Summary
We have examined the behaviourin vivo of regenerating PNS axons in the presence of grafts of optic nerve taken from the Browman-Wyse mutant rat. Browman-Wyse optic nerves are unusual because a 2–4 mm length of the proximal (retinal) end of the nerve lacks oligodendrocytes and CNS myelin and therefore retinal ganglion cell axons lying within the proximal segment are unmyelinated and ensheathed by processes of astrocyte cytoplasm. Schwann cells may also be present within some proximal segments. Distally, Browman-Wyse optic nerves are morphologically and immunohistochemically indistinguishable from control optic nerves.
When we grafted intact Browman-Wyse optic nerves or ‘triplets’ consisting of proximal, junctional and distal segments of Browman-Wyse optic nerve between the stumps of freshly transected sciatic nerves, we found that regenerating axons avoided all the grafts which did not contain Schwann cells, i.e., proximal segments which contained only astrocytes; regions of Schwann cell-bearing proximal segments which did not contain Schwann cells; junctional and distal segments (which contained astrocytes, oligodendrocytes and CNS myelin debris). However, axons did enter and grow through proximal segments which contained Schwann cells in addition to astrocytes. Schwann cells were seen within grafts even after mitomycin C pretreatment of sciatic proximal nerve stumps had delayed outgrowth of Schwann cells from the host nerves; we therefore conclude that the Schwann cells which became associated with regenerating axons within the grafts of Browman-Wyse optic nerve were derived from an endogenous population. Our findings indicate that astrocytes may be capable of supporting axonal regeneration in the presence of Schwann cells.
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Aguayo, A. J., Dickson, R., Trecarten, J., Attiwell, M., Bray, G. M. &Richardson, P. (1978) Ensheathment and myelination of regenerating PNS fibres by transplanted optic nerve glia.Neuroscience Letters 9, 97–104.
Berry, M., Rees, L. &Sievers, J. (1986a) Regeneration of axons in the mammalian visual system.Brain Research (Suppl)13, 18–33.
Berry, M., Rees, L. &Sievers, J. (1986b) Unequivocal regeneration of rat optic nerve axons into sciatic nerve isografts. InNeural Tissue Transplantation Research (edited byWallace, R. &Das, G.) pp. 63–79. New York: Springer.
Berry, M., Hall, S., Follows, R., Rees, L., Gregson, N. &Sievers, J. (1988) Response of axons and glia at the site of anastomosis between the optic nerve and cellular and acellular sciatic nerve grafts.Journal of Neurocytology 17, 727–44.
Berry, M., Hall, S., Follows, R. &Wyse, J. P. (1989) Defective myelination in the optic nerve of the Browman- Wyse (BW) mutant rat.Journal of Neurocytology 18, 141–59.
Berry, M., Hall, S., Rees, L. &Carlisle, J. (1992) Regeneration of axons in the optic nerve of the adult Browman-Wyse (BW) mutant rat.Journal of Neurocytology 21, 426–48.
Blakemore, W. F., Crang, A. J. &Curtis, R. (1986) The interaction of Schwann cells with CNS axons in regions containing normal astrocytes.Acta Neuropathologica 71, 295–300.
Caroni, P. &Schwab, M. (1988) Antibody against myelin associated inhibitor of neurite growth neutralises non- permissive substrate properties of CNS white matter.Neuron 1, 85–96.
David, S., Bouchard, C., Tstatas, O. &Giftochristos, N. (1990) Macrophages can modify the nonpermissive nature of the adult mammalian central nervous system.Neuron 5, 463–9.
Eng, L. F., Reier, P. J. &Houle, J. D. (1987) Astrocyte activation and fibrous gliosis: glial fibrillary acidic protein CNS tissue.Progress in Brain Research 71, 439–55.
Fawcett, J. W., Housden, E., Smith-Thomas, L. &Meyer, R. L. (1989) The growth of axons in three- dimensional astrocyte cultures.Developmental Biology 135, 449–58.
Giftochristos, N. &David, S. (1988) Immature optic nerve glia of rat do not promote axonal regeneration when transplanted into a peripheral nerve.Developmental Brain Research 39, 149–53.
Gilmore, S. A. &Sims, T. A. (1986) The role of Schwann cells in repair of glial cell deficits in the spinal cord. InNeural Transplantation and Regeneration (edited byDas, G. D. &Wallace, R. B.) pp. 245–69. Berlin: Springer Verlag.
Hall, S. M. (1989) Regeneration in the peripheral nervous system.Neuropathology and Applied Neurobiology 15, 513–29.
Hall, S. &Berry, M. (1989) Electron microscopic study of the interaction of axons and glia at the site of anastomosis between the optic nerve and cellular or acellular sciatic nerve grafts.Journal of Neurocytology 18, 171–84.
Hall, S. M. &Gregson, N. A. (1975) The effects of mitomycin C on the process of remyelination in the mammalian peripheral nervous system.Neuropathology and Applied Neurobiology 1, 149–70.
Hall, S. M. &Gregson, N. A. (1977) The effects of mitomycin C on the process of regeneration in the mammalian peripheral nervous system.Neuropathology and Applied Neurobiology 3, 65–78.
Hall, S. M. &Kent, A. P. (1987) The response of regenerating peripheral neurites to a grafted optic nerve.Journal of Neurocytology 16, 317–31.
Hall, S., Gregson, N. &Rickard, S. (1991) Interaction of regrowing PNS axons with transplanted aggregates of cultured CNS gliain vivo.Journal of Neurocytology 20, 299–309.
Jones, N. &Hall, S. (1991) Evaluation of a new method of neural anastomosis using nitrocellulose paper.Clinical Otolaryngology 16, 383–7.
Oorschot, D. E. &Jones, D. G. (1990) Axonal regeneration in the mammalian central nervous system — a critique of hypotheses.Advances in Anatomy, Embryology and Cell Biology 119, 1–121.
Pellegrino, R. G., Politis, M. J., Ritchie, J. M. &Spencer, P. S. (1986) Events in degenerating cat peripheral nerve: induction of Schwann cell S phase and its relation to nerve fibre degeneration.Journal of Neurocytology 15, 17–28.
Reier, P. J. (1986) Gliosis following CNS injury: the anatomy of astrocytic scars and their influence on axonal elongation. InAstrocytes (edited byFedoroff, S. &Vernadakis, A.) Vol. 3, pp. 263–324. New York: Academic Press.
Reier, P. J., Eng, L. E. &Jakeman, L. (1989) Reactive astrocytes and axonal outgrowth in the injured CNS. InNeural Regeneration and Transplantation, Frontiers of Clinical Neuroscience (edited bySeil, F. J.) Vol. 6, pp. 183–209. New York: Alan R. Liss.
Rudge, J. S., Smith, G. M. &Silver, J. (1989) Anin vitro model of wound healing in the CNS: analysis of cell reaction and interaction at different ages.Experimental Neurology 103, 1–16.
Sasaki, M. &Ide, C. (1989) Demyelination and remyelin- ation in the dorsal funiculus of the rat spinal cord after heat injury.Journal of Neurocytology 18, 225–39.
Savio, T. &Schwab, M. E. (1989) Rat CNS white matter, but not gray matter, is nonpermissive for neuronal cell adhesion and fiber growth.Journal of Neuroscience 9, 1126–33.
Schnell, L. &Schwab, M. E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors.Nature 343, 269–72.
Schwab, M. E. (1990) Myelin-associated inhibitors of neurite growth and regeneration in the CNS.Trends in Neuroscience 13, 452–7.
Schwab, M. E. &Caroni, P. (1988) Oligodendrocytes and CNS myelin are non-permissive substrates for neurite growth and fibroblast spreading in vitro.Journal of Neuroscience 8, 2381–93.
Steedman, H. F. (1957) Polyester wax. A new ribboning embedding medium for histology.Nature 179, 1345.
Vidal-Sanz, M., Bray, G. M., Villegas-Perez, M. P., Thanos, S. &Aguayo, A. J. (1987) Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat.Journal of Neuroscience 7, 2894–909.
Weinberg, E. L. &Spencer, P. S. (1979) Studies on the control of myelinogenesis. III. Signalling of oligodendro- cyte myelination by regenerating peripheral axons.Brain Research 162, 273–9.
Wells, M. K. &Bernstein, J. J. (1985) Scar formation and the barrier hypothesis in failure of mammalian central nervous system regeneration. InTrauma in the Central Nervous System (edited byDacy, R. G., Winn, H. R., Rimel, R. W. &Jane, J. A.) pp. 245–7. New York: Raven Press.
Windle, W. F. (1956) Regeneration of axons in the vertebrate central nervous system.Physiological Reviews 36, 351–79.
Wise, G., Dollery, C. &Henkind, P. (1971)The Retinal Circulation. New York: Harper & Row.
Wyse, J. P. H. &Hollenberg, M. J. (1976) Microphthalmia, retinal degeneration and optic nerve dysplasia in the Browman strain ofrattus norvegicus. InCanadian Federation of Biological Societies: Program and Proceedings of the 19th Annual Meeting 19, 160 (Abstract).
Wyse, J. P. H. &Hollenberg, M. J. (1977) Complicated colobomatous microphthalmos in the BW rat: a new form of inherited retinal degeneration.American Journal of Anatomy 149, 377–412.
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Hall, S.M., Berry, M. & Wyse, J.P.H. Regrowth of PNS axons through grafts of the optic nerve of the Browman-Wyse (BW) mutant rat. J Neurocytol 21, 402–412 (1992). https://doi.org/10.1007/BF01191505
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DOI: https://doi.org/10.1007/BF01191505