Skip to main content
SpringerLink
Log in

Node of Ranvier formation along fibres regenerating through silicone tube implants: A freeze-fracture and thin-section electron microscopic study

  • Published:
Journal of Neurocytology

Summary

Thin-section and freeze-fracture electron microscopy have been used to examine the morphogenesis of the node of Ranvier in peripheral nerves regenerating through silicone tubes. A major question posed by this study is whether node formation in fibres regenerating across a gap recapitulates that occurring in normal development. Node formation occurs concurrently with myelination and follows a similar spatial gradient of progression from a proximal to distal direction along the regenerated nerve. Presumptive nodal sites appear prior to myelin formation and are identified as a prominent subaxolemmal density in thin sections and axonal particle patches in freeze-fracture. Following the appearance of presumptive nodes in regenerating fibres, dimeric particles are inserted into the axolemma adjacent to the node. These particles are in close apposition to the overlying Schwann cell terminal processes and with maturity adopt the same circumferential orientation seen in adult nodes. The nodal axolemma of regenerating fibres shows a characteristic increase in the prominence of its subaxolemmal densification and number of heterogeneously sized particles. Mature regenerated nodes demonstrate a complete annulus of nodal particles indistinguishable from control nodes. The results of the present study show that the nodal architecture of regenerating fibres is a faithful reconstruction of normal mature nodes, thus indicating that the morphological correlates associated with saltatory conduction at the node are present in regenerated nodes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aguayo, A., Charron, L. &Bray, G. (1976a) Potential of Schwarm cells from unmyelinated nerves to produce myelin: a quantitative and radiographie study.Journal of Neurocytology 5, 565–73.

    Google Scholar 

  • Aguayo, A., Epps, J., Charron, J. &Bray, G. (1976b) Multipotentiality of Schwann cells in cross-anastomosed and -grafted myelinated and unmyelinated nerves: quantitative microscopy and radioautography.Brain Research 104, 1–20.

    Google Scholar 

  • Allt, G. (1969) Ultrastructural features of the immature peripheral nerve.Journal of Anatomy 105, 283–93.

    Google Scholar 

  • Ariyasu, R. G., Nichol, J. A. &Ellisman, M. H. (1985) Localization of sodium/potassium adenosine triphosphate in multiple cell types of the murine nervous system with antibodies raised against the enzyme from kidney.Journal of Neuroscience 5, 2581–96.

    Google Scholar 

  • Berthold, C. H. (1978) Morphology of normal peripheral axons. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.), pp. 3–63. New York: Raven Press.

    Google Scholar 

  • Berthold, C. H. &Rydmark, M. (1983) Electron microscopic serial section analysis of nodes of Ranvier in lumbosacral spinal roots of the cat. Ultrastructural organization of nodal compartments in fibres of different sizes.Journal of Neurocytology 12, 475–505.

    Google Scholar 

  • Berthold, C. H. &Skoglund, S. (1968) Postnatal development of feline paranodal myelin-sheath segments. II. Electron microscopy.Acta Societatis Medicorum Upsaliensis 73, 127–44.

    Google Scholar 

  • Black, J. A., Foster, R. E. &Waxman, S. (1982) Rat optic nerve: freeze-fracture studies during development of myelinated axons.Brain Research 250, 1–20.

    Google Scholar 

  • Bonnaud-Toulze, E. N. &Raine, C. S. (1980) Remodelling during remyelination in the peripheral nervous system.Neuropathology and Applied Neurobiology 6, 279–90.

    Google Scholar 

  • Bostock, H., Hall, S. M. &Smith, K. J. (1980) Demyelinated axons can form nodes prior to remyelination.Journal of Physiology (London) 308, 21P–22P.

    Google Scholar 

  • Brady, R. O. &Quarles, R. H. (1973) The enzymology of myelination.Molecular and Cellular Biochemistry 2, 23–9.

    Google Scholar 

  • Chiu, S. Y. &Ritchie, J. M. (1980) Potassium channels in nodal and internodal axonal membrane of mammalian myelinated fibers.Nature 284, 170–1.

    Google Scholar 

  • Deerinck, T. J. &Ellisman, M. H. (1984) Transcellular filaments at the node of Ranvier.Society for Neuroscience Abstracts 10, 163.

    Google Scholar 

  • Ellisman, M. H. (1976) The distribution of membrane molecular specializations characteristic of the node of Ranvier is not dependent upon myelination.Society for Neuroscience Abstracts 2, 410.

    Google Scholar 

  • Ellisman, M. H. (1979) Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination.Journal of Neurocytology 8, 719–35.

    Google Scholar 

  • Ellisman, M. H. (1984) A transcellular filament network that interconnects cells in tissues.Society for Neuroscience Abstracts 10, 44.

    Google Scholar 

  • Ellisman, M. H. &Levinson, S. R. (1982) Immunocytochemical localization of sodium channel distributions in the excitable membranes of Electrophorus electricus.Proceedings of the National Academy of Sciences USA 79, 6707–11.

    Google Scholar 

  • Ellisman, M. H. &Staehelin, L. A. (1979) Electronically interlocked electron gun shutter for preparing improved replicas of freeze-fracture specimens. InPreparation-Dependent Changes in Freeze-Fracture (edited byRash, J. E. &Hudson, C. S.), pp. 123–5. New York: Raven Press.

    Google Scholar 

  • Fields, R. D. &Ellisman, M. H. (1986) Axons regenerated through silicone tube splices. II. Conduction properties.Experimental Neurology 92, 61–74.

    Google Scholar 

  • Ghabriel, M. N. &Allt, G. (1977) Regeneration of the node of Ranvier: a light and electron microscope study.Acta neuropathologica 37, 153–63.

    Google Scholar 

  • Hildebrand, C., Kocsis, J. D., Berglund, S. &Waxman, S. G. (1985) Myelin sheath remodelling in regenerated rat sciatic nerve.Brain Research 358, 163–70.

    Google Scholar 

  • Hirano, A. &Dembitzer, H. M. (1969) The transverse bands as a means of access to the periaxonal space of the central myelinated nerve fiber.Journal of Ultrastructure Research 28, 141–9.

    Google Scholar 

  • Kocsis, J. D. (1984) Functional organization of potassium channels in normal and pathological mammalian axons. InThe Node of Ranvier (edited byZagoren, J. C. &Federoff, S.), pp. 183–211. Orlando: Academic Press.

    Google Scholar 

  • Livingston, R. B., Pfenninger, K., Moor, H. &Akert, K. (1973) Specialized paranodal and interparanodal glial-axonal junctions in the peripheral and central nervous system: a freeze-etching study.Brain Research 58, 1–24.

    Google Scholar 

  • Le Beau, J. M., Longo, F. M. &Ellisman, M. H. (1983) Morphological assessment of myelination occurring in adult peripheral nerves regenerating through a silicone chamber.Society for Neuroscience Abstracts 9, 49.

    Google Scholar 

  • Le Beau, J. M., Schubert, D., Powell, H. C. &Ellisman, M. H. (1986) Fluid conditioned by peripheral nerves regeneratingin vivo stimulates Schwann cell migration and proliferationin vitro.Journal of Cell Biology 101 (2), 227a.

    Google Scholar 

  • Lundborg, G., Gelberman, R. H., Longo, F. M., Powell, H. C. &Varon, S. (1982) In vivo regeneration of cut nerves encased in silicone tubes: growth across a six-millimeter gap.Journal of Neuropathology and Experimental Neurology 4, 412–22.

    Google Scholar 

  • Mollenhauer, H. H. (1964) Plastic embedding mixtures for use in electron microscopy.Stain Technology 39, 111–14.

    Google Scholar 

  • Phillips, D. D., Hibbs, R. G., Ellison, J. P. &Shapiro, H. (1972) An electron microscopic study of central and peripheral nodes of Ranvier.Journal of Anatomy 111, 229–38.

    Google Scholar 

  • Raine, C. S. (1982) Differences between the nodes of Ranvier of large and small diameter fibres in the P.N.S.Journal of Neurocytology 11, 935–47.

    Google Scholar 

  • Singer, I. (1979) The fibronexus: a transmembrane association of fibronectin-containing fibers and bundles of 5nm microfilaments in hamster and human fibroblasts.Cell 16, 675–85.

    Google Scholar 

  • Smith, K. J., Bostock, H. &Hall, S. M. (1982) Saltatory conduction precedes remyelination in axons demyelinated with lysophosphatidyl choline.Journal of The Neurological Sciences 54, 13–31.

    Google Scholar 

  • Sunderland, S. (1978)Nerves and Nerve Injuries (2nd edn). Edinburgh: Churchill Livingstone.

    Google Scholar 

  • Tao-Cheng, J. &Rosenbluth, J. (1982) Development of nodal and paranodal membrane specializations in amphibian peripheral nerves.Developmental Brain Research 3, 577–94.

    Google Scholar 

  • Uzman, B. G. &Villegas, G. M. (1983) Mouse sciatic nerve regeneration through semipermeable tubes: a quantitative model.Journal of Neuroscience Research 9, 325–38.

    Google Scholar 

  • Waxman, S. G. (1984) Reorganization of the axon membrane during the development of myelinated fibers. InNeuromuscular Diseases (edited bySerratrice, G., Cros, D., Desnuelle, C., Gastaut, J. L. Pellissier, J. F. &Pouget, J.), pp. 253–9. New York: Raven Press.

    Google Scholar 

  • Waxman, S. G., Black, J. A. &Foster, R. E. (1983) Ontogenesis of the axolemma and axoglial relationships in myelinated fibers: electrophysiological and freeze-fracture correlates of membrane plasticity.International Review of Neurobiology 24, 433–84.

    Google Scholar 

  • Weinberg, H. J. &Spencer, P. S. (1976) Studies on the control of myelinogenesis. II. Evidence for neuronal regulation of myelin production.Brain Research 113, 363–78.

    Google Scholar 

  • Wiley, C. A. &Ellisman, M. H. (1980) Rows of dimeric-particles within the axolemma and juxtaposed particles within glia, incorporated into a new model for the paranodal-glial junction at the node of Ranvier.Journal of Cell Biology 84, 261–80.

    Google Scholar 

  • Wiley-Livingston, C. A. &.Ellisman, M. H. (1980) Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration.Developmental Biology 79, 334–55.

    Google Scholar 

  • Williams, L. R.;Longo, F. M., Powell, H. C., Lundborg, G. &Varon, S. (1983) Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: parameters for a bioassay.Journal of Comparative Neurology 218, 469–70.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory for Neurocytology, Department of Neurosciences, University of California, 92093, San Diego, La Jolla, California, USA

    J. M. Le Beau & M. H. Ellisman

  2. The Veteran's Administration Medical Center San Diego and Department of Pathology, University of California, 92093, San Diego, La Jolla, California, USA

    H. C. Powell

Authors
  1. J. M. Le Beau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. C. Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. H. Ellisman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Beau, J.M., Powell, H.C. & Ellisman, M.H. Node of Ranvier formation along fibres regenerating through silicone tube implants: A freeze-fracture and thin-section electron microscopic study. J Neurocytol 16, 347–358 (1987). https://doi.org/10.1007/BF01611346

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01611346

Keywords

Search

Navigation