Skip to main content
Log in

New membrane formation and intercellular communication in the earlyXenopus embryo

I. Electrophysiological analysis

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. 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

    PubMed  Google Scholar 

  2. 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

    PubMed  Google Scholar 

  3. Bennett, M. V. L. 1966. Physiology of electrotonic junctions.Ann. N. Y. Acad. Sci. 137:509

    PubMed  Google Scholar 

  4. Bennett, M. V. L., 1973. Function of electrotonic junctions in embryonic and adult tissues.Fed. Proc. 32:65

    Google Scholar 

  5. Bennett, M. V. L., Spira, M. E., Pappas, G. D. 1972. Properties of electrotonic junctions between embryonic cells ofFundulus.Dev. Biol. 29:419

    Google Scholar 

  6. 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

    PubMed  Google Scholar 

  7. Bluemink, J. G. 1971. Effects of cytochalasin B on surface contractility and cell junction formation during egg cleavage inXenopus laevis.Cytobiologie 3:176

    Google Scholar 

  8. 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

    PubMed  Google Scholar 

  9. Decker, R. S., Friend, D. S. 1974. Assembly of gap junctions during neurulation.J. Cell Biol. 62:32

    PubMed  Google Scholar 

  10. DiCaprio, R. A., French, A. S., Sanders, E. J. 1974. Dynamic properties of electrotonic coupling between cells of earlyXenopus embryos.Biophys. J. 14:387

    Google Scholar 

  11. 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

    Google Scholar 

  12. Gilula, N. B., Reeves, O. r., Steinbach, A. 1972. Metabolic coupling, ionic coupling and cell contacts.Nature 235:262

    PubMed  Google Scholar 

  13. Hulser, D. F., Demsey, A. 1973. Gap and low-resistance junctions between cells in culture.Z. Naturforsch. 28:603

    Google Scholar 

  14. Ito, S., Hori, N. 1966. Electrical characteristics ofTriturus egg cells during cleavage.J. Gen. Physiol. 49:1019

    PubMed  Google Scholar 

  15. Ito, S., Loewenstein, W. R. 1969. Ionic communication between early embryonic cells.Dev. Biol. 19:228

    PubMed  Google Scholar 

  16. 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

    Google Scholar 

  17. 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

    Google Scholar 

  18. Johnson, R. G., Sheridan, J. D. 1971. Junctions between cancer cells in culture: Ultrastructure and permeability.Science 174:717

    PubMed  Google Scholar 

  19. 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

    Google Scholar 

  20. 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

    PubMed  Google Scholar 

  21. 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

    PubMed  Google Scholar 

  22. 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

    PubMed  Google Scholar 

  23. 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

    PubMed  Google Scholar 

  24. Loewenstein, W. R. 1966. Permeability of membrane junctions.Ann. N. Y. Acad. Sci. 137:441

    PubMed  Google Scholar 

  25. Loewenstein, W. R. 1968. Communication through cell junctions, implications in growth control and differentiation.Dev. Biol. 19, Suppl.2:151

    Google Scholar 

  26. Loewenstein, W. R. 1968. Some reflections on growth and differentiation.Perspect. Biol. Med. 11:260

    PubMed  Google Scholar 

  27. Loewenstein, W. R., Kanno, Y. 1964. Studies on an epithelial (gland) cell junction. I. Modification of surface membrane permeability.J. Cell Biol. 22:565

    PubMed  Google Scholar 

  28. 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

    PubMed  Google Scholar 

  29. Nieuwkoop, P. D., Faber, J. 1956. Normal Table ofXenopus laevis (Daudin). North-Holland Publishing Company, Amsterdam

    Google Scholar 

  30. Palmer, J. F., Slack, C. 1970. Some bio-electric parameters of earlyXenopus embryos.J. Gen. Physiol. 24:535

    Google Scholar 

  31. Payton, B. W., Bennett, M. V. L., Pappas, G. D. 1969. Permeability and structure of junctional membranes at an electrotonic synapse.Science 166:1641

    PubMed  Google Scholar 

  32. 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

    PubMed  Google Scholar 

  33. 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

    Google Scholar 

  34. 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

    PubMed  Google Scholar 

  35. Rose, B. 1971. Intercellular communication and some structural aspects of membrane junctions in a simple cell system.J. Membrane Biol. 5:1

    Google Scholar 

  36. Sanders, E. J., Zalik, S. E. 1972. The blastomere periphery ofXenopus laevis, with special reference to intercellular relationships.Wilhelm Roux' Archiv 171:181

    Google Scholar 

  37. Satir, P., Gilula, N. B. 1973. The fine structure of membranes and intercellular communication in insects.,Annu. Rev. Entomol. 18:143

    PubMed  Google Scholar 

  38. Sheridan, J. D. 1968. Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo.J. Cell Biol. 37:650

    PubMed  Google Scholar 

  39. Sheridan, J. D. 1971. Dye movement and low-resistance junctions between reaggregated embryonic cells.Dev. Biol. 26:627

    PubMed  Google Scholar 

  40. Singal, P. K., Sanders, E. J. 1974. An ultrastructural study of the first cleavage ofXenopus embryos.J. Ultrastruct. Res. 47:433

    PubMed  Google Scholar 

  41. 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

    PubMed  Google Scholar 

  42. Takahashi, M., Ito, S. 1968. Electrophysiological studies on membrane formation during cleavage of the amphibian egg.Zool. Mag. 77:307

    Google Scholar 

  43. Tupper, J. T., Saunders, J. W., Jr. 1972. Intercellular permeability in the earlyAsterias embryo.Dev. Biol. 27:546

    Google Scholar 

  44. 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

    PubMed  Google Scholar 

  45. Wiener, J., Spiro, D., Loewenstein, W. R. 1964. Studies on an epithelial (gland) cell junction. II. Surface structure.J. Cell Biol. 22:587

    PubMed  Google Scholar 

  46. Woodward, D. J. 1968. Electrical signs of new membrane production during cleavage ofRana pipiens eggs.J. Gen. Physiol. 52:509

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01869132

Keywords

Navigation