Skip to main content
SpringerLink
Log in

Expression of galactocerebroside in developing normal and jimpy oligodendrocytesin situ

  • Published:
Journal of Neurocytology

Summary

Intense and specific immunostaining of oligodendrocytesin vivo has been obtained for the first time using antibodies to galactocerebroside. We have examined the differentiation of oligodendrocytes in normal mice and then compared their differentiation to the myelin-deficient mouse jimpy, using immunoperoxidase, immunogold and immunofluorescence labelling techniques. We also compared staining for galactocerebroside with staining obtained using antibodies to myelin basic protein, carbonic anhydrase II, 2′, 3′-cyclic nucleotide 3′-phosphohydrolase and proteolipid protein. The results of this comparative study confirm previous tissue culture studies and show that galactocerebroside is specific for oligodendrocytesin situ. As in tissue culture, galactocerebroside is one of the earliest oligodendrocyte markers to be expressed, making it an important marker for studying the differentiation of this cell type.

The shape of oligodendrocytesin situ changes distinctly with time, shifting from an early stellate form with numerous spidery processes to a cell with a few processes radiating from the perikaryon. These morphological changes are observed for both normal and jimpy mice and they parallel those describedin vitro. Oligodendrocytes in jimpy mice express most myelin markers, but the staining within the cells is generally less intense than in normal oligodendrocytes and the antigens are restricted to the cell body and processes without being incorporated into myelin sheaths. Quantification of the number of oligodendrocytes stained for galactocerebroside in normal and jimpy mice show that their number is not reduced in the corpus callosum and cerebellum during the first 2 weeks postnatal. This finding shows that many cells in jimpy mice which were considered to be unclassifiable by the application of morphological criteria have, in fact, differentiated to the stage where they are galactocerebroside-positive.

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

  • Barbarese, E., Carson, J. H. &Braun, P. E. (1979) Subcellular distribution and structural polymorphism of myelin basic protein in normal and jimpy mouse brain.Journal of Neurochemistry 32, 1437–46.

    PubMed  Google Scholar 

  • Bartlett, W. P., Knapp, P. E. &Skoff (1988) Glial conditioned medium enables jimpy oligodendrocytes to express properties of normal oligodendrocytes: production of myelin antigens and membranes.Glia (in press).

  • Benjamins, J. A., Callahan, R. E., Montgomery, I. N., Studzinski, D. M. &Dyer, C. A. (1987) Production and characterization of high titer antibody to galactocerebroside.Journal of Neuroimmunology 14, 325–38.

    PubMed  Google Scholar 

  • Benjamins, J. A., Skoff, R. P. &Beyer, K. (1984) Biochemical expression of mosaicisim in female mice heterogygous for the jimpy gene.Journal of Neurochemistry 42, 487–92.

    PubMed  Google Scholar 

  • Bologa-Sandru, L., Zalc, B., Herschkowitz, N. &Baumann, N. (1981) Oligodendrocytes of jimpy mice express galactosylceramide. An immunofluorescence study on brain sections and dissociated brain cell cultures.Brain Research 225, 425–30.

    PubMed  Google Scholar 

  • Borrelli, E., Langley, O. K., Ghandour, M. S., Delaunoy, J. P. &Gombos, G. (1982) Immunocytology of carbonic anhydrase II in the central nervous system of jimpy mutant mice.Neuroscience Letters 32, 321–7.

    PubMed  Google Scholar 

  • Campagnoni, A. T., Campagnoni, C. W., Bourre, J.-M., Jacque, C. &Baumann, N. (1984) Cell-free synthesis of myelin basic proteins in normal and dysmyelinating mutant mice.Journal of Neurochemistry 42, 733–9.

    PubMed  Google Scholar 

  • Druse, M. J. &Hogan, E. L. (1972) Metabolismin vivo of brain galactolipids: the jimpy mutant.Journal of Neurochemistry 19, 2435–41.

    PubMed  Google Scholar 

  • Dubois-Dalcq, M., Behar, T., Hudson, L. &Lazzarini, R. A. (1986) Emergence of three myelin proteins in oligodendrocytes cultured without neurons.Journal of Cell Biology 102, 384–92.

    PubMed  Google Scholar 

  • Farkas-Bargeton, E., Robain, O. &Mandel, P. (1972) Abnormal glial maturation in the white matter in jimpy mice.Acta neuropathologica 21, 272–81.

    PubMed  Google Scholar 

  • Ghandour, M. S., Langley, O. K., Vincendon, G. &Gombos, G. (1979) Double immunohistochemical technique provides evidence of the specificity of glial cell markers.Journal of Histochemistry and Cytochemsitry 27, 1634–7.

    Google Scholar 

  • Ghandour, M. S., Vincendon, G. &Gombos, G., (1980a) Astrocyte and oligodendrocyte distribution in adult rat cerebellum: an immunohistological study.Journal of Neurocytology 9, 637–46.

    PubMed  Google Scholar 

  • Ghandour, M. S., Vincendon, G., Gombos, G., Limozin, N., Filippi, D., Dalmaso, C. &Laurent, G. (1980b) Carbonic anhydrase and oligodendroglia in developing rat cerebellum: a biochemical and immunohistological study.Developmental Biology 77, 73–83.

    PubMed  Google Scholar 

  • Gumpel, M., Lachapelle, F., Baulac, M., Baron Van Evercooren, A., Lubetzki, C., Gansmuller, A., Lombrail, P., Jacque, C. &Baumann, N. (1987) Myelination in the mouse by transplanted oligodendrocytes. InGlia-Neuronal Communication in Development and Regeneration (edited byAlthaus, H. S. &Seifer, W.), pp. 818–30. Berlin: Springer-Verlag.

    Google Scholar 

  • Hartman, B. K., Agrawal, H. C., Agrawal, D. &Kalmbach, S. (1982) Development and maturation of central nervous system myelin: comparison of immunohistochemical localization or proteolipid protein and basic protein in myelin and oligodendrocytes.Proceedings of the National Academy of Sciences USA 79, 4717–20.

    Google Scholar 

  • Hertz, L., Chaban, G. &Hertz, E. (1980) Abnormal metabolic response to excess potassium in astrocytes from the jimpy mouse, a convulsing neurological mutant.Brain Research 181, 482–7.

    PubMed  Google Scholar 

  • Hogan, E. L., Joseph, K. C. &Schmidt, G., (1970) Composition of cerebral lipids in murine sudanophilic leukodystrophy: the Jimpy mutant.Journal of Neurochemistry 17, 75–83.

    PubMed  Google Scholar 

  • Hudson, L., Berndt, J. A., Puckett, C., Kozak, C. &Lazzarini, R. (1987) Aberrant splicing of proteolipid protein mRNA in -the dysmyelinating jimpy mutant mouse.Proceedings of the National Academy of Sciences USA 84, 1456–8.

    Google Scholar 

  • Jacque, C., Delassalle, A., Raoul, M. &Baumann, N. (1983) Myelin basic protein deposition in the optic and sciatic nerves of dysmyelinating mutants quaking, jimpy, trembler, MLD and shiverer during development.Journal of Neurochemistry 41, 1335–40.

    PubMed  Google Scholar 

  • Knapp, P. E., Bartlett, W, P. &Skoff, R. P. (1987a) Conditioned medium restores a normal phenotype to jimpy oligodendrocytes grownin vitro.Society for Neuroscience Abstracts 13, 888.

    Google Scholar 

  • Knapp, P. E., Bartlett, W. P. &Skoff, R. P. (1987b) Cultured oligodendrocytes mimicin vivo phenotypic characteristics: cell shape, expression of myelin specific antigens, and membrane production.Developmental Biology 120, 356–65.

    PubMed  Google Scholar 

  • Knapp, P. E., Skoff, R. P. &Redstone, D. W. (1986) Oligodendroglial cell death in jimpy mice: An explanation for the myelin deficit.Journal of Neuroscience 6, 2813–22.

    PubMed  Google Scholar 

  • Kraus-Ruppert, R., Herschkowitz, N. &Furst, S. (1973) Morphological studies on neuroglial cells in the corpus callosum of the jimpy mutant mouse.Journal of Neuropathology and Experimental Neurology 32, 197–203.

    PubMed  Google Scholar 

  • Kurihara, Z. T., Nussbaum, J. L. &Mandel, P. (1970) 2′3′-cyclic nucleotide 3′ phosphohydrolase in brains of mutant mice with deficient myelination.Journal of Neurochemistry 17, 993–7.

    PubMed  Google Scholar 

  • Matthieu, J. M., Widmer, S. &Herschkowitz, N. (1973) Jimpy, an anomaly of maturation: Biochemical studies of myelination phases.Brain Research 55, 403–12.

    PubMed  Google Scholar 

  • McCarthy, K. D. &DeVellis, J., (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue.Journal of Cell Biology 85, 890–902.

    PubMed  Google Scholar 

  • Meier, C. &Bischoff, A. (1975) Oligodendroglial cell development in jimpy mice and controls: An electron microscopic study in the optic nerve.Journal of the Neurological Sciences 26, 517–28.

    PubMed  Google Scholar 

  • Monge, M., Kadiiski, D. Jacque, C. M. &Zalc, B. (1986) Oligodendroglial expression and deposition of four major myelin constituents in the myelin sheath during development.Developmental Neuroscience 8, 222–35.

    PubMed  Google Scholar 

  • Morello, D., Dantigny, A., Pham-Dinh, D. &Jolles, P. (1986) Myelin proteolipid protein (PLP and DM-20) transcripts are deleted injimpy mutant mice.European Molecular Biology Organization Journal 5, 3489–93.

    Google Scholar 

  • Nave, K. A., Lai, C., Bloom, F. &Milner, R. (1986) Jimpy mouse mutant: A 74-base deletion in the mRNA for myelin proteolipid protein and evidence for a primary defect in RNA splicing.Proceedings of the National Academy of Sciences USA 83, 9264–8.

    Google Scholar 

  • Noble, M. &Murray, K. (1984) Purified astrocytes promote thein vitro division of a bipotential glial progenitor cell.European Molecular Biology Organization Journal 3, 2243–47.

    Google Scholar 

  • Norton, W. T. (1976) Formation, structure and biochemistry of myelin, InBasic Neurochemistry (edited bySiegel, G., Albers, W., Katzman, R. &Agranoff, B. W.), pp. 74–99. Boston: Little, Brown and Company.

    Google Scholar 

  • Nussbaum, J. L., Neskovic, N. &Mandel, P. (1969) Effect of the jimpy mutation on expression of myelin proteins in heterozygous and hemizygous mouse brain.Journal of Neurochemistry 16, 927–34.

    PubMed  Google Scholar 

  • Omlin, F. X. &Anders, J. J. (1983) Abnormal cell relationships in jimpy mice: electron microscopic and immunocytochemical findings.Journal of Neurocytology 12, 767–84.

    PubMed  Google Scholar 

  • Privat, A., Robain, O. &Mandel, P. (1972) Aspects ultrastructuraux du corps calleux chez la souris jimpy.Acta neuropathologica 21, 282–95.

    PubMed  Google Scholar 

  • Privat, A., Valat, J., Lachapelle, F., Baumann, N. &Fulcrand, J. (1982) Radioautographic evidence for protracted proliferation of glial cells in the central nervous system of jimpy mice.Developmental Brain Research 2, 411–16.

    Google Scholar 

  • Raff, M. C., Miller, R. H. &Noble, M. (1983) A glial progenitor cell that developsin vitro into an astrocyte or an oligodendrocyte depending on culture medium.Nature 303, 390–6.

    PubMed  Google Scholar 

  • Raff, M. C., Mirsky, R., Fields, K. L., Lisak, R. P., Dorfman, S. H., Silberberg, D. H., Gregson, N. A., Leibowitz, S. &Kennedy, M. C. (1978) Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture.Nature 274, 813–16.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Saneto, R. P. &Devellis, J. (1985) Characterization of cultured rat oligodendrocytes proliferating in a serum free, chemically defined medium.Proceedings of the National Academy of Sciences USA 82, 3509–13.

    Google Scholar 

  • Sarlieve, L. L., Farooqui, A. A., Rebel, G. &Mandel, P. (1976) Arysulfatase A and 2′, 3′-cyclic nucleotide 3′-phosphohydrolase activities in the brains of myelin deficient mutant mice.Neuroscience 1, 519–22.

    PubMed  Google Scholar 

  • Schachner, M., Kim, S. K. &Zehnle, R. (1981) Developmental expression in central and peripheral nervous system of oligodendrocyte cell surface antigens (0 antigens) recognized by monoclonal antibodies.Developmental Biology 83, 328–38.

    PubMed  Google Scholar 

  • Sidman, R. L., Dickie, M. M. &Appel, S. H. (1964) Mutant mice (quaking and jimpy) with deficient myelination in the central nervous system.Science 144, 209–11.

    Google Scholar 

  • Skoff, R. P. (1976) Myelin deficit in the jimpy mouse may be due to cellular abnormalities in astroglia.Nature 264, 560–2.

    PubMed  Google Scholar 

  • Skoff, R. P. (1981) Proliferation of oligodendroglial cells in normal animals and in a myelin deficient mutant-Jimpy. InGlial and Neuronal Cell Biology (edited byVidrio, A. &Fedoroff, S.), pp. 93–103. New York: Alan R. Liss.

    Google Scholar 

  • Skoff, R. P. (1982) Increased proliferation of oligodendrocytes in the hypomyelinated mouse mutant-jimpy.Brain Research 248, 19–31.

    PubMed  Google Scholar 

  • Skoff, R. P., Skoff, A. M. &Katsnelson, I. (1979) Neonatal endocrine abnormalities in myelin deficient jimpy-tabby mice.Life Sciences 24, 2099–104.

    PubMed  Google Scholar 

  • Sorg, B., Smith, M. M. &Campagnoni, A. (1987) Developmental expression of the myelin proteolipid protein and basic protein in RNAs in normal and dysmyelinating mutant mice.Journal of Neurochemistry 49, 1146–54.

    PubMed  Google Scholar 

  • Sternberger, N. H., Itoyama, Y., Kies, M. W. &Webster, H. de F. (1978) Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat CNS.Journal of Neurocytology 7, 251–63.

    PubMed  Google Scholar 

  • Sternberger, N. H. (1984) Patterns of oligodendrocyte function seen by immunocytochemistry. InOligodendroglia (edited byNorton, W.), pp. 125–73. New York: Plenum Press.

    Google Scholar 

  • Szuchet, S., Stefansson, K., Wollmann, R. L., Dawson, G. &Arnason, B. G. (1980) Maintenance of isolated oligodendrocytes in long-term culture.Brain Research 200, 151–64.

    PubMed  Google Scholar 

  • Yanagisawa, K. &Quarles, R. (1986) Jimpy mice: Quantitation of myelin associated glycoprotein and other proteins.Journal of Neurochemistry 47, 322–5.

    PubMed  Google Scholar 

  • Zalc, B., Monge, M., Dupouey, P., Hauw, J. J. &Baumann, N. A. (1981) Immunohistochemical localization of galactosyl and sulfogalactosyl ceramide in the brain of the 30-day-old mouse.Brain Research 211, 341–54.

    PubMed  Google Scholar 

  • Zeller, N. K., Behar, T. N., Dubois-Dal1cq, M. E. &Lazzarini, R. A. (1985) The timely expression of myelin basic protein gene in cultured rat brain oligodendrocytes is independent of continuous neuronal influences.Journal of Neuroscience 5, 2955–62.

    PubMed  Google Scholar 

  • Zimmerman, T. R., Jr &Cohen, S. R. (1979) The distribution of myelin basic protein in subcellular fractions of developing jimpy mouse brain.Journal of Neurochemistry 32, 817–21.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cell Biology, Wayne State University, School of Medicine, 540 E. Canfield Avenue, 48201, Detroit, MI, USA

    M. S. Ghandour & R. P. Skoff

Authors
  1. M. S. Ghandour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. P. Skoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Chargé de Recherche au CNRS Visiting Associate Professor at Wayne State University.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ghandour, M.S., Skoff, R.P. Expression of galactocerebroside in developing normal and jimpy oligodendrocytesin situ . J Neurocytol 17, 485–498 (1988). https://doi.org/10.1007/BF01189804

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01189804

Keywords

Search

Navigation