Summary
Histochemical and electron microscopical studies have shown that Marchi-positive bodies in the normal mammalian CNS are associated with paranodal regions and it has been proposed that the formation of Marchi-positive bodies represents a step in the catabolic events of normal myelin turnover. After a two-step density gradient ultracentrifugation a light ‘floating fraction’ highly enriched in these structures can be collected and in the present study two monoclonal antibodies, FC4 and 3B5, were produced against proteins present in the floating fraction but absent from the myelin fraction. Immunohistochemical studies showed that these antibodies bound preferentially to the PNS-CNS transitional region and the glia limitans. Double-staining experiments demonstrated an extensive overlap in these regions with cells stained by antibodies against the astrocyte marker glial fibrillary acidic protein. Centrally in the white matter, FC4 and 3B5 mainly stained cells which also stained with the microglia lectin markerBandeiraea simplicifolia isolectin B4. Three-dimensional reconstructions made from confocal microscopic scans showed that FC4/3B5-positive cells in the white matter extend processes enveloping paranodal Marchi-positive bodies and nodes of Ranvier. It is suggested that astrocyte-like and microglia-like cells both are participants in paranodal myelin turnover and that a division of labour with respect to, for example, protein degradation and immunological functions, may be present between the two cell types.
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References
Ashwell, K. (1989) Development of microglia in the albino rabbit retina.Journal of Comparative Neurology 287, 286–301.
Berlet, H. H., Ilzenhöfer, H. &Kaefer, M. (1988) Soluble and bound acid protease activity of myelin from bovine cerebral white matter and spinal cord.Neurochemical Research 13, 409–16.
Berthold, C.-H. (1973) Histochemistry of postnatally developing feline spinal roots. I. A study with the ‘OTAN’ method.Neurobiology 3, 275–90.
Berthold, C.-H. (1974) A comparative morphological study of the developing node-paranode region in lumbar spinal roots. II. Light microscopy after ‘OTAN’ staining.Neurobiology 4, 117–31.
Berthold, C.-H. &Carlstedt, T. (1977a) Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. III. Myelinated fibres in S1 dorsal rootlets.Acta Physiologica Scandinavica 446 (Supplement), 43–60.
Berthold, C.-H. &Carlstedt, T. (1977b) A light microscopical and histochemical study of S1 dorsal rootlets in developing kittens.Acta Physiologica Scandinavica 446 (Suppl.), 73–85.
Berthold, C.-H., Carlstedt, T. &Corneliuson, O. (1984) Anatomy of the nerve root at the central-peripheral transitional region. InPeripheral Neuropathy, 2nd edn. (edited byDyck, P. J., Thomas, P. K., Lambert, E. H. &Bunge, R.) pp. 156–70. Philadelphia: Saunders.
Bignami, A., Eng, L. F., Dahl, D. &Uyeda, C. T. (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence.Brain Research 43, 429–35.
Black, J. A. &Waxman, S. G. (1988) The perinodal astrocyte.Glia 1, 169–89.
Black, J. A., Waxman, S. G., Friedman, B., Elmer, L. M. &Angelides, K. J. (1989) Sodium channels in astrocytes of rat optic nervein situ: immuno-electron microscopic studies.Glia 2, 353–69.
Borgeson, M., Tallent, M. W. &Keane, R. W. (1989) Astrocyte modulation of central nervous system immune responses. InNeuroimmune Networks (edited byGoetzl, E. J. &Spector, N. H.) pp. 51–5. New York: Alan R. Liss.
Caspi, R. R. &Roberge, F. G. (1989) Glial cells as suppressor cells: characterization of the inhibitory function.Journal of Autoimmunity 2, 709–22.
Cook, R. D. &Wisniewski, H. M. (1973) The role of oligodendroglia and astroglia in Wallerian degeneration of the optic nerve.Brain Research 61, 191–206.
Corneliuson, O., Berthold, C.-H. &Fredman, P. (1987) Isolation of myelinoid Marchi-positive bodies from normal rabbit spinal cord.Brain Research 416, 43–53.
Corneliuson, O., Berthold, C.-H., Fabricius, C., Gatzinsky, K. &Carlstedt, T. (1988a) Marchi-positive myelinoid bodies at the transition between the central and the peripheral nervous system.Journal of Anatomy 163, 17–31.
Corneliuson, O., Berthold, C.-H., Persson, H. &Fredman, P. (1988b) Aspects on the protein and the lipid composition of myelinoid Marchi-positive bodies from mammalian spinal cord.Neurochemical Research 13, 1149–56.
Epstein, L. G., Prineas, J. W. &Raine, C. S. (1983) Attachment of myelin to coated pits on macrophages in experimental allergic encephalomyelitis.Journal of the Neurological Sciences 61, 341–8.
Fulcrand, J. &Privat, A. (1977) Neuroglial reactions secondary to Wallerian degeneration in the optic nerve of the postnatal rat; ultrastructural and quantitative study.Journal of Comparative Neurology 176, 189–224.
Franson, P. &Ronnevi, L-O. (1989) Myelin breakdown in the posterior funiculus of the kitten after dorsal rhizotomy: a qualitative and quantitative light and electron microscopic study.Anatomy and Embryology 180, 273–80.
Frohman, E. M., Frohman, T. C., Dustin, M. L., Vayuvegula, B., Choi, B., Gupta, A., Van Den Noort, S. &Gupta, S. (1989) The induction of intercellular adhesion molecule 1 (ICAM 1) expression on human fetal astrocytes by interferon-γ, tumor necrosis factor α, lymphotoxin and interleukin 1: relevance to intracerebral antigen presentation.Journal of Neuroimmunology 23, 117–24.
Galfré, G. &Milstein, C. (1981) Preparation of monoclonal antibodies: strategies and procedures.Methods of Enzymology 73, 3–47.
Hickey, W. F. &Kimura, H. (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigenin vivo.Science 239, 290–2.
Hildebrand, C. (1977) Presence of Marchi-positive myelinoid bodies in the spinal cord white matter of some vertebrate species.Journal of Morphology 153, 1–22.
Hildebrand, C. (1982) Electron-microscopic identification of Gomori-positive rings in normal spinal cord white matter.Acta Neuropathologica 56, 29–34.
Hildebrand, C. &Skoglund, S. (1971) Histochemical studies of adult and developing feline spinal cord white matter.Acta Physiologica Scandinavica 364 (Supplement), 145–73.
Koeppen, A. H. (1985) Wallerian degeneration. InHandbook of Neurochemistry, Vol. 7, 2nd edn (edited byLajtha, A.) pp. 443–506. New York and London: Plenum Press.
Lassman, H., Ammerer, H. P. &Kulnig, W. (1978) Ultrastructural sequence of myelin degradation.Acta Neuropathologica 102, 91–102.
Lee, S. C., Wayne Moore, G. R., Golenwsky, G. &Raine, C. S. (1990) Multiple sclerosis: a role for astroglia in active demyelination suggested by class II MHC expression and ultrastructural study.Journal of Neuropathology and Experimental Neurology 49, 122–36.
Levich, J. D., Signorella, A. P., Wittenberg, G. &Weigle, W. O. (1987) Macrophage handling of a tolerogen and the role of IL 1 in tolerance induction in a T cell clonein vitro.Journal of Immunology 138, 3675–9.
Ling, E. A., Wong, W. C., Yick, T. Y. &Leong, S. K. (1986) Ultrastructural changes in the dorsal motor nucleus of monkey following lateral cervical vagotomy.Journal of Neurocytology 15, 1–15.
Lowe, J., Maclennan, K. A., Powe, D. G., Pound, J. D. &Palmer, J. B. (1989) Microglial cells in human brain have phenotypic characteristics related to possible function as dendritic antigen-presenting cells.Journal of Pathology 159, 143–9.
Markmann, J., Lo, D., Naji, A., Palmiter, R. D., Brinster, R. L. &Heber-Katz, E. (1988) Antigen presenting function of class II MHC-expressing beta-cells.Nature 336, 476–9.
Norton, W. T. &Poduslo, S. E. (1973) Myelination in rat brain: method of myelin isolation.Journal of Neurochemistry 21, 749–57.
Persson, H. &Corneliuson, O. (1989) Presence of degradation products of myelin in a light CNS subcellular fraction.Neurochemical Research 12, 1177–80.
Peterson, G. L. (1983) Determination of total protein.Methods of Enzymology 91, 95–119.
Ranscht, B., Clapshaw, P. A., Price, J., Noble, M. &Seifert, W. (1982) Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside.Proceedings of the National Academy of Sciences (USA)79, 2709–13.
Sasaki, A., Levinson, S. W. &Ting, J. P-Y. (1989) Comparison and quantitation of Ia antigen expression on cultured macroglia and ameboid microglia from Lewis rat cerebral cortex: analyses and implications.Journal of Neuroimmunology 25, 63–74.
Stoll, G., Trapp, B. D. &Griffin, J. W. (1989) Macrophage function during Wallerian degeneration of rat optic nerve.Journal of Neuroscience 9, 2327–35.
Streit, W. J., Graeber, M. B. &Kreutzberg, G. W. (1989) Expression of Ia antigen on perivascular and microglial cells after sublethal and lethal motor neuron injury.Experimental Neurology 105, 115–26.
Streit, W. J. &Kreutzberg, G. W. (1987) Lectin binding by resting and active microglia.Journal of Neurocytology 16, 249–60.
Strich, S. J. (1968) Notes on the Marchi method for staining degenerating myelin in the peripheral and central nervous system.Journal of Neurology, Neurosurgery and Psychiatry 31, 110–14.
Towbin, H., Staehelin, T. &Gordon, J. (1979) Electrophoretic transfer of proteins from acrylamide gels to nitrocellulose sheets: procedure and some applications.Proceedings of the National Academy of Sciences (USA)76, 4350–4.
Wekerle, H., Sun, D., Oropeza-Wekerle, R. L. &Meyermann, R. (1987) Immune reactivity in the nervous system: modulation of T-lymphocyte activation of glial cells.Journal of Experimental Biology 132, 43–57.
Whitham, R. H., Vandenbark, A. A., Bourdette, D. N., Chou, Y. K. &Offner, H. (1990) Suppressor cell regulation of encephalitogenic T cell lines: generation of suppressor macrophages with cyclosporin A and myelin basic protein.Cellular Immunology 126, 290–303.
Wray, W., Boulikas, T., Wray, V. P. &Hancock, R. (1981) Silver staining of proteins in polyacrylamide gels.Analytical Biochemistry 118, 197–203.
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Persson, H., Berthold, C.H. Cellular relationships of paranodal Marchi-positive bodies studied with monoclonal antibodies against partially degraded CNS myelin fragments. J Neurocytol 20, 277–289 (1991). https://doi.org/10.1007/BF01235545
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DOI: https://doi.org/10.1007/BF01235545