Skip to main content
SpringerLink
Log in

Contacts between regenerating axons and the Schwann cells of sciatic nerve segments grafted to the optic nerve of adult rats

  • Published:
Journal of Neurocytology

Summary

The relation between Schwann cells, basal laminae and axons during retinal ganglion cell regeneration was studied by using cellular, acellular and partially acellular sciatic nerve autografts into the optic nerve. Acellular grafts were achieved by temporary compression which eliminates living Schwann cells and axons. The compressed sciatic nerve together with the intact portion was used as a partially acellular graft. The compressed portion was anastomosed to the optic nerve and the intact portion was situated distally. After 3–21 days post-operation, the grafts were studied by thin sectioning and freeze-fracture. Axons were seen to regenerate into cellular grafts in contact with Schwann cells after one week, but not into acellular grafts for the entire period. In the partially acellular grafts, regenerating axons were first observed after two weeks and were always in contact with Schwann cells migrating from the intact portion. Moreover, membrane specializations, fuzzy materials in the space between apposed membranes, and putative tight junctions, were found between regenerated axons including growth cone and Schwann cells, and between adjoining Schwann cells. An extensive meshwork of putative tight junctions was displayed between reforming perineurial cells surrounding the groups of Schwann cells and associated axons. Gap junctions were seen between adjoining Schwann cells, and between reforming perineurial cells. These results suggest that the axonal contact with Schwann cell surfaces plays an important role in retinal ganglion cell regeneration.

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

  • Aguayo, A. J., David, S., Richardson, P. &Bray, G. M. (1982) Axonal elongation in peripheral and central nervous system transplants. InAdvances in Cellular Neurobiology (edited byFedoroff, S. &Hertz, L.) pp. 215–34. New York: Academic Press.

    Google Scholar 

  • Aguayo, A. J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. InSynoptic Plasticity, (edited byCotman, C. W.) pp. 457–84. New York: Guilford Press.

    Google Scholar 

  • Ard, M. D., Bunge, R. P. &Bunge, M. B. (1987) Comparison of the Schwann cell surface and Schwann cell extracellular matrix as promoters of neurite growth.Journal of Neurocytology 16, 539–55.

    Google Scholar 

  • Berry, M., Rees, L. &Sievers, J. (1986) Unequivocal regeneration of rat optic nerve axons into sciatic nerve isografts. InNeural Transplantation and Regeneration. (edited byDas, G. D. &Wallace, R. B.) pp. 63–79. New York: Springer-Verlag.

    Google Scholar 

  • Berry, M., Hall, S., Follows, R., Rees, L., Gregson, N. &Sievers, J. (1988a) Response of axons and glia at the site of anastomosis between the optic nerve and cellular or acellular sciatic nerve grafts.Journal of Neurocytology 17, 727–44.

    Google Scholar 

  • Berry, M., Rees, L., Hall, S., Yiu, P. &Sievers, J. (1988b) Optic axons regenerate into sciatic nerve isografts only in the presence of Schwann cells.Brain Research Bulletin 20, 223–31.

    Google Scholar 

  • Carmignoto, G., Maffei, L., Candeo, P., Canella, R. &Comelli, C. (1989) Effect of NGF on the survival of rat retinal ganglion cells following optic nerve section.Journal of Neuroscience 9, 1263–72.

    Google Scholar 

  • Carter, D. A., Bray, G. M. &Aguayo, A. J. (1989) Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters.Journal of Neuroscience 9, 4042–50.

    Google Scholar 

  • Crossin, K. L., Hoffman, S., Grumet, M., Thiery, J. -P. &Edelman, G. M. (1986) Site-restricted expression of cytotactin during development of the chick embryo.Journal of Cell Biology 102, 1917–30.

    Google Scholar 

  • David, S. (1988) Neurite outgrowth from mammalian CNS neurons on astrocytesin vitro may not be mediated primarily by laminin.Journal of Neurocytology 17, 131–44.

    Google Scholar 

  • Dermietzel, R. &Kroczek, H. (1980) Interlamellar tight junctions of central myelin. I. Developmental mechanisms during myelinogenesis.Cell and Tissue Research 213, 81–94.

    Google Scholar 

  • Dermietzel, R., Leibstein, A. G. &Schuncke, D. (1980) Interlamellar tight junctions of central myelin. II. A freeze-fracture and cytochemical study on their arrangement and composition.Cell and Tissue Research 213, 95–108.

    Google Scholar 

  • Denny-Brown, D. &Brenner, C. (1944) Lesion in peripheral nerve resulting from compression by spring clip.Archives of Neurology and Psychiatry 52, 1–19.

    Google Scholar 

  • Fallon, J. R. (1985) Preferential outgrowth of central nervous system neuntes on astrocytes and Schwann cells as compared with nonglial cellsin vitro.Journal of Cell Biology 100, 198–207.

    Google Scholar 

  • Fukuda, Y., Sasaki, H., Adachi, E., Inoue, T. &Morigiwa, K. (1990) Optic nerve regeneration by peripheral nerve transplant.Neuroscience Research, (Supplement)13, S24-S30.

    Google Scholar 

  • Giftochristos, N. &David, S. (1988) Laminin and heparan sulphate proteoglycan in the lesioned adult mammalian central nervous system and their possible relationship to axonal sprouting.Journal of Neurocytology 17, 385–97.

    Google Scholar 

  • Haftek, J. &Thomas, P. K. (1968) Electron-microscope observations on the effects of localized crush injuries on the connective tissues of peripheral nerve.Journal of Anatomy 103, 233–43.

    Google Scholar 

  • Hall, S. M. (1986a) Regeneration in cellular and acellular autografts in the peripheral nervous system.Neuropathology and Applied Neurobiology 12, 27–46.

    Google Scholar 

  • Hall, S. M. (1986b) The effect of inhibiting Schwann cell mitosis on the re-innervation of acellular autografts in the peripheral nervous system of the mouse.Neuropathology and Applied Neurobiology 12, 401–14.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hatta, K., Nose, A., Nagafuchi, A. &Takeichi, M. (1988) Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family.Journal of Cell Biology 106, 873–81.

    Google Scholar 

  • Hopkins, J. M. &Bunge, R. P. (1991) Regeneration of axons from adult rat retinal ganglion cells on cultured Schwann cells is not dependent on basal lamina.Glia 4, 46–55.

    Google Scholar 

  • Ide, C., Tohyama, K., Yokota, R., Nitatori, T. &Onodera, S. (1983) Schwann cell basal lamina and nerve regeneration.Brain Research 288, 61–75.

    Google Scholar 

  • Kleitman, N., Wood, P., Johnson, M. I. &Bunge, R. P. (1988a) Schwann cell surfaces but not extracellular matrix organized by Schwann cells support neurite outgrowth from embryonic rat retina.Journal of Neuroscience 8, 653–63.

    Google Scholar 

  • Kleitman, N., Simon, D. K., Schachner, M. &Bunge, R. P. (1988b) Growth of embryonic retinal neurites elicited by contact with Schwann cell surfaces is blocked by antibodies to L1.Experimental Neurology 102, 298–306.

    Google Scholar 

  • Kromer, L. F. &Cornbrooks, C. J. (1985) Transplants of Schwann cell cultures promote axonal regeneration in the adult mammalian brain.Proceedings of the National Academy of Sciences (USA)82, 6330–4.

    Google Scholar 

  • Lavie, V., Harel, A., Doron, A., Solomon, A., Lobel, D., Belkin, M., Ben-Basat, S., Sharma, S. &Schwartz, M. (1987) Morphological response of injured adult rabbit optic nerve to implants containing media conditioned by growing optic nerves.Brain Research 419, 166–72.

    Google Scholar 

  • Lavie, V., Murray, M., Solomon, A., Ben-Bassat, S., Belkin, M., Rumelt, S. &Schwartz, M. (1990) Growth of injured rabbit optic axons within their degenerating optic nerve.Journal of Comparative Neurology 298, 293–314.

    Google Scholar 

  • Maffei, L., Carmignoto, G., Perry, V. H., Candeo, P. &Ferrari, G. (1990) Schwann cells promote the survival of rat retinal ganglion cells after optic nerve section.Proceedings of the National Academy of Sciences (USA)87, 1855–9.

    Google Scholar 

  • McLoon, L. K. &McLoon, S. C. (1988) Schwann cell-conditioned medium promotes neurite outgrowth from expiants of fetal rat retina and tectumin vitro.Developmental Brain Research 39, 61–8.

    Google Scholar 

  • Nieke, J. &Schachner, M. (1985) Expression of the neural cell adhesion molecules L1 and N-CAM and their common carbohydrate epitope L2/HNK-1 during development and after transection of the mouse sciatic nerve.Differentiation 30, 141–51.

    Google Scholar 

  • Noble, M., Albrechtsen, M., Moller, C., Lyles, J., Bock, E., Goridis, C., Watanabe, M. &Rutishauser, U. (1985) Glial cells express N-CAM/D2-CAM-like polypeptides in vitro.Nature 316, 725–8.

    Google Scholar 

  • Politis, M. J. &Spencer, P. S. (1986) Regeneration of rat optic axons into peripheral nerve grafts.Experimental Neurology 91, 52–9.

    Google Scholar 

  • Politis, M. J., Ederle, K. &Spencer, P. S. (1982) Tropism in nerve regeneratingin vivo. Attraction of regenerating axons by diffusible factors derived from cells in distal nerve stumps of transected peripheral nerves.Brain Research 253, 1–12.

    Google Scholar 

  • Powell, H. C. &Myers, R. R. (1986) Pathology of experimental nerve compression.Laboratory Investigation 55, 91–100.

    Google Scholar 

  • Reale, E., Luciano, L. &Spitznas, M. (1975) Freeze-fracture faces of the perineurial sheath of the rabbit sciatic nerve.Journal of Neurocytology 4, 261–70.

    Google Scholar 

  • Scalia, F. &Matsumoto, D. E. (1985) The morphology of growth cones of regenerating optic nerve axons.Journal of Comparative Neurology 231, 323–38.

    Google Scholar 

  • Schwab, M. E. &Thoenen, H. (1985) Dissociated neurons regenerate into sciatic but not optic nerve expiants in culture irrespective of neurotrophic factors.Journal of Neuroscience 5, 2415–23.

    Google Scholar 

  • Smith, G. V. &Stevenson, J. A. (1988) Peripheral nerve grafts lacking viable Schwann cells fail to support central nervous system axonal regeneration.Experimental Brain Research 69, 299–306.

    Google Scholar 

  • So, K. -F. &Aguayo, A. J. (1985) Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats.Brain Research 328, 349–54.

    Google Scholar 

  • Sternberger, N. H., Quarles, R., Itoyama, Y. &Webster, H. F. (1979) Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rat.Proceedings of the National Academy of Sciences (USA)76, 1510–14.

    Google Scholar 

  • Tetzlaff, W. (1978) The development of a zonula occludens in peripheral myelin of the chick embryo. A freeze-fracture study.Cell and Tissue Research 189, 187–201.

    Google Scholar 

  • Tetzlaff, W. (1982) Tight junction contact events and temporary gap junctions in the sciatic nerve fibers of the chicken during Wallerian degeneration and subsequent regeneration.Journal of Neurocytology 11, 839–58.

    Google Scholar 

  • Thanos, S., Bahr, M., Barde, Y. A. &Vanselow, J. (1989) Survival and axonal elongation of adult rat retinal ganglion cells.In vitro effects of lesioned sciatic nerve and brain derived neurotrophic factor.European Journal of Neuroscience 1, 19–26.

    Google Scholar 

  • Thomas, P. K. &Jones, D. G. (1967) The cellular response to nerve injury. 2. Regeneration of the perineurium after nerve section.Journal of Anatomy 101, 45–55.

    Google Scholar 

  • Tomaselli, K. J., Reichardt, L. F. &Bixby, J. L. (1986) Distinct molecular interactions mediate neuronal process outgrowth on non-neuronal cell surfaces and extracellular matrices.Journal of Cell Biology 103, 2659–72.

    Google Scholar 

  • Varon, S. &Williams, L. R. (1986) Nerve regeneration chamber: physical and molecular influences. InProcesses of Recovery from Neural Trauma (edited byGilad, G. M., Gorio, A. &Kreutzberg, G. W.) pp. 309–16. Berlin: Springer-Verlag.

    Google Scholar 

  • 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.

    Google Scholar 

  • Villegas-Perez, M. P., Vidal-Sanz, M., Bray, G. M. &Aguayo, A. J. (1988) Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats.Journal of Neuroscience 8, 265–80.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, School of Medicine, Chiba University, 1-8-1 Inhana, Chuo-ku, 260, Chiba City, Japan

    M. Dezawa & T. Nagano

Authors
  1. M. Dezawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Nagano
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dezawa, M., Nagano, T. Contacts between regenerating axons and the Schwann cells of sciatic nerve segments grafted to the optic nerve of adult rats. J Neurocytol 22, 1103–1112 (1993). https://doi.org/10.1007/BF01235752

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01235752

Keywords

Search

Navigation