Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve

Summary

There is evidence that oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells migrate along the developing rat optic nerve from the chiasm toward the eye before differentiating into oligodendrocytes that myelinate the retinal ganglion cell axons in the nerve. Why, then, do these progenitor cells not migrate into the eye, differentiate into oligodendrocytes and myelinate the nerve fibre layer of the retina? Myelination would opacify the neural retina and thereby severely impair vision. Here we provide evidence that there is a barrier at the eye-end of the rat optic nerve that prevents the migration of O-2A progenitor cells into the retina. Our findings in the rat support a previous hypothesis that such a barrier keeps myelin-forming glial cells out of the human retina.

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References

  1. BARBARESE, E., NEILSON, M. L. & CARSON, J. H. (1983) The effect of the shiverer mutation on myelin basic protein expression on homozygous and heterozygous mouse brain.Journal of Neurochemistry 40, 1680–6.

    PubMed  Google Scholar 

  2. BERLINER, M. L. (1931) Cytologic studies on the retina I. Normal coexistence of oligodendroglia and myelinated nerve fibres.Archives of Ophthalmology 6, 740–51.

    Google Scholar 

  3. BIGNAMI, A., ENC, L. F., DAHL, D. & UYEDA, C. T. (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence.Brain Research 43, 429–35.

    PubMed  Google Scholar 

  4. BLAKEMORE, W. F. & PATTERSON, R. C. (1975) Observations on the interactions of Schwann cells and astrocytes following X-irradiation of neonatal rat spinal cord.Journal of Neurocytology 4, 573–85.

    PubMed  Google Scholar 

  5. COHEN, J., BURNE, J. F., WINTER, J. & MCKINLAY, C. (1987) The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons.Developmental Biology 122, 407–18.

    PubMed  Google Scholar 

  6. DAVIS, F. A. (1929) The anatomy and histology of the eye and orbit of the rabbit.Transactions of the American Ophthalmological Society 27, 401–41.

    Google Scholar 

  7. EISENBARTH, G. S., WALSH, F. S. & NIRENBERG, M. (1979) Monoclonal antibody to plasma membrane antigen of neurons.Proceedings of the National Academy of Sciences USA 76, 4913–7.

    Google Scholar 

  8. FFRENCH-CONSTANT, C., MILLER, R. H., KRUSE, J., SCHACHNER, M. & RAFF, M. C. (1986) Molecular specialization of astrocyte processes at nodes of Ranvier in rat optic nerve.Journal of Cell Biology 102, 844–52.

    PubMed  Google Scholar 

  9. FFRENCH-CONSTANT, C. & RAFF, M. C. (1986a) Proliferating bipotential glial progenitor cells in adult rat optic nerve.Nature 319, 499–502.

    PubMed  Google Scholar 

  10. FFRENCH-CONSTANT, C. & RAFF, M. C. (1986b) The oligodendrocyte type-2 astrocyte cell lineage is specialized for myelination.Nature 323, 335–8.

    PubMed  Google Scholar 

  11. FINE, B. S. & YANOFF, M. (1979)Ocular History: A Text and Atlas, pp. 273–86. Hagerstown: Harper and Row.

    Google Scholar 

  12. FLAGE, T. (1977) Permeability properties of the tissues in the optic nervehead of the rabbit and monkey: an ultrastructural study.Acta ophthalmologica 55, 652–64.

    PubMed  Google Scholar 

  13. HILDEBRAND, C., REMAHL, S. & WAXMAN, S. G. (1985) Axo-glial relations in the retina—optic nerve junction of the adult rat: electron-microscopic observations.Journal of Neurocytology 14, 597–617.

    PubMed  Google Scholar 

  14. JOHNSON, G. D., DAVIDSON, R. S., MCNAMEE, K. C., RUSSELL, G., GOODWIN, D. & HOLBOROW, E. J. (1982) Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy.Journal of Immunological Methods 55, 231–42.

    PubMed  Google Scholar 

  15. KISTLER, H. B. & LAVAIL, J. H. (1981) Penetration of horseradish peroxidase into the optic nerve after vitreal or vascular injections in the developing chick.Investigative Ophthalmology and Visual Science 20, 705–16.

    PubMed  Google Scholar 

  16. KRUSE, J., KREILHAUER, G., FAISSNER, A., TIMPL, R. & SCHACHNER, M. (1985) The J1 glycoprotein — a novel nervous system cell adhesion molecule of the L2/HNK-1 family.Nature 316, 146–8.

    PubMed  Google Scholar 

  17. LACHAPELLE, F., GUMPEL, M., BAULAC, M., JACQUE, C., DUE, P. & BAUMANN, N. (1984) Transplantation of CNS fragments into the brain of shiverer mutant mice: extensive myelination by implanted oligodendrocytes. I. Immunological studies.Developmental Neuroscience 6, 325–34.

    Google Scholar 

  18. LEVI, G., GALLO, V., WILKIN, G. P. & COHEN, J. (1986) Astrocyte subpopulations and glial precursors in rat cerebellar cell cultures.Advances in Bioscience 61, 21–30.

    Google Scholar 

  19. LEVINE, J. & CARD, J. P. (1987) Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: association with protoplasmic astrocytes.Journal of Neuroscience 7, 2711–20.

    PubMed  Google Scholar 

  20. LEVINE, J. & STALLCUP, W. (1987) Plasticity of developing cerebellar cellsin vitro studied with antibodies against the NG2 antigen.Journal of Neuroscience 7, 2721–31.

    PubMed  Google Scholar 

  21. MAXWELL, D. S. & KRUGER, L. (1965) The fine structure of astrocytes in the cerebral cortex and their response to focal injury produced by heavy ionizing particles.Journal of Cell Biology 25, 141–57.

    Google Scholar 

  22. MCLEAN, I. W. & NAKANE, P. K. (1974) Periodate—lysine—periodate: a new fixative for immunoelectron microscopy.Journal of Histochemistry and Cytochemistry 22, 1077–83.

    PubMed  Google Scholar 

  23. MILLER, R. H., ABNEY, E. R., DAVID, S., FFRENCH-CONSTANT, C., LINDSAY, R., PATEL, R., STONE, J. & RAFF, M. C. (1986) Is reactive gliosis a property of a distinct subpopulation of astrocytes?Journal of Neuroscience 6, 22–9.

    PubMed  Google Scholar 

  24. MILLER, R. H., DAVID, S., PATEL, R., ABNEY, E. R. & RAFF, M. C. (1985) A quantitative immunohistochemical study of macroglial cell development in the rat optic nerve:in vivo evidence for two distinct astrocyte lineages.Developmental Biology 111, 35–41.

    PubMed  Google Scholar 

  25. MILLER, R. H. & RAFF, M. C. (1984) Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct.Journal of Neuroscience 4, 585–92.

    PubMed  Google Scholar 

  26. NARANG, H. K. & WISNIEWSKI, H. M. (1977) The sequence of myelination in the epiretinal portion of the optic nerve in the rabbit.Neuropathology and Applied Neurobiology 3, 15–27.

    Google Scholar 

  27. NICHOLLS,. J. V. V. & TANSLEY, K. (1938) Colobomata of the optic nerve sheath in rats.British Journal of Ophthalmology 22, 165–8.

    Google Scholar 

  28. NOBLE, M. & MURRAY, K. (1984) Purified astrocytes promote thein vitro division of a bipotential glial progenitor cell.EMBO Journal 3, 2243–7.

    PubMed  Google Scholar 

  29. PRUSS, R. (1979) Thy-1 antigen on astrocytes in long-term cultures of rat central nervous system.Nature 280, 688–90.

    PubMed  Google Scholar 

  30. 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.

    PubMed  Google Scholar 

  31. RAFF, M. C., ABNEY, E. R. & FOK-SEANG, J. (1985) Reconstitution of a developmental clockin vitro: a critical role for astrocytes in the timing of oligodendrocyte differentiation.Cell 42, 61–9.

    PubMed  Google Scholar 

  32. RAFF, M. C., ABNEY, E. R. & MILLER, R. H. (1984a) Two glial cell lineages diverge prenatally in rat optic nerve.Developmental Biology 106, 53–60.

    PubMed  Google Scholar 

  33. RAFF, M. C., FIELDS, K. L., HAKOMORI, S.-I., MIRSKY, R., PRUSS, R. M. & WINTER, J. (1979) Cell-type-specific markers for distinguishing and identifying neurons and the major classes of glial cells in culture.Brain Research 174, 283–308.

    PubMed  Google Scholar 

  34. RAFF, M. C. & MILLER, R. H. (1984) Glial cell development in the rat optic nerve.Trends in Neuroscience 7, 469–72.

    Google Scholar 

  35. 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.

    PubMed  Google Scholar 

  36. RAFF, M. C., MIRSKY, R., FIELDS, K. L., LISAK, R. P., 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, 813–6.

    PubMed  Google Scholar 

  37. RAFF, M. C., WILLIAMS, B. P. & MILLER, R. H. (1984b) Thein vitro differentiation of a bipotential glial progenitor cell.EMBO Journal 3, 1857–64.

    PubMed  Google Scholar 

  38. RANSCHT, B., CLAPSHAW, P. A., PRICE, J., NOBLE, M. & SIEFERT, 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 

  39. REYNERS, H., GIANFELICI DE REYNERS, E. & MAISIN, J.-R. (1982) The beta astrocyte: a newly recognized radiosensitive glial cell type in the cerebral cortex.Journal of Neurocytology 11, 967–83.

    PubMed  Google Scholar 

  40. REYNERS, H., GIANFELICI DE REYNERS, E. REGNIERS, L. & MAISIN, J.-R. (1986) A glial progenitor cell in the cerebral cortex of the adult rat.Journal of Neurocytology 15, 53–61.

    PubMed  Google Scholar 

  41. ROACH, A., BOYLAN, K., HORVATH, S., PRUSINER, S. B. & HOOD, I. E. (1983) Characterization of clones of cDNA representing ray myelin basic protein: absence of expression in brain of shiverer mutant mice.Cell 34, 799–806.

    PubMed  Google Scholar 

  42. ROACH, A., TAKAHASHI, N., PRAVTCHEVA, D. & HOOD, L. (1985) Chromosomal mapping of mouse myelin basic protein gene and structure and transcription of the partially deleted gene in shiverer mutant mice.Cell 42, 149–55.

    PubMed  Google Scholar 

  43. ROUGON, G., HIRSCH, M. R., HIRN, M., GUENET, J. L. & GORIDIS, C. (1983) Monoclonal antibody to neural cell surface protein: identification of a glycoprotein family of restricted cellular localization.Neuroscience 10, 511–20.

    PubMed  Google Scholar 

  44. SCHNITZER, J. (1985) Distribution and immunoreactivity of glia in the retina of the rabbit.Journal of Comparative Neurology 240, 128–42.

    PubMed  Google Scholar 

  45. SCHNITZER, J. (1986) Developmental expression of glial markers in the retina of rabbit.Abstracts of the Society for Neuroscience 12, 396.

    Google Scholar 

  46. SKOFF, R., KNAPP, P. E. & BARTLETT, W. P. (1986) Astrocyte diversity in the optic nerve: a cytoarchitectural study, InAstrocytes, Vol. I (edited by FEDOROFF, S. & VERNADAKIS, A.), pp. 269–91. New York: Academic Press.

    Google Scholar 

  47. SMALL, R. K. (1986) Evidence that progenitor cells of the oligodendrocyte type-2 astrocyte lineage migrate into the developing rat optic nerve.Abstracts of the Society for Neuroscience 12, 183.

    Google Scholar 

  48. SMALL, R. K., RIDDLE, P. & NOBLE, M. (1987) Evidence for migration of oligodendrocyte type-2 astrocyte progenitor cells into the developing rat optic nerve.Nature 329, 155–7.

    Google Scholar 

  49. SOMMER, I. & SCHACHNER, M. (1981) Monoclonal antibodies (O1 to O4) for oligodendrocyte cell surfaces: an immunological study in the central nervous system.Developmental Biology 83, 311–27.

    PubMed  Google Scholar 

  50. SOMMER, I. & SCHACHNER, M. (1982) Cells that are O4 antigen-positive and O1 antigen-negative differentiate into O1 antigen-positive oligodendrocytes.Neuroscience Letters 29, 183–8.

    PubMed  Google Scholar 

  51. SOMMER, I. & NOBLE, M. (1986) Plasticity and commitment in oligodendrocyte development.Abstracts of the Society for Neuroscience 12, 1585.

    Google Scholar 

  52. STONE, J. & DREHER, Z. (1987) Relationship between astrocytes and ganglion cells and vasculature of the retina.Journal of Comparative Neurology 255, 35–49.

    PubMed  Google Scholar 

  53. TSO, M. O. M., SHIH, C.-Y. & MCLEAN, M. I. W. (1975) Is there a blood—brain barrier at the optic nerve head?Archives of Ophthalmology 93, 815–25.

    PubMed  Google Scholar 

  54. VAUGHN, J. E. & PEASE, D. C. (1970) Electron microscopic studies of Wallerian degeneration in rat optic nerves II. Astrocytes, oligodendrocytes and adventitial cells.Journal of Comparative Neurology 140, 207–26.

    PubMed  Google Scholar 

  55. WEINBERG, E. I. & SPENCER, P. S. (1979) Studies on the control of myelinogenesis. III. Signalling of oligodendrocyte myelination by regenerating peripheral axons.Brain Research 162, 273–9.

    PubMed  Google Scholar 

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Ffrench-Constant, C., Miller, R.H., Burne, J.F. et al. Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. J Neurocytol 17, 13–25 (1988). https://doi.org/10.1007/BF01735374

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Keywords

  • Retina
  • Progenitor Cell
  • Glial Cell
  • Optic Nerve
  • Nerve Fibre