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The development of a zonula occludens in peripheral myelin of the chick embryo

A freeze-fracture study

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Summary

Sciatic nerves of chick embryos, 12 to 18 days incubation, were examined in freeze-fracture replicas with special emphasis placed on the development of tight junctional contacts in the myelin sheaths. In stages of beginning myelination short isolated particulate chains (focal tight junctions) appear in fracture faces of the adjacent membranes in the outer myelin lamellae, i.e., the outer mesaxon. In stages of progressing myelination these tight junctional elements elongate and become more numerous. They can also be found in the membranes of the inner mesaxons, the paranodal loops and the intramyelinic cytoplasmic inclusions. In fibers of advanced myelinogenesis a fusion of these isolated tight junctions — either end-to-end or at an angle — gives rise to continuous zonulae occludentes. This contact zone extends in the mesaxonal membranes along the direction of the fiber, whereas in paranodal myelin it acquires a helical course joining the membranes of the paranodal loops. It is proposed that this zonula occludens, which seals the cytoplasmic border of the Schwann cell, separates an intramyelinic from an extramyelinic, extracellular space already during the developmental stages of myelinogenesis.

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References

  • Branton, D.: Fracture faces of frozen membranes. Proc. nat. Acad. Sci. (Wash.) 55, 1048–1056 (1966)

    Google Scholar 

  • Branton, D.: Fracture faces of frozen myelin. Exp. Cell Res. 45, 703–707 (1967)

    Google Scholar 

  • Branton, D., Bullivant, S., Gilula, N.B., Karnovsky, M.J., Moor, H., Mühlethaler, K., Northcote, D.H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L.A., Steere, R.L., Weinstein, R.S.: Freeze- etching nomenclature. Science 190, 54–56 (1975)

    Google Scholar 

  • Claude, P., Goodenough, D.A.: Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J. Cell Biol. 58, 390–400 (1973)

    Google Scholar 

  • Decker, R.S., Friend, D.S.: Assembly of gap junctions during amphibian neurulation. J. Cell Biol. 62, 32–47 (1974)

    Google Scholar 

  • Dermietzel, R.: Junctions in the central nervous system of the cat. I. Membrane fusion in central myelin. Cell Tiss. Res. 148, 565–576 (1974)

    Google Scholar 

  • Dermietzel, R., Meller, K., Tetzlaff, W., Waelsch, M.: In vivo and in vitro formation of the junctional complex in choroid epithelium. Cell Tiss. Res. 181, 427–441 (1977)

    Google Scholar 

  • Farquhar, M.G., Palade, G.E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963)

    Google Scholar 

  • Friede, R.L., Control of myelin formation by axon caliber (with a model of the control mechanism). J. comp. Neurol. 144, 233–252 (1972)

    Google Scholar 

  • Friede, R.L., Miyagishi, T.: Adjustment of the myelin sheath to changes in axon caliber. Anat. Rec. 172, 1–14 (1972)

    Google Scholar 

  • Geren, B.B.: The formation from the Schwann cell surface of myelin in the peripheral nerves of chick embryos. Exp. Cell Res. 7, 558–562 (1954)

    Google Scholar 

  • Gilula, N.B., Fawcett, D.W., Aoki, A.: The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Develop. Biol. 50, 142–168 (1976)

    Google Scholar 

  • Hall, S.M., Williams, P.L.: The distribution of electron-dense tracers in peripheral nerve fibers. J. Cell Sci. 8, 541–555 (1971)

    Google Scholar 

  • Klemm, H.: Das Perineurium als Diffusionsbarriere gegenüber Peroxydase bei epi- und endoneuraler Applikation. Z. Zellforsch. 108, 431–445 (1970)

    Google Scholar 

  • Luft, J.H.: Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat. Rec. 171, 369–416 (1971)

    Google Scholar 

  • Machen, T.E., Erlij, D., Wooding, F.B.P.: Permeable junctional complexes. The movement of lanthanum across rabbit gallbladder and intestine. J. Cell Biol. 54, 302–312 (1972)

    Google Scholar 

  • Meller, K., Tetzlaff, W.: The development of membrane specializations in the receptor-bipolar-horizontal cell synapse of the chick embryo retina. Cell Tiss. Res. 181, 319–326 (1977)

    Google Scholar 

  • Møllgård, K.: Membrane specializations in immature dendrites visualized by freeze-etching. In: Golgi Centennial Symposium (M. Santini, ed.), pp. 367–377. New York: Raven Press 1975

    Google Scholar 

  • Montesano, R., Friend, D.S., Perrelet, A., Orci, L.: In vivo assembly of tight junctions in fetal rat liver. J. Cell Biol. 67, 310–319 (1975)

    Google Scholar 

  • Mugnaini, E., Osen, K.K., Schnapp, B., Friedrich, V.L.: Distribution of Schwann cell cytoplasm and plasmalemmal vesicles (caveolae) in peripheral myelin sheaths. An electron microscopic study with thin sections and freeze-fracturing. J. Neurocytol. 6, 647–668 (1977)

    Google Scholar 

  • Mugnaini, E., Schnapp, B.: Possible role of zonula occludens of the myelin sheath in demyelinating conditions. Nature (Lond.) 251, 725–727 (1974)

    Google Scholar 

  • Pannese, E., Luciano, L., Iurato, S., Reale, E.: Intercellular junctions and other membrane specializations in developing spinal ganglia: A freeze-fracture study. J. Ultrastruct. Res. 60, 169–180 (1977)

    Google Scholar 

  • Peters, A.: A radial component of central myelin sheaths. J. biophys. biochem. Cytol. 11, 733–735 (1961)

    Google Scholar 

  • Peters, A., Vaughn, J.E.: Morphology and development of the myelin sheath. In: Myelination (A.N. Davison and A. Peters, eds.), pp. 3–79. Springfield, Ill.: Charles C. Thomas 1970

    Google Scholar 

  • Peterson, R.G., Pease, D.C.: Myelin embedded in polymerized glutaraldehyde-urea. J. Ultrastruct. Res. 41, 115–132 (1972)

    Google Scholar 

  • Pfenninger, K.H., Bunge, R.P.: Freeze-fracturing of nerve growth cones and young fibers. A study of developing plasma membrane. J. Cell Biol. 63, 180–196 (1974)

    Google Scholar 

  • Reale, E., Luciano, L., Spitznas, M.: Zonulae occludentes of the myelin lamellae in the nerve fibre layer of the retina and in the optic nerve of the rabbit: a demonstration by the freeze-fracture method. J. Neurocytol. 4, 131–140 (1975)

    Google Scholar 

  • Revel, J.-P., Brown, S.S.: Cell junctions in development, with particular reference to the neural tube. In: Cold Spr. Harb. Symp. quant. Biol. 40, 443–455 (1976)

    Google Scholar 

  • Revel, J.-P., Hamilton, D.W.: The double nature of the intermediate dense line in peripheral nerve myelin. Anat. Rec. 163, 7–16 (1969)

    Google Scholar 

  • Robertson, J.D.: Structural alterations in nerve fibers produced by hypotonic and hypertonic solutions. J. biophys. biochem. Cytol. 4, 349–364 (1958)

    Google Scholar 

  • Robertson, J.D.: The molecular structure and contact relationships of cell membranes. Progr. Biophys. 10, 343–418 (1960)

    Google Scholar 

  • Schnapp, B., Mugnaini, E.: The myelin sheath: Electron microscopic studies with thin sections and freeze-fracture. In: Golgi Centennial Symposium (M. Santini, ed.), pp. 209–233. New York: Raven Press 1975

    Google Scholar 

  • Staehelin, L.A.: Structure and function of intercellular junctions. In: International Rev. Cytol. (G.H. Bourne and J.F. Danielli, eds.), Vol. 39, pp. 191–283. New York-London: Academic Press 1974

    Google Scholar 

  • Tani, E., Ikeda, K., Nishiura, M.: Freeze-etching images of central myelinated nerve fibres. J. Neurocytol. 2, 305–314 (1973)

    Google Scholar 

  • Wade, J.B., Karnovsky, M.J.: Fracture faces of osmotically disrupted zonulae occludentes. J. Cell Biol. 62, 344–350 (1974)

    Google Scholar 

  • Webster, H. de F.: The geometry of peripheral myelin sheaths during their formation and growth in rat sciatic nerves. J. Cell Biol. 48, 348–367 (1971)

    Google Scholar 

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The author is especially indebted to Prof. K. Meller for his continuous encouragement and support. This study was made possible by a grant (Az. 11 2977) from the Stiftung Volkswagenwerk to K.M. The author thanks Miss. K. Rascher for her help with the English translation, Mr. K. Donberg for the photographic assistance and Mrs. C. Bloch for typing the manuscript

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Tetzlaff, W. The development of a zonula occludens in peripheral myelin of the chick embryo. Cell Tissue Res. 189, 187–201 (1978). https://doi.org/10.1007/BF00209269

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