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Permeability and Structure of Electrotonic Junctions and Intercellular Movements of Tracers

  • M. V. L. Bennett

Abstract

In this paper I shall present a brief review of the data that led to our concept of the structure of the electrotonic junction or synapse. Some find the arguments persuasive, to a variable degree, and certainly the idea is at least hinted at in the work of many who have studied these junctions. In the second part of the paper I shall deal with some effects of histological fixation on junctional properties and the implications for interpretation of tracer measurements. Much of this work is in progress, and I am indebted to my colleagues for permission to use and refer to unpublished findings of collaborative work.

Keywords

Nerve Cord Horse Radish Peroxidase Electrical Coupling Close Apposition Couple Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Asada, Y., and M. V. L. Bennett: Experimental alteration of coupling resistance at an electrotonic synapse. J. Cell Biol. 49, 159–172 (1971).PubMedCrossRefGoogle Scholar
  2. Benedetti, E. L., and P. Emmelot: Hexagonal array of subunits in tight junctions separated from isolated rat liver plasma membranes. J. Cell Biol. 38, 15–24 (1968).PubMedCrossRefGoogle Scholar
  3. Bennett, M. V. L.: Electroreception. In: Fish Physiology. Ed. W. S. Hoar and D. S. Randall. pp. 493–574. New York: Academic Press, 1971.Google Scholar
  4. Bennett, M. V. L.: A comparison of electrically and chemically mediated transmission. In: Structure and Function of Synapses. Ed. G. D. Pappas and D. P. Purpura, pp. 221–256. New York: Raven Press, 1972.Google Scholar
  5. Bennett, M. V. L., and A. A. Auerbach: Calculation of electrical coupling of cells separated by a gap. Anat. Rec. 163, 152 (1969).Google Scholar
  6. Bennett, M. V. L., and P. B. Dunham: Sucrose permeability of junctional membrane at an electrotonic synapse. Biophys. J. 10, 117a (1970).Google Scholar
  7. Bennett, M. V. L., and J. P. Trinkaus: Electrical coupling between embryonic cells by way of extracellular space and specialized junctions. J. Cell Biol. 44, 592–610 (1970).PubMedCrossRefGoogle Scholar
  8. Bennett, M. V. L., G. D. Pappas, E. Aljure, and Y. Nakajima: Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in Morymyrid fish. J. Neurophysiol. 30, 180–208 (1967a).PubMedGoogle Scholar
  9. Bennett, M. V. L., Y. Nakajima, and G. D. Pappas: Physiology and ultrastructure of electronic junctions. III. Giant electromotor neurons of Malapterurus electricus. J. Neurophysiol. 30, 209–235 (1967b).PubMedGoogle Scholar
  10. Bennett, M. V. L., G. D. Pappas, M. Gimenez, and Y. Nakajima: Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish. J. Neurophysiol. 30, 236–301 (1967c).PubMedGoogle Scholar
  11. Bennett, M. V. L., P. B. Dunham, and G. D. Pappas: Ion fluxes through a “tight junction.” J. gen. Physiol 50, 1094 (1967d).CrossRefGoogle Scholar
  12. Bennett, M. V. L., M. E. Spira, and G. D. Pappas: Properties of electrotonic junctions between embryonic cells of Fundulus. Developmental Biol. 29, 419–435 (1972a).CrossRefGoogle Scholar
  13. Bennett, M. V. L., M. E. Spira, and G. D. Pappas: Effect of fixatives for electron microscopy on properties of electrotonic junctions between embryonic cells. J. Cell Biol. 55, 17a (1972b).Google Scholar
  14. Bennett, M. V. L., N. Feder, T. S. Reese, and W. Stewart: Movement during fixation of peroxidases injected into the crayfish septate axon. J. gen. Physiol., (in the press).Google Scholar
  15. Brightman, M. W., and T. S. Reese: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969).PubMedCrossRefGoogle Scholar
  16. Chalcroft, J. P., and S. Bullivant: An interpretation of liver cell membrane and junction structure based on observation of freeze-fracture replicas of both sides of the fracture. J. Cell Biol. 47, 49–60 (1970).PubMedCrossRefGoogle Scholar
  17. Feder, N.: Microperoxid ase. An ultrastructural tracer of low molecular weight. J. Cell Biol. 51, 339–343 (1970).CrossRefGoogle Scholar
  18. Friend, D. S., and N. B. Gilula: Variations in tight and gap junctions in mammalian tissues. J. Cell Biol. 53, 758–776 (1972).PubMedCrossRefGoogle Scholar
  19. Furshpan, E. J., and D. D. Potter: Low-resistance junctions between cells in embryos and tissue culture. In: Current Topics in Developmental Biology. Ed. A. A. Moscona, and A. Monroy. Vol. 3, pp. 95–127, 1968.Google Scholar
  20. Gilula, N. B., O. R. Reeves, and A. Steinbach: Metabolic coupling, ionic coupling and cell contacts. Nature, Lond. 235, 262–265 (1972).CrossRefGoogle Scholar
  21. Gilula, N. B., and P. Satir: Septate and gap junctions in molluscan gill epithelium. J. Cell Biol. 51, 869–872 (1971).PubMedCrossRefGoogle Scholar
  22. Goodenough, D. A., and W. Stoeckenius: The isolation of mouse hepatocyte gap junctions. Preliminary chemical characterization and x-ray diffraction. J. Cell Biol. 54, 646–656 (1972).PubMedCrossRefGoogle Scholar
  23. Heppner, D. B., and R. Plonsey: Simulation of electrical interaction of cardiac cells. Biophys. J. 10, 1057–1075 (1970).PubMedCrossRefGoogle Scholar
  24. Heuser, J. E. and R. Miledi: Effect of lanthanum ions on function and structure of frog neuromuscular junctions. Proc. Roy. Soc. (Lond.) B179, 247–260 (1971).Google Scholar
  25. Johnson, R. G., and J. D. Sheridan: Junctions between cancer cells in culture: ultrastructure and permeability. Science 174, 717–719 (1971).PubMedCrossRefGoogle Scholar
  26. Kaneko, A.: Electrical connexions between horizontal cells in the dogfish retina. J. Physiol., Lond. 213, 95–105 (1971a).PubMedGoogle Scholar
  27. Karlsson, U., and R. L. Schultz: Fixation of the central nervous system for electron microscopy by aldehyde perfusion. J. Ultrastruct. Res. 12, 160–206 (1965).PubMedCrossRefGoogle Scholar
  28. Karnovsky, M. J.: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213–236 (1967).PubMedCrossRefGoogle Scholar
  29. Kristensson, K., Y. Olsson, and J. Sjostrand: Axonal uptake and retrograde transport of exogenous proteins in the hypoglossal nerve. Brain Res. 32, 399–406 (1971).PubMedCrossRefGoogle Scholar
  30. LaVail, J. H., and M. M. LaVail: Retrograde axonal transport in the central nervous system. Science 16, 1416–1417 (1972).CrossRefGoogle Scholar
  31. McNutt, N. S., and R. S. Weinstein: The ultrastructure of the nexus. A correlated thin section and freeze cleave study. J. Cell Biol. 47, 666–688 (1970).PubMedCrossRefGoogle Scholar
  32. Pappas, G. D., and M. V. L. Bennett: Specialized junctions involved in electrical transmission between neurons. Ann. N.Y. Acad. Sci. 131, 495–508 (1966).CrossRefGoogle Scholar
  33. Pappas, G. D., Y. Asada, and M. V. L. Bennett: Morphological correlates of increased coupling resistance at an electrotonic synapse. J. Cell Biol. 49, 173–188 (1971).PubMedCrossRefGoogle Scholar
  34. Payton, B. W.: Histological staining properties of Procion yellow. J. Cell Biol. 45, 659–662 (1970).PubMedCrossRefGoogle Scholar
  35. Payton, B. W., M. V. L. Bennett, and G. D. Pappas: Permeability and structures of junctional membranes at an electrotonic synapse. Science 166, 1641–1643 (1969).PubMedCrossRefGoogle Scholar
  36. Politoff, A., and G. D. Pappas: Mechanisms of increase in coupling resistance at electrotonic synapses of the crayfish septate axon. Anat. Rec. 172, 384–385 (1972).Google Scholar
  37. Politoff, A., and M. V. L. Bennett: Cobalt: a tracer for light and electron microscopy hat can cross an electrotonic synapse. J. Cell Biol. 55, 204a (1972).Google Scholar
  38. Potter, D. D., E. J. Furshpan, and E. S. Lennox: Connections between cells of the developing quid as revealed by electrophysiological methods. Proc. natn. Acad. Sci. U.S.A. 55, 28–336 (1966).CrossRefGoogle Scholar
  39. Reese, T. S., M. V. L. Bennett, and N. Feder: Cell-to-cell movement of peroxidases injected into the septate axon of crayfish. Anat. Rec. 169, 409 (1971).Google Scholar
  40. Revel, J. P., and M. J. Karnovsky: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7–C12 (1967).PubMedCrossRefGoogle Scholar
  41. Robertson, J. D.: The occurrence of a subunit pattern in the unit membranes of club endings in Mauthner cell synapses in goldfish brains. J. Cell Biol. 19, 201–221 (1963).PubMedCrossRefGoogle Scholar
  42. Rose, B.: Intercellular communication and some structural aspects of membrane junctions in a simple cell system. J. Membrane Biol. 5, 1–9 (1971).CrossRefGoogle Scholar
  43. Sheridan, J. D.: Dye movement and low resistance junctions between reaggregated embryonic cells. Devl. Biol. 26, 627–656 (1971).CrossRefGoogle Scholar
  44. Slack, C., and J. F. Palmer: The permeability of intercellular junctions in the early embryo of Xenopus laevis, studied with a fluorescent tracer. Expl Cell Res. 55, 416–419 (1969).CrossRefGoogle Scholar
  45. Tupper, J. T., and J. W. Saunders: Intercellular permeability in the early Asterias embryo. Devl Biol. 27, 546–554 (1972).CrossRefGoogle Scholar
  46. Weidmann, S.: The diffusion of radiopotassium across intercalated disks of mammalian cardiac muscle. J. Physiol., Lond. 187, 323–342 (1966).PubMedGoogle Scholar

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© Springer-Verlag New York Inc. 1973

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  • M. V. L. Bennett

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