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Ultrastructure and permeability of the Schwann cell layer surrounding the giant axon of the squid

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Journal of Neurocytology

Summary

The ultrastructure of the Schwann cell layer surrounding the giant axon of the squidAlloteuthis subulata is described, and the permeability of extracellular compartments assessed by exposure to electron-dense tracers. Morphometric analysis is used to deduce the number, size and shape of the Schwann cells, and the routes for ion flux across the Schwann cell layer. Axons (mean diameter 233 μm) were surrounded by a 1–2 μm thick layer of Schwann cells which were ∼ 1 μm thick, ∼ 70 μm long and ∼ 23 μm wide. There were around 62 000 Schwann cells per cm2 axon surface. The outer (abaxonal) surface of the Schwann cells was invaginated, with evidence for a covering of fine Schwann cell processes; the inner (adaxonal) surface of the Schwann cells was less folded. The percentage area occupied by mesaxonal cleft openings to the axon and to the basal lamina was 0.02% and 1.09% respectively. A system of tubules, the glial tubular system, occupied 3.9% of the Schwann cell volume, and opened to both axonal and basal lamina surfaces, with more elaborate lattice-like clusters towards the basal side of the cell. Tubule openings accounted for 0.26% of the surface area facing the axon and 0.37% of the area facing the basal lamina (where there was greater clustering of openings). The electron dense tracers horseradish peroxidase, ionic lanthanum and tannic acid filled mesaxon clefts, glial tubular system and periaxonal space. If ion flux occurred via the mesaxonal clefts, a theoretical series resistance (Rsth) of > 20Ω cm2, would be predicted, whereas if it occurred via the tubular system, the figure would be < 2 Ω cm2, closer to physiological estimates. The results presented show that the glial tubular system is likely to be the major route for ion flux into and across the Schwann cell layer, and for clearance of K+ from the periaxonal space during periods of axonal stimulation. The implications for K+ homeostasis in the axonal microenvironment are discussed.

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References

  • Abbott, N. J. &Brown, E. R. (1989) Effects of osmotic manipulation on extracellular routes for ion regulation in the squid Schwann cell.Journal of Physiology 418, 16P.

    Google Scholar 

  • Abbott, N. J. &Bundgaard, M. (1987) Microvessel surface area, density and dimensions in brain and muscle of the cephalopodSepia officinalis.Proceedings of the Royal Society of London, Series B 230, 459–82.

    Google Scholar 

  • Abbott, N. J., Larmet, Y. &Pichon, Y. (1985) A giant axon preparation for the study of periaxonal ion regulationin situ: the squidAlloteuthis.Journal of Physiology 369, 164P.

  • Abbott, N. J., Lieberman, E. M., Pichon, Y., Hassan, S. &Larmet, Y. (1988) Periaxonal K+ regulation in the small squidAlloteuthis: studies on isolated andin situ axons.Biophysical Journal 53, 275–9.

    PubMed  Google Scholar 

  • Abbott, N. J., Pichon, Y., Inoue, I., Brown, E. R., Lieberman, E. M. &Revest, P. A. (1989) Role Of Schwann cells in periaxonal ion regulation in the squid.Acta Physiologica Scandinavica 136, Suppl. 582, 42.

    Google Scholar 

  • Adelman, W. J., Jr., Palti, Y. &Senft, J. P. (1973) Potassium accumulation in a periaxonal space and its effect on the measurement of membrane potassium ion conductance.Journal of Membrane Biology 13, 387–410.

    PubMed  Google Scholar 

  • Adelman, W. J., Jr., Moses, J. &Rice, R. V. (1977) An anatomical basis for the resistance and capacitance in series with the excitable membrane of the squid giant axon.Journal of Neurocytology 6, 621–46.

    PubMed  Google Scholar 

  • Astion, M. L., Coles, J. A., Orkand, R. K. &Abbott, N. J. (1988) K+ accumulation in the space between giant axon and Schwann cell in the squidAlloteuthis.Biophysical Journal 53, 281–5.

    PubMed  Google Scholar 

  • Binstock, L., Adelman, W. J., Jr., Senft, J. P. &Lecar, H. (1975) Determination of the resistance in series with the membranes of giant axons.Journal of Membrane Biology 21, 25–47.

    PubMed  Google Scholar 

  • Brown, E. R. (1991)Axon-Schwann Cell Interaction in the Squid. Ph.D. Thesis, London University.

  • Brown, E. R. &Abbott, N. J. (1989) Pathways for ion regulation in the Schwann cell layer surrounding the giant axon of the squidAlloteuthis subulata.Acta Physiologica Scandinavica 136, Suppl. 582, 66.

    Google Scholar 

  • Brown, E. R., Bone, Q., Ryan, K. P. &Abbott, N. J. (1991) Morphology and electrical properties of Schwann cells around the giant axon of the squidsLoligo forbesi andLoligo vulgaris.Proceedings of the Royal Society of London Series B 243, 255–62.

    Google Scholar 

  • Bundgaard, M., Frøkjaer-Jensen, J. &Crone, C. (1979) Endothelial plasmalemmal vesicles as elements in a system of branching invaginations from the cell surface.Proceedings of the National Academy of Sciences (USA) 76, 6439–42.

    Google Scholar 

  • Frankenhaeuser, B. &Hodgkin, A. L. (1956) The after-effects of impulses in the giant nerve fibres ofLoligo.Journal of Physiology 131, 341–76.

    PubMed  Google Scholar 

  • Geren, B. B. &Schmitt, F. O. (1954) The structure of the Schwann cell and its relation to the axon in certain invertebrate nerve fibers.Proceedings of the National Academy of Sciences (USA) 40, 863–70.

    Google Scholar 

  • Glauert, A. M. (1986) Fixatives. InPractical Methods in Electron Microscopy, Vol. 3. Fixation, Dehydration and Embedding of Biological Specimens, Part 1 (edited byGlauert, A. M.), 48, Elsevier North-Holland Biomedical Press.

  • Grossman, Y., Parnas, I. &Spira, M. E. (1979) Ionic mechanisms involved in differential conduction of action potentials at high frequency in a branching axon.Journal of Physiology 295, 307–22.

    PubMed  Google Scholar 

  • Hama, K. (1962) Some observations on the fine structure of the giant synapse in the stellate ganglion of the squid,Doryteuphis bleekeri.Zeitschrift für Zellforschung 56, 437–44.

    Google Scholar 

  • Holtzman, E., Freeman, A. R. &Kashner, L. A. (1970) A cytochemical and electron microscope study of channels in the Schwann cells surrounding lobster giant axons.Journal of Cell Biology 44, 438–45.

    PubMed  Google Scholar 

  • Hootman, S. R. &Philpott, C. W. (1979) Ultracytochemical localization of Na+K+-activated ATPase in chloride cells from the gills of a euryhaline teleost.Anatomical Record 193, 99–130.

    PubMed  Google Scholar 

  • Karnovsky, M. J. (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy.Journal of Cell Biology 27, 137A.

    Google Scholar 

  • Karnovsky, M. J. (1967) The ultrastructural basis of capillary permeability studied with peroxidase as a tracer.Journal of Cell Biology 35, 213–236.

    PubMed  Google Scholar 

  • Komuro, T. &Yamamoto, T. (1975) The renal chloride cell of the fresh-water catfish,Parasilurus asotus, with special reference to the tubular membrane system.Cell and Tissue Research 160, 263–71.

    PubMed  Google Scholar 

  • Lane, N. J. &Abbott, N. J. (1975) The organization of the nervous system in the crayfishProcambarus clarkii, with emphasis on the blood-brain interface.Cell and Tissue Research 156, 173–87.

    PubMed  Google Scholar 

  • Lane, N. J., Swales, L. S. &Abbott, N. J. (1977) Lanthanum penetration in crayfish nervous system: observations on intact and ‘desheathed’ preparations.Journal of Cell Science 23, 315–24.

    PubMed  Google Scholar 

  • Larmet, Y. &Pichon, Y. (1988) Lack of potassium accumulation in fresh axons ofLoligo forbesi.Journal of Physiology 396, 166P.

    Google Scholar 

  • Leeson, T. S. &Leeson, C. R. (1982) The use of lanthanum chloride as a marker for intercellular junctions in rat exocrine pancreas.Stain Technology 57, 245–8.

    PubMed  Google Scholar 

  • Magalhaes, M. M. &Coimbra, A. (1972) The rabbit retinal Müller cell. A fine structural and cytochemical study.Journal of Ultrastructure Research 39, 310–26.

    PubMed  Google Scholar 

  • Peracchia, C. &Robertson, J. D. (1971) Increase in osmiophilia of axonal membranes of crayfish as a result of electrical stimulation, asphyxia, or treatment with reducing agents.Journal of Cell Biology 51, 223–39.

    PubMed  Google Scholar 

  • Pichon, Y., Abbott, N. J., Lieberman, E. M. &Larmet, Y. (1987) Potassium homeostasis in the nervous system of cephalopods and Crustacea.Journal de Physiologie (Paris) 82, 346–56.

    Google Scholar 

  • Pumplin, D. W. &Reese, T. S. (1978) Membrane ultrastructure of the giant synapse of the squidLoligo pealei.Neuroscience 3, 685–96.

    PubMed  Google Scholar 

  • Shivers, R. R. &Brightman, M. W. (1976) Trans-glial channels in ventral nerve roots of crayfish.Journal of Comparative Neurology 167, 1–26.

    PubMed  Google Scholar 

  • Shrager, P., Starkus, J. C., Lo, M.-V. C. &Peracchia, C. (1983) The periaxonal space of crayfish giant axons.Journal of General Physiology 82, 221–44.

    PubMed  Google Scholar 

  • Villegas, G. M. &Villegas, R. (1960) The ultrastructure of the giant nerve fiber of the squid: axon-Schwann cell relationship.Journal of Ultrastructure Research 3, 362–73.

    PubMed  Google Scholar 

  • Villegas, G. M. &Villegas, R. (1964) Extracellular pathways in the peripheral nerve fibres: Schwann cell layer permeability to thorium dioxide.Biochemica et Biophysica Acta 88, 231–3.

    Google Scholar 

  • Villegas, G. M. &Villegas, R. (1968) Ultrastructural studies of the squid nerve fibers.Journal of General Physiology 51, 44S-60S.

    PubMed  Google Scholar 

  • Villegas, G. M. &Villegas, R. (1984) Squid axon ultrastructure. InCurrent Topics in Membranes and Transport, Vol. 22 (edited byBaker, P. F.) pp. 3–37. London: Academic Press.

    Google Scholar 

  • Villegas, G. M., Lane, N. J. &Villegas, J. (1987) Freeze-fracture studies on the giant axon and ensheathing Schwann cells of the squid.Journal of Neurocytology 16, 11–21.

    PubMed  Google Scholar 

  • Villegas, J. (1972) Axon-Schwann cell interaction in the squid nerve fibre.Journal of Physiology 225, 275–96.

    PubMed  Google Scholar 

  • Villegas, R., Villegas, L., Gimenez, M. &Villegas, G. (1963) Schwann cell and axon electrical potential differences. Squid nerve structure and excitable membrane location.Journal of General Physiology 46, 1047–64.

    PubMed  Google Scholar 

  • Ward, B. J., Bauman, K. F. &Firth, J. A. (1988) Interendothelial junctions of cardiac capillaries in rats: their structure and permeability properties.Cell and Tissue Research 252, 57–66.

    PubMed  Google Scholar 

  • Young, J. Z. (1936) The structure of nerve fibres in Cephalopods and Crustacea.Proceedings of the Royal Society of London, Series B 121, 319–37.

    Google Scholar 

  • Zwahlen, M. J., Sandri, C. &Greeff, N. J. (1988) Transglial pathway of diffusion in the Schwann sheath of the squid giant axon.Journal of Neurocytology 17, 145–59.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Marine Biological Association Laboratory, Citadel Hill, PL1 2PB, Plymouth, UK

    E. R. Brown & N. J. Abbott

  2. Physiology Group, Biomedical Sciences Division, King's College, University of London, WC2R 2LS, Strand, London, UK

    E. R. Brown & N. J. Abbott

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  1. E. R. Brown
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  2. N. J. Abbott
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Brown, E.R., Abbott, N.J. Ultrastructure and permeability of the Schwann cell layer surrounding the giant axon of the squid. J Neurocytol 22, 283–298 (1993). https://doi.org/10.1007/BF01187127

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  • DOI: https://doi.org/10.1007/BF01187127

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