. N., 1981, Plant protoplast fusion and somatic hybrids, in: Plant Tissue Culture (H. Han, ed.), pp. 331–339, The Pitman International Series in Applied Biology, Proceedings of Beijing Symposium, London.Google Scholar
  32. Kao, K. N., and Michayluk, M. R., 1974, A method for high frequency of intergeneric fusion of plant protoplasts, Planta 115:355–367.CrossRefGoogle Scholar
  33. Karsten, U., Papsdorf, G., Roloff, G., Stolley, P., Abel, H., Walther, I., and Weiss, H., 1985, Monoclonal anti-cytokeratin antibody from a hybridoma clone generated by electrofusion, Eur. J. Cancer Clin. Oncol. 21:733–740.PubMedCrossRefGoogle Scholar
  34. Kartha, K. K., Gamborg, O. L., Constabel, F., and Kao, K. N., 1974, Fusion of rapeseed and soybean protoplasts and subsequent division of heterokaryocytes, Can. J. Bot. 52:2435–2436.CrossRefGoogle Scholar
  35. Kinosita, K., and Tsong, T.Y., 1977a Hemolysis of human erythrocytes by a transient electric field, Proc. Natl. Acad. Sci. U.S.A. 74:1923–1927.PubMedCrossRefGoogle Scholar
  36. Kinosita, K., and Tsong, T.Y., 1977b, Formation and resealing of pores of controlled sizes in human erythrocyte membrane, Nature (Lond.) 268:438–441.CrossRefGoogle Scholar
  37. Kinosita, K., and Tsong, T. Y, 1979, Voltage-induced conductance in human erythrocyte membranes, Biochim. Biophys. Acta 554:479–497.PubMedCrossRefGoogle Scholar
  38. Kohn, H., Schieder, R., and Schieder, O., 1985, Somatic hybrids in tobacco mediated by electrofusion, Plant Sci. 38:121–128.CrossRefGoogle Scholar
  39. Koop, H. U., Dirk, J., Wolff, D., and Scheiger, H. G., 1983, Somatic hybridization of two selected single cells, Cell Biol. Int. Rep. 7:1123–1128.PubMedCrossRefGoogle Scholar
  40. Lo, M. M. S., Tsong, T. Y, Conrad, M. D., Strittmatter, S. M., Hester, L. D., and Snyder, S. H., 1984, Monoclonal antibody production by receptor-mediated electrically induced cell fusion, Nature (Lond.) 310:792–794.CrossRefGoogle Scholar
  41. Lucy, J. A., 1984, Fusogenic mechanisms, in: Cell Fusion, Ciba Foundation Symposium 103 (J. Evered and J. Whelan, eds.), pp. 28–39, Pitman, London.Google Scholar
  42. McCloskey, M. A., Liu, Z. y, and Poo, M. M., 1984, Lateral electromigration and diffusion of Fce receptors on rat basophilic leukemia cells: Effects of IgE binding, J. Cell Biol. 99:778–787.PubMedCrossRefGoogle Scholar
  43. Mehrle, W., Zimmermann, U., and Hampp, R., 1985, Evidence for asymmetrical uptake of fluorescent dyes through electro-permeabilized membranes of Avena mesophyll protoplasts, FEBS Lett. 185:89–94.CrossRefGoogle Scholar
  44. Melikyan, G. B., Abidor, I. G., Chernomordik, L. V., and Chailakhyan, L. M., 1983, Electro-stimulated fusion and fission of bilayer lipid membranes, Biochim. Biophys. Acta 730:395.CrossRefGoogle Scholar
  45. Mishra, K. P., Binh, L. D., and Singh, B. B., 1981, Effect of dielectric discharge on drug treated mammalian cells, Ind. J. Exp. Biol 19:520–523.Google Scholar
  46. Neumann, E., and Katchalsky, A., 1972, Long-lived conformation changes induced by electric impulses in biopolymers, Proc. Natl. Sci. U.S.A. 69:993–997.CrossRefGoogle Scholar
  47. Neumann, E., Gerisch, G., and Opatz, K., 1980, Cell fusion induced by high electric impulses applied to Dictyostelium, Naturwissenschaften 67:414–415.CrossRefGoogle Scholar
  48. Neumann, E., Schaefer-Ridder, M., Wang, Y, and Hofschneider, P. H., 1982, Gene transfer into mouse lymphoma cells by electroporation in high electric fields, EMBO J. 1:841–845.PubMedGoogle Scholar
  49. Ohno-Shosaku, T., and Okada, Y, 1984, Facilitation of electrofusion of mouse lymphoma cells by the proteolytic action of proteases, Biochem. Biophys. Res. Commun. 120:138–143.PubMedCrossRefGoogle Scholar
  50. Pethig, R., 1979, Dielectric and Electronic Properties of Biological Materials, Wiley, New York.Google Scholar
  51. Pilwat, G., Zimmermann, U., and Riemann, F., 1975, Dielectric breakdown measurements of human and bovine erythrocyte membranes using benzyl alcohol as a probe molecule, Biochim. Biophys. Acta 406:424–432.PubMedCrossRefGoogle Scholar
  52. Pliquett, F., and Wunderlich, S., 1980, Relationship between cell parameters and pulse deformation due to these cells as well as its change after electrically induced membrane breakdown, Bioelectrochem. Bioenerg. 10:467–475.CrossRefGoogle Scholar
  53. Podesta, E. J., Solano, A. R., Molina, Y, Vedia, L., Paladini, A., Sanchez, M. L., and Torres, H. N., 1984, Production of steroid hormone and cyclic AMP in hybrids of adrenal and Leydig cells generated by electrofusion, Eur. J. Biochem. 145:329–332.PubMedCrossRefGoogle Scholar
  54. Pohl, H. A., 1978, Dielectrophoresis, Cambridge University Press, London.Google Scholar
  55. Pohl, H. A., and Crane, J. S., 1971, Dielectrophoresis of cells, Biophys. J. 11:711–728.PubMedCrossRefGoogle Scholar
  56. Pohl, H. A., Pollock, K., and Rivera, H., 1984, The electrofusion of cells, Int. J. Quant. Chem. Quant. Biol. Symp. 11:327–345.CrossRefGoogle Scholar
  57. Poo, M., 1981, Insitu electrophoresis of membrane components, Annu. Rev. Biophys. Bioeng. 10:245–276.PubMedCrossRefGoogle Scholar
  58. Poste, G., and Pasternak, C. A., 1978, Virus-induced cell fusion, in: Membrane Fusion (G. Poste and G. L. Nicolson, eds.), pp. 306–367, North-Holland, Amsterdam.Google Scholar
  59. Potter, H., Weir, L., and Leder, P., 1984, Enhancer-dependent expression of human k immunoglobulin genes introduced into mouse pre-B lymphocytes by electroporation, Proc. Natl Acad. Sci. U.S.A.81:7161–7165.PubMedCrossRefGoogle Scholar
  60. Richter, H. P., Scheurich, P., and Zimmermann, U., 1981, Electric field-induced fusion of sea urchin eggs, Dev. Growth Diff.23:479–486.CrossRefGoogle Scholar
  61. Riemann, F., Zimmermann, U., and Pilwat, G., 1975, Release and uptake of haemoglobin and ions in red blood cells induced by dielectric breakdown, Biochim. Biophys. Acta 394:449–462.PubMedCrossRefGoogle Scholar
  62. Ruthe, H. J., and Adler, J., 1985, Fusion of bacterial spheroplasts by electric fields, Biochim. Biophys. Acta 819:105–113.PubMedCrossRefGoogle Scholar
  63. Sale, A. J. H., and Hamilton, W. A., 1968, Effects of high electric fields on micro-organisms. III. Lysis of erythrocytes and protoplasts, Biochim. Biophys. Acta 163:37–43.PubMedCrossRefGoogle Scholar
  64. Salhani, N., Vienken, J., Zimmermann, U., Ward, M., Davey, M. R., Clothier, R. H., Balls, M., Cocking, E. C., and Lucy, J. A., 1985, Haemoglobin synthesis and cell wall regeneration by electric field-induced interkingdom heterokaryons, Protoplasma 126:30–35.CrossRefGoogle Scholar
  65. Sauer, F. A., 1983, Forces on suspended particles in the electromagnetic field, in: Coherent Excitations in Biological Systems (H. Fröhlich and F. Kremer, eds.), pp. 134–144, Springer-Verlag, Berlin.CrossRefGoogle Scholar
  66. Saunders, J. A., Roskos, L. A., Mischke, S., Aly, M., and Owens, L. D., 1986, Behavior and viability of tobacco protoplasts in response to electrofusion parameters, Plant Physiol.80:117–121.PubMedCrossRefGoogle Scholar
  67. Scheurich, P., and Zimmermann, U., 1980, Membrane fusion and deformation of red blood cells by electric fields, Z. Naturforsch.35c:1081–1085.Google Scholar
  68. Scheurich, P., and Zimmermann, U., 1981a, Electrically stimulated fusion of different plant cell protoplasts, Plant Physiol. 67:849–853.PubMedCrossRefGoogle Scholar
  69. Scheurich, P., and Zimmermann, U., 1981b, Giant human erythrocytes by electric-field-induced cell-to-cell fusion, Naturwissenschaften 68:45–47.PubMedCrossRefGoogle Scholar
  70. Schwister, K., and Deuticke, B., 1985, Formation and properties of aqueous leaks induced in human erythrocytes by electrical breakdown, Biochim. Biophys. Acta 816:332–348.PubMedCrossRefGoogle Scholar
  71. Senda, M., Takeda, J., Abe, S., and Nakamura, T., 1979, Induction of cell fusion of plant protoplasts by electrical stimulation, Plant Cell Physiol.20:1441–1443.Google Scholar
  72. Serpersu, E. H., Kinosita, K., and Tsong, T. y, 1985, Reversible and irreversible modification of erythrocyte membrane permeability by electric field, Biochim. Biophys. Acta 812:779–785.PubMedCrossRefGoogle Scholar
  73. Shimmen, T., and Tazawa, M., 1983, Permeabilization of Nitella internodal cell with electrical pulses, Protoplasma 117:93–96.CrossRefGoogle Scholar
  74. Shivarova, N., and Grigorova, R., 1983, Microbiological implications of electric field effects. Part VIII. Fusion of Bacillus thuringiensis protoplasts by high electric field phase, Bioelectrochem. Bioenerget. 11:181–185.CrossRefGoogle Scholar
  75. Shivarova, N., Forster, W., Jacob, H. E., and Grigorova, R., 1983, Microbiological implications of electric field effects. VII. Stimulation of plasmid transformation of Bacillus cereus protoplasts by electric field pulses, Allg. Mikrobiol.23:595–599.CrossRefGoogle Scholar
  76. Sowers, A. E., 1983, Fusion of mitochondrial inner membranes by electric fields produces inside-out vesicles. Visualization by freeze-fracture electron microscopy, Biochem. Biophys. Acta 735:426–428.PubMedCrossRefGoogle Scholar
  77. Sowers, A. E., 1984, Characterization of electric field-induced fusion in erythrocyte ghost membranes, J. Cell Biol.99:1989–1996.PubMedCrossRefGoogle Scholar
  78. Sowers, A. E., 1985, Movement of a fluorescent lipid label from a labeled erythrocyte membrane to an unlabeled erythrocyte membrane following electric-field-induced fusion, Biophys. J. 47:519–525.PubMedCrossRefGoogle Scholar
  79. Sowers, A E., 1986, A long-lived fusogenic state is induced in erythrocyte ghosts by electric pulses, J. Cell Biol. 102:1358–1362.PubMedCrossRefGoogle Scholar
  80. Steinbiss, H. H., 1978, Dielektrischer Durchbruch des Plasmalemmas von Valerianella locusta-Protoplasten, Z. Pflanzenphysiol. 88:95–102.Google Scholar
  81. Takashima, S., and Schwan, H. P., 1985, Alignment of microscopic particles in electric fields and its biological implications, Biophys. J. 47:513–518.PubMedCrossRefGoogle Scholar
  82. Teissie, J., and Blangero, C., 1984, Direct experimental evidence of the vectorial character of the interaction between electric pulses and cells in cell electrofusion, Biochim. Biophys. Acta 775:446–448.PubMedCrossRefGoogle Scholar
  83. Teissie, J., and Tsong, T. y, 1981, Electric field induced transient pores in phospholipid bilayer vesicles, Biochemistry 20:1548–1554.PubMedCrossRefGoogle Scholar
  84. Teissie, J., Knutson, V. P., Tsong, T. y, and Lane, M. D., 1982, Electric pulse-induced fusion of 3T3 cells in monolayer culture, Science 216:537–538.PubMedCrossRefGoogle Scholar
  85. Teixeira-Pinto, A. A., Nejelski, L. L., Jr., Cutler, J. L., and Heller, J. H., 1960, The behavior of unicellular organisms in an electromagnetic field, Exp. Cell Res. 20:548–564.CrossRefGoogle Scholar
  86. Tempelaar, M. J., and Jones, M. G. K., 1985a, Directed electrofusion between protoplasts with different responses in a mass fusion system, Plant Cell Rep. 4:92–95.CrossRefGoogle Scholar
  87. Tempelaar, M. J., and Jones, M. G. K., 1985b, Fusion characteristics of plant protoplasts in electric fields, Planta 165:205–216.CrossRefGoogle Scholar
  88. Tsong, T. Y, 1983, Voltage modulation of membrane permeability and energy utilization in cells, Biosci. Rep.3:487–505.PubMedCrossRefGoogle Scholar
  89. Verhoek-Köhler, B., Hampp, R., Ziegler, H., and Zimmermann, U., 1983, Electro-fusion of mesophyll protoplasts of Avena sativa, Planta 158:199–204.CrossRefGoogle Scholar
  90. Vienken, J., and Zimmermann, U., 1982, Electric field-induced fusion: electro-hydraulic procedure for production of heterokaryon cells in high yield, FEBS Lett. 137:11–13.PubMedCrossRefGoogle Scholar
  91. Vienken, J., Ganser, R., Hampp, R., and Zimmermann, U., 1981, Electric field-induced fusion of isolated vacuoles and protoplasts of different developmental and metabolic provenience, Physiol. Plant 53:64–70.CrossRefGoogle Scholar
  92. Vienken, J., Zimmermann, U., Fouchard, M., and Zagury, D., 1983a, Electrofusion of myeloma cells on the single cell level; fusion under sterile conditions without proteolytic enzyme treatment, FEBS Lett. 163:54–56.PubMedCrossRefGoogle Scholar
  93. Vienken, J., Zimmermann, U., Ganser, R., and Hampp, R., 1983b, Vesicle formation during electro-fusion of mesophyll protoplasts of Kalanchoe diagremontiana, Planta 157:331–335.CrossRefGoogle Scholar
  94. Watts, J. W., and King, J. M., 1984, A simple method for large-scale electrofusion and culture of plant protoplasts, Biosci. Rep.4:335–342.PubMedCrossRefGoogle Scholar
  95. Weber, H., Forster, W., Berg, H., and Jacob, H. E., 1981a, Parasexual hybridization of yeasts by electric field stimulated fusion of protoplasts, Curr. Genet. 4:165–166.CrossRefGoogle Scholar
  96. Weber, H., Forster, W., Jacob, H. E., and Berg, H., 1981b, Microbiological implications of electric field effects. III. Stimulation of yeast protoplast fusion by electric field pulses, Allg. Mikrobiol. 21:555–562.CrossRefGoogle Scholar
  97. White, S. H., 1980, How electric fields modify alkane solubility in lipid bilayers, Science 207:1075–1077.PubMedCrossRefGoogle Scholar
  98. White, S. H., and Chang, W., 1981, Voltage dependence of the capacitance and area of black lipid membranes, Biophys. J. 36:449–453.PubMedCrossRefGoogle Scholar
  99. Wong, T. K., and Neumann, E., 1982, Electric field mediated gene transfer, Biochem. Biophys. Res. Commun.107:584–587.PubMedCrossRefGoogle Scholar
  100. Zachrisson, A., and Bornman, C. H., 1984, Application of electric field fusion in plant tissue culture, Physiol. Plant 61:314–320.CrossRefGoogle Scholar
  101. Zimmermann, U., 1982, Electric field-mediated fusion and related electrical phenomena, Biochem. Biophys. Acta 694:227–277.PubMedCrossRefGoogle Scholar
  102. Zimmermann, U., and Benz, R., 1980, Dependence of electrical breakdown voltage on the charging time in Valonia utricularis, J. Membrane Biol.53:33–43.CrossRefGoogle Scholar
  103. Zimmermann, U., and Scheurich, P., 1981, High frequency fusion of plant protoplasts by electric fields, Planta 151:26–32.CrossRefGoogle Scholar
  104. Zimmermann, U., and Vienken, J., 1982, Electric field-induced cell-to-cell fusion, J. Membrane Biol.67:165–182.CrossRefGoogle Scholar
  105. Zimmermann, U., Pilwat, G., Beckers, F., and Riemann, F., 1976, Effects of external electrical fields on cell membranes, Bioelectrochem. Bioenerget.3:58–83.CrossRefGoogle Scholar
  106. Zimmermann, U., Beckers, F., and Coster, H. G. L., 1977, The effect of pressure on the electrical breakdown in the membranes of Valonia utricularis, Biochim. Biophys. Acta 464:399–416.CrossRefGoogle Scholar
  107. Zimmermann, U., Vienken, J., and Pilwat, G., 1980, Development of drug carrier systems: Electrical field induced effects in cell membranes, Bioelectrochem. Bioenerget 7:553–574.CrossRefGoogle Scholar
  108. Zimmermann, U., Pilwat, G., and Richter, H. P., 1981a, Electric-field-stimulated fusion: Increased field stability of cells induced by pronase, Naturwissenschaften 68:577–579.PubMedCrossRefGoogle Scholar
  109. Zimmermann, U., Vienken, J., and Pilwat, G., 1981b, Rotation of cells in an alternating electric field: The occurrence of a resonance frequency, Z. Naturforsch. 36c: 173–177.Google Scholar
  110. Zimmermann, U., Buchner, K. H., and Arnold, W. M., 1984a, 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.), pp. 293–318, Abacus Press, Normal, Ill.Google Scholar
  111. Zimmermann, U., Vienken, J., Pilwat, G., and Arnold, W. M., 1984b, Electrofusion of cells: principles and potential for the future, in: Cell Fusion, CIBA Foundation Symposium 103, pp. 60–73, Pitman, London.Google Scholar

Copyright information

© Springer Science+Business Media New York 1987

Authors and Affiliations

  • George W. Bates
    • 1
  • James A. Saunders
    • 2
  • Arthur E. Sowers
    • 3
  1. 1.Department of Biological Science and Institute of Molecular BiophysicsFlorida State UniversityTallahaseeUSA
  2. 2.Germplasm Quality and Enhancement LaboratoryUSDA Plant Genetics and Germplasm InstituteBeltsvilleUSA
  3. 3.Jerome H. Holland Laboratory for the Biomedical SciencesAmerican National Red CrossRockvilleUSA

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