Skip to main content
Log in

Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination

  • Published:
Journal of Neurocytology

Summary

Nodes of Ranvier from normal and ‘dystrophic’ mice have been examined with quantitative freeze-fracture electron microscopy. Regions of nodal, paranodal and interparanodal axolemma of normal fibres are clearly distinguishable on the basis of particle size distributions in electron micrographs of freeze-fractured replicas. Protoplasmic fracture faces of normal nodes of Ranvier, contain approximately 40% 100 Å particles and about 25% elongated particles 150 by 250 Å. Paranodal and interparanodal membranes contain a more uniform distribution of smaller diameter particles. ‘Dystrophic’ mice of the 129/ReJ-Dy strain have a genetic defect of Schwann cell development and myelinogenesis. Axons of the sciatic and deep peroneal nerves in dystrophic mice, which appear to be normally myelinated, possess approximately the same distributions of particles as axons in normal mice. However, in affected regions of the ventral and dorsal roots, Schwann cell wrappings may be missing, creating heminodes of Ranvier where the myelination terminates or begins again. At such heminodes, there is a circular band of axonal membrane which bears particles of sizes and packing densities similar to that found at normal nodes. High voltage electron microscopic examination of 0.25–1 μm thick sections from these hemi-nodal regions reveals the presence of a filamentous layer beneath the particle-rich membrane. In addition, completely amyelinated regions of root axons contain particle patches having size-density distributions similar to that of both normal and hemi-nodal membranes. Thus, the nodal membrane displays a characteristic particle-size distribution profile. The occurrence of this particle profile does not appear to be dependent upon the presence or absence of Schwann cells. These observations suggest that the functions subserved by the numerous particles at the node of Ranvier are not dependent upon myelination for their local differentiation within the axonal membrane.

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

  • Agnew, W. S., Levinson, S. R., Brabson, J. S. andRaftery, M. A. (1978) Purification of the tetrodotoxin-binding component associated with the voltage-sensitive sodium channel fromElectrophorus electrieus electroplax membranes.Proceedings of the National Academy of Sciences (U.S.A.)75, 2606–10.

    Google Scholar 

  • Biscoe, T. J., Caddy, K., Pallot, D., Pherson, M. andStirling, C. A. (1974) The neurological lesion in the dystrophic mouse.Brain Research 76, 534–6.

    PubMed  Google Scholar 

  • Bradley, W. G. andJenkinson, M. (1973) Abnormalities of peripheral nerves in murine muscular dystrophy.Journal of the Neurological Sciences 18, 227–47.

    PubMed  Google Scholar 

  • Bray, G. M. andAguayo, A. J. (1975) Quantitative ultrastructural studies of the axon Schwann cell abnormality in spinal nerve roots from dystrophic mice.Journal of Neuropathology and Experimental Neurology 54, 517–30.

    Google Scholar 

  • Bray, G. M., Perkins, S., Peterson, A. L. andAguayo, A. J. (1977) Schwann cell multiplication deficit in nerve roots of new-born dystrophic mice: A radioautographic and ultrastructural study.Journal of the Neurological Sciences 32, 203–12.

    PubMed  Google Scholar 

  • Cragg, B. G. andThomas, P. K. (1957) The relationships between conduction velocity and the diameter and internodal length of peripheral nerve fibres.Journal of Physiology 136, 606–14.

    PubMed  Google Scholar 

  • Deguchi, N., Jongensen, P. L. andMaunsbach, A. B. (1977) Ultrastructure of the sodium pump.Journal of Cell Biology 75, 619–34.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Ellisman, M. H. (1977) High voltage electron microscopy of cortical specializations associated with membranes at nodes of Ranvier.Journal of Cell Biology 75, 108a.

    Google Scholar 

  • Ellisman, M. H., Brooke, M. H., Kaiser, K. K. andRash, J. E. (1977) Appearance in slow muscle sarcolemma of specializations characteristic of fast muscle after reinnervation by a fast muscle nerve.Experimental Neurology 58, 59–67.

    Google Scholar 

  • Ellisman, M. H., Rash, J. E., Staehelin, L. A. andPorter, K. R. (1976) Studies of excitable membranes. II. A comparison of specializations at neuromuscular junctions and non-junctional sarcolemmas of mammalian fast and slow twitch muscle fibres.Journal of Cell Biology 68, 752–74.

    PubMed  Google Scholar 

  • Friede, R. L. andSamorajski, T. (1967) Relation between the number of myelin lamellae and axon circumference in fibers of vagus and sciatic nerves of mice.Journal of Comparative Neurology 130, 223–31.

    PubMed  Google Scholar 

  • Gasser, H. S. (1955) Properties of dorsal root unmedullated fibers on two sides of the ganglion.Journal of General Physiology 38, 709–28.

    PubMed  Google Scholar 

  • Huxley, A. F. andStämpfli, R. (1949) Evidence for saltatory conduction in peripheral myelinated nerve fibres.Journal of Physiology 108, 315–39.

    Google Scholar 

  • Kristol, C., Akert, K., Sandri, C., Wyss, U. R., Bennett, M. V. L. andMoor, H. (1977) The Ranvier nodes in the neurogenic electric organ of the knifefishStenarchus: A freeze-etching study on the distribution of membrane-associated particles.Brain Research 125, 197–212.

    PubMed  Google Scholar 

  • Kristol, C., Sandri, C. andAkert, K. (1978) Intramembranous particles at the nodes of Ranvier of the cat spinal cord: A morphometric study.Brain Research 142, 391–400.

    PubMed  Google Scholar 

  • Kubo, M., Onot, S. andTasaki, I. (1954)The Microphysiology of Nerve (edited byKaro, G.), pp. 68–76. Tokyo: Mauruzen.

    Google Scholar 

  • Levinson, S. R. andEllory, J. C. (1973) Molecular size of the tetrodotoxin binding site estimated by irradiation inactivation.Nature New Biology 245, 122–3.

    PubMed  Google Scholar 

  • Livingston, R. B., Pfenninger, K., Moor, H. andAkert, 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.

    PubMed  Google Scholar 

  • Madrid, R. E., Jaros, E., Cullen, M. J. andBradley, W. G. (1975) Genetically determined defect of Schwann cell basement membrane in dystrophic mouse.Nature 257, 319–21.

    PubMed  Google Scholar 

  • Nonner, W., Rojas, E. andStämpfli, R. (1975) Gating currents in the node of Ranvier: Voltage and time dependence.Philosophical Transactions of the Royal Society (London)B270, 483–92.

    Google Scholar 

  • Peters, A. (1966) The node of Ranvier in the central nervous system.Quarterly Journal of Experimental Physiology 51, 229–39.

    Google Scholar 

  • Quick, D. C. andWaxman, S. G. (1977) Specific staining of the axon membrane at nodes of Ranvier with ferric ion and ferrocyanide.Journal of the Neurological Sciences 31, 1–11.

    PubMed  Google Scholar 

  • Rasminsky, M. (1977) Cross-talk between single fibres in spinal roots of dystrophic mice.Neurology 27, 394.

    Google Scholar 

  • Ritchie, J. M. andRogart, R. B. (1977) Density of sodium channels in mammalian myelinated nerve fibres and nature of the axonal membrane under the myelin sheath.Proceedings of the National Academy of Sciences (U.S.A.) 74, 211–5.

    Google Scholar 

  • Rosenbluth, J. (1976) Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain.Journal of Neurocytology 5, 731–45.

    PubMed  Google Scholar 

  • Schnapp, B., Peracchia, C. andMugnaini, E. (1973) Freeze-fracture of Ranvier nodes.Journal of Cell Biology 59, 360a.

    Google Scholar 

  • Schnapp, B., Peracchia, C. andMugnaini, E. (1976) The paranodal axo-glial junction in the central nervous system studied with thin sections and freeze-fracture.Neuroscience 1, 181–90.

    PubMed  Google Scholar 

  • Stämpfli, R. (1954) Saltatory conduction in nerve.Physiological Reviews 34, 101–12.

    PubMed  Google Scholar 

  • Stirling, C. A. (1974) Abnormalities in Schwann cell sheaths in spinal nerve roots of dystrophic mice.Journal of Anatomy 119, 169–80.

    Google Scholar 

  • Tasaki, I. (1959) Conduction of the nerve impulse. InHandbook of Physiology, Section 1, Vol. 1, (edited byField, J., Magoun, H. W. andHall, V. E.), pp. 75–121. Washington, D.C.: American Physiological Society.

    Google Scholar 

  • Thomas, P. K. (1955) Growth changes in the myelin sheath of peripheral nerve fibres.Proceedings of the Royal Society (London) B143, 380–91.

    Google Scholar 

  • Webster, H. deF. (1971) The geometry of peripheral myelin sheaths during their formation and growth in rat sciatic nerves.Journal of Cell Biology 48, 348–67.

    Google Scholar 

  • Webster, H. deF., Martin, J. R. andO'connell, M. F. (1973) The relationships between interphase Schwann cells and axons before myelination: A quantitative electron microscopic study.Developmental Biology 32, 401–16.

    PubMed  Google Scholar 

  • Wood, J. G., Jean, D. H., Whitaker, J. N., McLaughlin, B. J. andAlbers, R. W. (1977) Immunocytochemical localization of the sodium, potassium activated ATPase in knifefish brain.Journal of Neurocytology 6, 571–81.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ellisman, M.H. Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination. J Neurocytol 8, 719–735 (1979). https://doi.org/10.1007/BF01206672

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01206672

Keywords

Navigation