Summary
We have previously provided evidence that the rat optic nerve contains three types of macroglial cells that develop as two distinct lineages: one lineage comprises type 1 astrocytes, which develop before birth, while the other comprises oligodendrocytes and type 2 astrocytes, which develop after birth from a common, bipotential glial progenitor cell. In the present study we have examined the influence of axons on the development of these two glial cell lineages by cutting the optic nerve at birth so that the retinal ganglion cell axons in the nerve degenerate. Using antibodies to distinguish the different types of glial cells in suspensions and semithin frozen sections of cut and uncut optic nerves, we show that neonatal transection results in a striking decrease in the total number of oligodendrocytes, type 2 astrocytes and their progenitor cells but has much less effect on the number of type 1 astrocytes. Since the [3H]thymidine labelling indices of oligodendrocytes and their progenitor cells were not significantly decreased in cut nerves, our results suggest that the progenitor cells and/or their progeny die in large numbers following neonatal nerve transection. We conclude that axons are required for the survival of cells of the oligodendrocyte-type 2 astrocyte lineage, at least during postnatal development.
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References
Abney, E., Williams, B. &Raff, M. C. (1983) Tracing the development of oligodendrocytes from precursor cells using monoclonal antibodies, fluorescence activated cell sorting and cell culture.Developmental Biology 100, 166–71.
Eisenbarth, G. S., Walsh, F. S. &Nirenberg, M. (1979) Monoclonal antibody to a plasma membrane antigen of neurons.Proceedings of the National Academy of Sciences, USA 76, 4913–17.
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.
Kuwabara, T. (1974) Development of the optic nerve of the rat.Investigative Ophthalmology 13, 732–45.
Lam, K., Sefton, J. &Bennett, M. R. (1982) Loss of axons from the optic nerve of the rat during early postnatal development.Developmental Brain Research 3, 487–91.
Miller, R. H. &Raff, M. C. (1984) Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct.Journal of Neuroscience 4, 585–92.
Noble, M. &Murray, K. (1984) Purified astrocytes promote thein vitro division of a bipotential glial progenitor cell.EMBO Journal 3, 2243–47.
Potts, R., Dreher, B. &Bennett, M. R. (1982) The loss of ganglion cells in the developing retina of the rat.Developmental Brain Research 3, 481–6.
Privat, A., Valat, J. &Fulcrand, J. (1981) Profileration of neuroglial cell lines in the degenerating optic nerve of young rats. A radioautographic study.Journal of Neuropathology and Experimental Neurology 40, 46–60.
Pruss, R. (1979) Thy-1 antigen on astrocytes in long-term cultures of rat central nervous system.Nature 280, 688–90.
Raff, M. C., Abney, E. R., Cohen, J., Lindsay, R. &Noble, M. (1983a) Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides and growth characteristics.Journal of Neuroscience 3, 1289–300.
Raff, M. C., Abney, E. R. &Miller, R. H. (1984) Two glial cell lineages diverge prenatally in rat optic nerve.Developmental Biology (in press).
Raff, M. C., Miller, R. H. &Noble, M. (1983b) A glial progenitor cell that developsin vitro into an astrocyte or an oligodendrocyte depending on the culture medium.Nature 303, 390–6.
Raff, M. C., Mirsky, R., Fields, K. L., Lisak, R., Dorfman, S. H., Silberberg, D. H., Gregson, N. A., Liebowitz, S. &Kennedy, M. (1978) Galactocerebroside: a specific cell surface antigenic marker for oligodendrocytes in culture.Nature 274, 813–16.
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.
Skoff, R., Price, D. &Stocks, A. (1976a) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. I. Cell proliferation.Journal of Comparative Neurology 169, 291–312.
Skoff, R., Price, D. &Stocks, A. (1976b) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. II. Time of origin.Journal of Comparative Neurology 169, 313–33.
Valat, J., Privat, A. &Fulcrand, J. (1983) Multiplication and differentiation of glial cells in the optic nerve of the postnatal rat.Anatomy and Embryology 167, 335–46.
Vaughn, J. E. (1969) An electron microscopic analysis of gliogenesis in rat optic nerves.Zeitschrift für Zellforschung und mikroskopische Anatomie 94, 293–324.
Vaughn, J. E. &Peters, A. (1967) Electron microscopy of the early postnatal development of fibrous astrocytes.American Journal of Anatomy 121, 131–52.
Wood, J. D. &Anderton, B. H. (1981) Monoclonal antibodies to mammalian neurofilaments.Bioscience Reports 1, 263–8.
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David, S., Miller, R.H., Patel, R. et al. Effects of neonatal transection on glial cell development in the rat optic nerve: evidence that the oligodendrocyte-type 2 astrocyte cell lineage depends on axons for its survival. J Neurocytol 13, 961–974 (1984). https://doi.org/10.1007/BF01148596
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DOI: https://doi.org/10.1007/BF01148596