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Growth of nerve-cell body and myelinogenesis in mouse trigeminal ganglion and root: A combined cytofluorometric and morphometric study

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Journal of Neurocytology

Summary

Postnatal growth of mouse trigeminal ganglion cells and myelinogenesis in the central and peripheral portions of the trigeminal root were studied in animals aged 0–120 days. The trigeminal ganglion cells were dispersed into single cell suspensions. The growth of individual nerve cells was quantitated by measuring total protein content with a new cytofluorometric method based ono-phthaldialdehyde binding to cells fixed in a mixture of ethanol and acetic acid. White matter from the C.N.S. protrudes from the brainstem into the trigeminal root, and comes into direct contact with the P.N.S. in a transitional region. C.N.S. and P.N.S. myelinogenesis were studied in the same population of trigeminal sensory nerve fibres. Myelinogenesis was quantitated at the ultrastructural level by morphometric techniques.

A prominent peak in nerve cell body growth occurred between 3 and 6 days. Myelinogenesis in terms of established contacts between axons and their myelinating cells started at the same time in C.N.S. and P.N.S. and the transformation from nonmyelinated to promyelinated and myelinated fibres occurred concurrently in the central and peripheral parts of the trigeminal root. The growth of the myelin sheath, that is, the addition of myelin lamellae, was faster and more intense in P.N.S. than in C.N.S. This could reflect the fact that a Schwann cell myelinates only one internode, whereas an oligodendrocyte provides myelin for several internodes in different axons. These results support the concept of a common ‘signal’ for myelinogenesis in C.N.S. and P.N.S.

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References

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

    Google Scholar 

  • Aguayo, A. J., Dickson, R., Trecarten, J., Attiwell, M., Bray, G. M. &Richardson, P. (1978) Ensheathment and myelination of regenerating PNS fibres by transplanted optic nerve glia.Neurosdence Letters 9, 97–104.

    Google Scholar 

  • Andres, K. H. (1961) Untersuchungen über den Feinbau von Spinalganglien.Zeitschrift für Zellforschung und mikroskopische Anatomie 55, 1–48.

    Google Scholar 

  • Berthold, C.-H. &Carlstedt, T. (1977a) General organization of the transitional region in S1 dorsal rootlets.Acta Physiologica Scandinavica Suppl.446, 23–42.

    Google Scholar 

  • Berthold, C.-H. &Carlstedt, T. (1977b) A light microscopical and histochemical study of S1 dorsal rootlets in developing kittens.Acta Physiologica Scandinavica Suppl.446, 73–85.

    Google Scholar 

  • Blakemore, W. F. (1975) Remyelination by Schwann cells of axons demyelinated by intraspinal injection of 6-aminonicotinamide in the rat.Journal of Neurocytology 4, 745–57.

    PubMed  Google Scholar 

  • Bunge, R. P. &Bunge, M. B. (1978) Evidence that contact with connective tissue matrix is required for normal interaction between Schwann cells and nerve fibres.Journal of Cell Biology 78, 943–50.

    Google Scholar 

  • Carlstedt, T. (1977) A preparative procedure useful for electron microscopy of the lumbosacral dorsal rootlets.Acta Physiologica Scandinavica Suppl.446, 5–22.

    Google Scholar 

  • Droz, B., Di Giamberardino, L., Koenig, H. L., Boyenval, J. &Hassig, R. (1978) Axon-myelin transfer of phospholipid components in the course of their axonal transport as visualized by radioautography.Brain Research 155, 347–53.

    PubMed  Google Scholar 

  • Enerbäck, L. &Johansson, K.-A. (1973) Fluorescence fading in quantitative fluorescence microscopy: a cytofluorometer for the automatic recording of fluorescent peaks of very short duration.Histochemical Journal 5, 351–62.

    PubMed  Google Scholar 

  • Enerbäck, L., Kristensson, K. &Persson, L. A. (1979) Cytofluorometric quantitation of retrograde axonal transport in single dorsal root ganglia neurons.Experimental Cell Research 119, 399–403.

    PubMed  Google Scholar 

  • Fraher, J. P. (1972) A quantitative study of anterior root fibres during early myelination.Journal of Anatomy 112, 99–124.

    PubMed  Google Scholar 

  • Fraher, J. P. (1973) A quantitative study of anterior root fibres during early myelination. II. Longitudinal variation in sheath thickness and axon circumference.Journal of Anatomy 115, 421–44.

    PubMed  Google Scholar 

  • Fraher, J. P. (1976) The growth and myelination of central and peripheral segments of ventral motorneurone axons. A quantitative ultrastructural study.Brain Research 105, 193–211.

    PubMed  Google Scholar 

  • Fraher, J. P. (1978) Quantitative studies on the maturation of central and peripheral parts of individual ventral motorneuron axons.Journal of Anatomy 126, 509–33.

    PubMed  Google Scholar 

  • Friede, R. L. (1973) Principles of quantitative organization of peripheral nerve fibres and their relation to growth and pathologic changes.Zeitschrift für Neurologie 204, 243–54.

    Google Scholar 

  • Friede, R. L. &Bischhausen, R. (1978) How do axons control myelin formation? The model of 6-aminonicotinamide neuropathy.Journal of Neurological Sciences 35, 341–53.

    Google Scholar 

  • Friede, R. L. &Samorajski, T. (1968) Myelin formation in the sciatic nerve of the rat. A quantitative electron microscope, histochemical and radioautographic study.Journal of Neuropathology and Experimental Neurology 27, 546–71.

    PubMed  Google Scholar 

  • Gamble, H. J. (1976) Spinal and cranial nerve roots. InThe Peripheral Nerve (edited byLandon, D. N.), pp. 330–54. London: Chapman and Hall.

    Google Scholar 

  • Ghatak, N. R., Hirano, A., Doron, Y. &Zimmerman, H. M. (1973) Remyelination in multiple sclerosis with peripheral type myelin.Archives of Neurology 29, 262–7.

    Google Scholar 

  • Haley, J. E. &Ledeen, R. W. (1979) Incorporation of axonally transported substances into myelin lipids.Journal of Neurochemistry 32, 735–42.

    PubMed  Google Scholar 

  • Haltia, M. (1970) Postnatal development of spinal anterior horn neurons in normal and undernourished rats.Acta Physiologica Scandinavica Suppl.352, 1–70.

    Google Scholar 

  • Harding, I. (1949) The use of probability paper for the graphical analysis of polymodal frequency distributions.Journal of the Marine Biology Association 28, 140–53.

    Google Scholar 

  • Hillarp, N. A. &Olivecrona, H. (1946) The role played by the axon and the Schwann cells in the degree of myelination of the peripheral nerve fibre.Acta Anatomica 2, 17–32.

    Google Scholar 

  • Hirano, A., Zimmerman, H. M. &Levine, S. (1969) Electron microscopic observations of peripheral myelin in a central nervous system lesion.Acta Neuropathologica 12, 348–65.

    PubMed  Google Scholar 

  • Hökfelt, T., Kellerth, J.-O., Elde, R., Luft, R., Johansson, O., Nilsson, G., Pernow, B. &Arimura, A. (1976) Immunohistochemical studies on the distribution of substance-P and somatostatin in primary sensory neurons. InSensory Functions of the Skin in Primates (edited byZotterman, Y.), pp 583–602. Oxford: Pergamon Press.

    Google Scholar 

  • Honjin, R., Nakamura, T. &Nakamura, I. (1974) Electron microscopy of the central-peripheral transition of nerve fibres in the mouse trigeminal root.Archivum Histologicum Japonicum 36, 163–71.

    PubMed  Google Scholar 

  • Katzman, R., Broida, R. &Raine, C. S. (1978) Re-innervation, myelination and organization of iris tissue implanted into the rat midbrain — an ultrastructural study.Brain Research 138, 423–43.

    Google Scholar 

  • Kobayashi, T. (1963) Brain-to-body ratios and time of maturation of the mouse brain.American Journal of Physiology 204, 343–6.

    PubMed  Google Scholar 

  • Kristensson, K., Svennerholm, B., Persson, L. A., Vahlne, A. &Lycke, E. (1979) LatentHerpes simplex virus trigeminal ganglionic infection in mice and demyelination in the central nervous system.Journal of the Neurological Sciences 43, 253–64.

    PubMed  Google Scholar 

  • Kristensson, K., Vahlne, A., Persson, L. A. &Lycke, E. (1978) Neural spread ofHerpes simplex virus type 1 and 2 after corneal or subcutaneous (footpad) inoculation.Journal of the Neurological Sciences 35, 331–40.

    PubMed  Google Scholar 

  • Lawson, S. N. (1979) The postnatal development of large light and small dark neurons in mouse dorsal root ganglia: a statistical analysis of cell numbers and size.Journal of Neurocytology 8, 275–94.

    PubMed  Google Scholar 

  • Lieberman, A. R. (1976) Sensory ganglia. InThe Peripheral Nerve (edited byLandon, D. N.). pp. 188–278. London: Chapman and Hall.

    Google Scholar 

  • Martinez, J. A. &Friede, R. L. (1970) Changes in nerve cell bodies during the myelination of their axons.Journal of Comparative Neurology 138, 329–38.

    Google Scholar 

  • Matthieu, J.-M., Webster, H. de F., De Vries, G. H., Corthay, S. &Koellreutter, B. (1978) Glial versus neuronal origin of myelin proteins and glycoproteins studied by combined intraocular and intracerebral labelling.Journal of Neurochemistry 31, 93–102.

    PubMed  Google Scholar 

  • Meier, C. &Sollman, H. (1978) Glial outgrowth and central-type myelination of regenerating axons in spinal nerve roots following transection and suture: light and electron microscopic study in the pig.Neuropathology and Applied Neurobiology 4, 21–35.

    PubMed  Google Scholar 

  • Persson, L. A., Norlander, B. &Kristensson, K. (1978) Studies on hexachlorophene-induced myelin lesions in the trigeminal root transitional region in developing and adult mice.Acta Neuropathologica 42, 115–20.

    PubMed  Google Scholar 

  • Peters, A., Palay, S. &Webster, de F. H. (1976)The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: Saunders.

    Google Scholar 

  • Peterson, E. R. &Murray, M. R. (1955) Myelin sheath formation in cultures of avian spinalganglia.American Journal of Anatomy 96, 319–55.

    PubMed  Google Scholar 

  • Rundquist, I. &Enerbäck, L. (1976) Millisecond fading and recovery phenomena in fluorescent biological objects.Histochemistry 47, 79–87.

    PubMed  Google Scholar 

  • Sabri, M. I. &Davison, A. N. (1977) The synthesis of myelin in developing rat brain.Journal of Neurochemistry 29, 321–8.

    PubMed  Google Scholar 

  • Scheinberg, L. C., Taylor, J. M., Herzog, I. &Manuell, S. (1966) Optic and peripheral nerve response to triethyltin intoxication in the rabbit — Biochemical and ultrastructural studies.Journal of Neuropathology and Experimental Neurology 25, 202–13.

    PubMed  Google Scholar 

  • Simpson, S. A. &Young, J. Z. (1945) Regeneration of fibre diameter after cross-unions of visceral and somatic nerves.Journal of Anatomy 79, 48–65.

    Google Scholar 

  • Singer, M. (1968) Penetration of labelled amino acids into the peripheral nerve fibre from surrounding body fluids. InCiba Foundation Symposium. Growth of the Nervous System (edited byWolstenholme, G. andO'Connor, M.), pp. 98–126. London: Churchill.

    Google Scholar 

  • Speidel, C. C. (1964)In vivo studies of myelinated nerve fibres.International Review of Cytology 16, 174–233.

    Google Scholar 

  • Spencer, P. S. (1979) Neuronal regulation of myelinating cell function. InAspects of Developmental Neurobiology. Society for Neuroscience Symposia (edited byFerendelli, J. A.). Bethesda.

  • Spencer, P. S., Raine, C. S. &Wisniewski, H. M. (1973) Axon diameter and myelin sheath thickness — unusual relationships in dorsal root ganglia.Anatomical Record 176, 225–44.

    PubMed  Google Scholar 

  • Spencer, P. S. &Weinberg, H. J. (1978) Axonal specification of Schwann cell expression and myelination. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.), pp. 389–406. New York: Raven Press.

    Google Scholar 

  • Steer, J. M. (1971) Some observations on the fine structure of rat dorsal spinal nerve roots.Journal of Anatomy 109, 467–85.

    PubMed  Google Scholar 

  • Townsend, J. J. &Baringer, J. R. (1978a) Central nervous system susceptibility toHerpes simplex infection.Journal of Neuropathology and Experimental Neurology 37, 255–62.

    PubMed  Google Scholar 

  • Townsend, J. J. &Baringer, J. R. (1978b) Alteration ofHerpes simplex induced CNS lesions by immunosuppression.Journal of Neuropathology and Experimental Neurology 37, 701.

    Google Scholar 

  • Varon, S. S. &Bunge, R. P. (1978) Trophic mechanism in the peripheral nervous system.Annual Review of Neurosciences 1, 327–61.

    Google Scholar 

  • Webster, H. de F. (1975) Development of peripheral myelinated and unmyelinated nerve fibers. InPeripheral Neuropathy (edited byDyck, P. J., Thomas, P. andLambert, E. H.), Vol. 1, pp. 37–61. Philadelphia: Saunders.

    Google Scholar 

  • Weinberg, E. L. &Spencer, P. S. (1979) Studies on the control of myelinogenesis: 3. Signalling of oligodendrocyte myelination by regenerating peripheral axons.Brain Research 162, 273–79.

    PubMed  Google Scholar 

  • Weinberg, H. J. &Spencer, P. S. (1975) Studies on the control of myelinogenesis. I. Myelination of regenerating axons after entry into a foreign unmyelinated nerve.Journal of Neurocytology 4, 395–418.

    PubMed  Google Scholar 

  • Weinberg, H. J., Spencer, P. S. &Raine, C. S. (1975) Abberant PNS development in dystrophic mice.Brain Research 88, 532–7.

    PubMed  Google Scholar 

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  1. Division of Neuropathology, Department of Pathology, Karolinska Institutet, Huddinge Hospital, S-14186, Huddinge

    Lennart A. Persson

  2. Linköping University, Sweden

    Lennart A. Persson

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Persson, L.A. Growth of nerve-cell body and myelinogenesis in mouse trigeminal ganglion and root: A combined cytofluorometric and morphometric study. J Neurocytol 10, 169–182 (1981). https://doi.org/10.1007/BF01257965

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  • DOI: https://doi.org/10.1007/BF01257965

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