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Paranodal Schwann cell mitochondria in spinal roots of the cat. An ultrastructural morphometric analysis

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Journal of Neurocytology

Abstract

We have calculated the number of paranodal Schwann cell mitochondria in adult feline ventral and dorsal lumbar spinal roots using ultrastructural serial section analysis. Distinct accumulations of paranodal mitochondria were noted in nerve fibres more than 4-5 mm in diameter. The calculated number of paranodal mitochondria increased linearly with fibre diameter from a few hundred up to 20 000-30 000 per node. A linear increase in the number of paranodal mitochondria per node also appeared as a function of nodal variables such as ‘nodal axon membrane area’, ‘nodal Schwann cell membrane area’, and ‘node gap extracellular volume’. In large fibres (D=15-18 mm), a calculated number of about 20 000 paranodal Schwann cell mitochondria were accumulated at each node of Ranvier and related to nodal axon membrane area of about 20 mm2. Our calculations indicate that, on the average, 1000 paranodal Schwann cell mitochondria with a total volume of 6.7 mm3, a total outer membrane area of 250 mm2 and a total inner membrane area of 580 mm2 projected to each mm2 of the nodal axon membrane via the nodal Schwann cell brush border.

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References

  • Bergoffen, J., Scherer, S. S., Wang, S., Scott, M. O., Bone, L. J., Paul, D. L., Chen, K., Lensch, M. W., Chance, P. F. & Fischbeck, K. H. (1993) Connexin mutation in X-linked Charcot-Marie-Tooth disease. Science 262,2039-42.

    Google Scholar 

  • Berthold, C.-H. (1973) Histochemistry of postnatally developing feline spinal roots. II. Occurrence of acid phosphatase activity as studied by light and electron microscopical methods. Neurobiology 3,291-310.

    Google Scholar 

  • Berthold, C.-H., Corneliuson, O. & Rydmark, M. (1982a) Changes in the shape and size of cat spinal root myelinated nerve fibres during fixation and Vestopal-W embedding for electron microscopy. Journal of Ultrastructure Research 80,23-41.

    Google Scholar 

  • Berthold, C.-H., Fabricius, C., Rydmark, M. & AndersÉn, B. (1993) Axoplasmic organelles at nodes of Ranvier. I. Occurrence and distribution in large myelinated spinal roots axons of the adult cat. Journal of Neurocytology 22,925-40.

    Google Scholar 

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

    Google Scholar 

  • Berthold, C.-H. & Rydmark, M. (1983b) Anatomy of the paranode-node-para node region in the cat. Experientia 39,964-75.

    Google Scholar 

  • Berthold, C.-H. & Rydmark, M. (1995) Morphology of normal peripheral axons. In The Axon(edited by Waxman, S. G., Kocsis, J. D. & Stys, P. K.) pp. 13-48. Oxford: Oxford University Press.

    Google Scholar 

  • Berthold, C.-H., Rydmark, M. & Corneliuson, O. (1982b) Estimation of sectioning compression and thickness of ultrathin sections through Vestopal-W embedded cat spinal roots. Journal of Ultrastructure Research 80,42-52.

    Google Scholar 

  • Brismar, T. (1983) Nodal function of pathological nerve fibres. Experientia 39,946-53.

    Google Scholar 

  • Chiu, S. Y. (1991) Function and distribution of voltagegated sodium and potassium channels in mammalian Schwann cells. Glia 4, 541-58.

    Google Scholar 

  • Chiu, S. Y. (1995) Schwann cell function in saltatory conduction. In Neuroglia(edited by Kettenmann, H. & Ransom, B. R.) pp. 777-92. Oxford: Oxford University Press.

    Google Scholar 

  • Corneliuson, O., Berthold, C.-H., Fabricius, C., Gatzinsky, K. & Carlstedt, T. (1988) Marchi-positive myelinoid bodies at the transition between the central and the peripheral nervous system. Journal of Anatomy 163,17-31.

    Google Scholar 

  • deWaegh, S. & Brady, S. T. (1990) Altered slow axonal transport and regeneration in a myelin-deficient mutant mouse: The trembler as an in vivomodel for Schwann cell-axon interactions. Journal of Neuroscience 10,1855-65.

    Google Scholar 

  • deWaegh, S. & Brady, S. T. (1991) Local control of axonal properties by the Schwann cells: neurofilaments and axonal transport in homologous and heterologous nerve grafts. Journal of Neuroscience Research 30,201-12.

    Google Scholar 

  • deWaegh, S. M., Lee, V. M. & Brady, S. T. (1992) Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68,451-63.

    Google Scholar 

  • Dubois, J.-M. & Coulombe, A. (1984) Current-dependent inactivation of sodium depletion in normal and batrachotoxin-treated frog node of Ranvier. Journal of General Physiology 84,25-48.

    Google Scholar 

  • Ellisman, M. H., Friedman, P. L. & Hamilton, W. J. (1980) The localization of sodium and calcium to Schwann cell paranodal loops at nodes of Ranvier and of calcium to compact myelin. Journal of Neurocytology 9,185-205.

    Google Scholar 

  • Gatzinsky, K. P. (1996) Node-paranode regions as local degradative centers in alpha-motor axons. Microscopy Research and Technique 34,492-506.

    Google Scholar 

  • Gatzinsky, K. P. & Berthold, C.-H. (1990) Lysosomal activity at nodes of Ranvier during retrograde axonal transport of horseradish peroxidase in alphamotor neurons of the cat. Journal of Neurocytology 19,989-1002.

    Google Scholar 

  • Gatzinsky, K. P., Berthold, C.-H. & Rydmark, M. (1991) Axon-Schwann cell networks are regular components of nodal regions in normal large nerve fibres of cat spinal roots. Neuroscience Letters 124,264-8.

    Google Scholar 

  • Gatzinsky, K. P., Persson, H. & Berthold, C.-H. (1997) Removal of retrogradely transported material from rat lumbosacral alpha-motor axons by paranodal axon-Schwann cell networks. Glia 20,115-26.

    Google Scholar 

  • Griffiths, I. R., Mitchell, L. S., McPhilemy, K., Morrison, S., Kyriakides, E. & Barrie, J. A. (1989) Expression of myelin protein genes in Schwann cells. Journal of Neurocytology 18,345-52.

    Google Scholar 

  • Hildebrand, C. (1971) Ultrastructural and light-microscopical studies of the nodal region in large myelinated fibres of the adult feline spinal cord white matter. Acta Physiologica Scandinavica Suppl. 364,43-79.

    Google Scholar 

  • Landon, D. N. & Langley, O. K. (1971) The local chemical environment of nodes of Ranvier: a study of cation binding. Journal of Anatomy 108,419-32.

    Google Scholar 

  • Mi, H., Deerinck, T. J., Ellisman, L. H. & Schwartz, T. L. (1995) Differential distribution of closely related potassium channels in rat Schwann cells. Journal of Neuroscience 15,3761-74.

    Google Scholar 

  • Mi, H., Deerinck, T. J., Jones, M., Ellisman, L. H. & Schwartz, T. L. (1996) Inwardly rectifying K] channels that may participate in K] buffering are localized in microvilli of Schwann cells. Journal of Neuroscience 16,2421-9.

    Google Scholar 

  • Munn, E. A. (1974) The Sructure of Mitochondria.London: Academic Press.

    Google Scholar 

  • MÜller-Mohnssen, H., Tippe, A., Hillenkamp, F. & UnsÖld, E. (1975) Über die Bedeutung paranodaler Strukturen fÜr die Impulsregeneration am Ranvierschen Schnurring. Zeitschrift für Naturforschung 30c,271-7.

    Google Scholar 

  • Orkland, R. K., Nicholls, J. G. & Kuffler, S. W. (1964) Effect of nerve impulses on membrane potential of glial cells in the central nervous system of amphibia. Journal of Neurophysiology 29,788-806.

    Google Scholar 

  • Pannese, E., Ledda, M., Arcidiacono, G., Fratolla, D., Rigamonti, L. & Procacci, P. (1988) Qualitative and quantitative observations on the structure of the Schwann cells in myelinated fibres. Acta Anatomica 131,314-26.

    Google Scholar 

  • Persson, H., Berthold, C.-H., Rydmark, M., & Fabricius, C. (1992) Metabolic relationships between proteins of myelin and paranodally shedded, partially degraded myelin fragments in the rabbit CNS. Neuroscience Research 33,310-18.

    Google Scholar 

  • Prebble, J. N. (1981) Mitochondria, Chloroplasts and Bacterial Membranes.London: Longman.

    Google Scholar 

  • Price, R. L., Lasek, R. J. & Katz, M. J. (1990) Internal axonal cytoarchitecture is shaped locally by external compressive forces. Brain Research 530,205-14.

    Google Scholar 

  • Ritchie, J. E. (1995) Physiology of axons. In The Axon(edited by Waxman, S. G., Kocsis, J. D. & Stys, P. K.) pp. 68-96. Oxford: Oxford University Press.

    Google Scholar 

  • Robin, E. D. & Wong, R. (1988) Mitochondrial DNA molecules and virtual number of mitochondria per cell in mammalian cells. Journal of Cellular Physiology 136,507-13.

    Google Scholar 

  • RÖper, J. & Schwarz, J. R. (1989) Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres. Journal of Physiology 416,93-110.

    Google Scholar 

  • Rushton, W. A. H. (1951) A theory of the effect of fibre size in medullated nerve. Journal of Physiology 115,101-22.

    Google Scholar 

  • Rydmark, M. (1981) Nodal axon diameter correlates linearly with internodal axon diameter in spinal roots of the cat. Neuroscience Letters 24,247-50.

    Google Scholar 

  • Rydmark, M. & Berthold, C.-H. (1983) Electron microscopic serial section analysis of nodes of Ranvier in lumbar spinal roots of the cat: a morphometric study of nodal compartments in fibres of different sizes. Journal of Neurocytology 12,537-65.

    Google Scholar 

  • Salzer, J. L. (1997) Clustering sodium channels at the node of Ranvier: Close encounter of the axon-glia kind. Neuron 18,843-6.

    Google Scholar 

  • Spencer, P. S. & Thomas, P. K. (1974) Ultrastructural studies of the dying-back process. II. The sequestration and removal by Schwann cells and oligodendrocytes of organelles from normal and diseased axons. Journal of Neurocytology 3,763-83.

    Google Scholar 

  • Spray, D. C. & Dermietzel, R. (1995) X-linked dominant Charcot-Marie-Tooth disease and other potential gap-junction diseases of the nervous system. Trends in Neurosciences 18,256-62.

    Google Scholar 

  • Thomas, P. K., Berthold, C.-H. & Ochoa, J. (1993) Microscopic anatomy of the peripheral nervous system. In Peripheral Neuropathy, 3rd edn(edited by Dyck, P. J. & Thomas, P. K.), pp. 28-91. Philadelphia: W.B. Saunders.

    Google Scholar 

  • Tzagoloff, A. (1982) Mitochondria.New York: Plenum Press.

    Google Scholar 

  • Veltri, K. L., Espiritu, M. & Sing, G. (1990) Distinct genomic copy number in mitochondria of different mammalian organs. Journal of Cellular Physiology 143,160-4.

    Google Scholar 

  • Waxman, S. G. (1995) Voltage-gated channels in axons: Localization, function and development. In The Axon(edited by Waxman, S. G., Kocsis, J. D. & Stys, P. K.) pp. 218-43. Oxford: Oxford University Press.

    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-axonal junction at the node of Ranvier. Journal of Cell Biology 84,261-80.

    Google Scholar 

  • Williams, P. L. & Landon, D. N. (1964) The energy source of the nerve fibre. New Scientist 374,166-9.

    Google Scholar 

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Rydmark, M., Berthold, CH. & Gatzinsky, K.P. Paranodal Schwann cell mitochondria in spinal roots of the cat. An ultrastructural morphometric analysis. J Neurocytol 27, 99–108 (1998). https://doi.org/10.1023/A:1006995205504

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