Summary
The ionic permeability of the nonjunctional and newly formed junctional membranes was investigated in embryos ofXenopus laevis up to the onset of the fifth cleavage. Continuous measurements were made of the equivalent nonjunctional (R ′0 ) and junctional resistances (R ′ i ) in different pairs of adjacent cells separated by one of the four cleavage membranes formed in that period. The specific, resistance of the nonjunctional membranes (r 0) and of each cleavage membrane (r i ) as a function of time were derived using a generally applicable computer simulation model.r 0 decreased from about 40 kΩ cm2 in the uncleaved egg to about 10 kΩ cm2 at the 16-cell stage, due to the insertion of a small fraction of the relatively permeable newly formed cleavage membranes into the outer surface. Superimposed on this overall decline, a transient decrease ofr 0 was observed during each cycle, caused by a temporary partial separation of the peripheral parts of adjacent blastomeres. The changes inR ′0 followed the same pattern.R ′ i increased stepwise during each cleavage cycle. At the onset of each cleavage there were no significant differences inR ′ i as measured between different pairs of cells. After an initial phase of membrane formationr i of all cleavage membranes remained constant at about 400 Ω cm2. In the stages investigated the coupling ratio ranged from 0.8 to 1. It is argued that this close coupling could be the result of the highly impermeable outer surface even in the absence of specialized junctions in the intercellular membranes.
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Ashman, R. F., Kanno, Y., Loewenstein, W. R. 1964. The intercellular electrical coupling at a forming membrane junction in a dividing cell.Science 145:604
Azarnia, R., Larsen, W. J., Loewenstein, W. R. 1974. The membrane junctions in communicating and noncommunicating cells, their hybrids, and segregants.Proc. Nat. Acad. Sci. USA 71:880
Bennett, M. V. L. 1966. Physiology of electrotonic junctions.Ann. N. Y. Acad. Sci. 137:509
Bennett, M. V. L., 1973. Function of electrotonic junctions in embryonic and adult tissues.Fed. Proc. 32:65
Bennett, M. V. L., Spira, M. E., Pappas, G. D. 1972. Properties of electrotonic junctions between embryonic cells ofFundulus.Dev. Biol. 29:419
Bennett, M. V. L., Trinkaus, J. P. 1970. Electrical coupling between embryonic cells by way of extracellular space and specialized junctions.J. Cell Biol. 44:592
Bluemink, J. G. 1971. Effects of cytochalasin B on surface contractility and cell junction formation during egg cleavage inXenopus laevis.Cytobiologie 3:176
Bluemink, J. G., de Laat, S. W. 1973. New membrane formation during cytokinesis in normal and cytochalasin B-treated eggs ofXenopus laevis. I. Electron-microscopical observations.J. Cell Biol. 59:89
Decker, R. S., Friend, D. S. 1974. Assembly of gap junctions during neurulation.J. Cell Biol. 62:32
DiCaprio, R. A., French, A. S., Sanders, E. J. 1974. Dynamic properties of electrotonic coupling between cells of earlyXenopus embryos.Biophys. J. 14:387
Furshpan, E. J., Potter, D. D. 1968. Low resistance junctions between cells in embryos and tissue culture.In: Current Topics in Developmental Biology. A. A. Moscona and A. Monroy, editors. Vol. 3, p. 95. Academic Press Inc., New York
Gilula, N. B., Reeves, O. r., Steinbach, A. 1972. Metabolic coupling, ionic coupling and cell contacts.Nature 235:262
Hulser, D. F., Demsey, A. 1973. Gap and low-resistance junctions between cells in culture.Z. Naturforsch. 28:603
Ito, S., Hori, N. 1966. Electrical characteristics ofTriturus egg cells during cleavage.J. Gen. Physiol. 49:1019
Ito, S., Loewenstein, W. R. 1969. Ionic communication between early embryonic cells.Dev. Biol. 19:228
Ito, S., Sato, E., Loewenstein, W. R. 1974. Studies on the formation of a permeable cell membrane junction. I. Coupling under various conditions of membrane contact. Effects of colchicine, cytochalasin B, dinitrophenol.J. Membrane Biol. 19:305
Ito, S., Sato, E., Loewenstein, W. R. 1974. Studies on the formation of a permeable cell membrane junction. II. Evolving junctional conductance and junctional insulation.J. Membrane Biol. 19:339
Johnson, R. G., Sheridan, J. D. 1971. Junctions between cancer cells in culture: Ultrastructure and permeability.Science 174:717
de Laat, S. W., Barts, P. W. J. A. 1976. New membrane formation and intercellular communication in the earlyXenopus embryo. II. Theoretical analysis.J. Membrane Biol. 27:131
de Laat, S. W., Bluemink, J. G. 1974. New membrane formation during cytokinesis in normal and cytochalasin B-treated eggs ofXenopus laevis. II. Electrophysiological observations.J. Cell Biol. 60:529
de Laat, S. W., Buwalda, R. J. A., Habets, A. M. M. C. 1974. Intracellular ionic distribution, cell membrane permeability and membrane potential of theXenopus egg during first cleavage.Exp. Cell Res. 89:1
de Laat, S. W., Luchtel, D., Bluemink, J. G. 1973. The action of cytochalasin B during egg cleavage inXenopus laevis: Dependence on cell membrane permeability.Dev. Biol. 31:163
de Laat, S. W., Wouters, W., Marques da Silva Pimenta Guarda, M. M., da Silva Guarda, M. A. 1975. Intracellular ionic compartmentation, electrical membrane properties, and cell membrane permeability before and during the first cleavage in theAmbystoma egg.Exp. Cell Res. 91:15
Loewenstein, W. R. 1966. Permeability of membrane junctions.Ann. N. Y. Acad. Sci. 137:441
Loewenstein, W. R. 1968. Communication through cell junctions, implications in growth control and differentiation.Dev. Biol. 19, Suppl.2:151
Loewenstein, W. R. 1968. Some reflections on growth and differentiation.Perspect. Biol. Med. 11:260
Loewenstein, W. R., Kanno, Y. 1964. Studies on an epithelial (gland) cell junction. I. Modification of surface membrane permeability.J. Cell Biol. 22:565
McDonald, T. F., Sachs, H. G., Orr, C. W., Ebert, J. D. 1972. External potassium and baby hamster kidney cells: Intracellular ions, ATP, growth, DNA synthesis and membrane potentialDev. Biol. 28:290
Nieuwkoop, P. D., Faber, J. 1956. Normal Table ofXenopus laevis (Daudin). North-Holland Publishing Company, Amsterdam
Palmer, J. F., Slack, C. 1970. Some bio-electric parameters of earlyXenopus embryos.J. Gen. Physiol. 24:535
Payton, B. W., Bennett, M. V. L., Pappas, G. D. 1969. Permeability and structure of junctional membranes at an electrotonic synapse.Science 166:1641
Potter, D. D., Furshpan, E. J., Lennox, E. S. 1966. Connections between cells of the developing squid as revealed by electrophysiological methods.Proc. Nat. Acad. Sci. USA 55:328
Reese, T. S., Bennett, M. V. L., Feder, N. 1971. Cell-to-cell movement of peroxidases injected into the septate axon of crayfish.Anat. Rec. 169:409
Revel, J. P., Yee, A. G., Hudspeth, A. J. 1971. Gap junctions between electrotonically coupled cells in tissue culture and in brown fat.Proc. Nat. Acad. Sci. USA 68:2924
Rose, B. 1971. Intercellular communication and some structural aspects of membrane junctions in a simple cell system.J. Membrane Biol. 5:1
Sanders, E. J., Zalik, S. E. 1972. The blastomere periphery ofXenopus laevis, with special reference to intercellular relationships.Wilhelm Roux' Archiv 171:181
Satir, P., Gilula, N. B. 1973. The fine structure of membranes and intercellular communication in insects.,Annu. Rev. Entomol. 18:143
Sheridan, J. D. 1968. Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo.J. Cell Biol. 37:650
Sheridan, J. D. 1971. Dye movement and low-resistance junctions between reaggregated embryonic cells.Dev. Biol. 26:627
Singal, P. K., Sanders, E. J. 1974. An ultrastructural study of the first cleavage ofXenopus embryos.J. Ultrastruct. Res. 47:433
Slack, C., Palmer, J. F. 1969. The permeability of intercellular junctions in the early embryo ofXenopus laevis, studied with a fluorescent tracer.Exp. Cell Res. 55:416
Takahashi, M., Ito, S. 1968. Electrophysiological studies on membrane formation during cleavage of the amphibian egg.Zool. Mag. 77:307
Tupper, J. T., Saunders, J. W., Jr. 1972. Intercellular permeability in the earlyAsterias embryo.Dev. Biol. 27:546
Tupper, J. T., Saunders, J. W., Jr., Edwards, C. 1970. The onset of electrical communication between cells in the developing starfish embryo.J. Cell Biol. 46:187
Wiener, J., Spiro, D., Loewenstein, W. R. 1964. Studies on an epithelial (gland) cell junction. II. Surface structure.J. Cell Biol. 22:587
Woodward, D. J. 1968. Electrical signs of new membrane production during cleavage ofRana pipiens eggs.J. Gen. Physiol. 52:509
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de Laat, S.W., Barts, P.W.J.A. & Bakker, M.I. New membrane formation and intercellular communication in the earlyXenopus embryo. J. Membrain Biol. 27, 109–129 (1976). https://doi.org/10.1007/BF01869132
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DOI: https://doi.org/10.1007/BF01869132