Tenascin-C expression during Wallerian degeneration in C57BL/Wlds mice: possible implications for axonal regeneration
Purchase on Springer.com
$39.95 / €34.95 / £29.95*
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.
Schwann cells in the distal stumps of lesioned peripheral nerves strongly express the extracellular matrix glycoprotein tenascin-C. To gain insights into the relationship between Wallerian degeneration, lesion induced tenascin-C upregulation and regrowth of axons we have investigated C57BL/Wlds (C57BL/Ola) mice, a mutant in which Wallerian degeneration is considerably delayed. Since we found a distinct difference in the speed of Wallerian degeneration between muscle nerves and cutaneous nerves in 16-week-old C57BL/Wlds mice, as opposed to 6-week-old animals in which Wallerian degeneration is delayed in both, we chose the older animals for closer investigation. Five days post lesion tenascin-C was upregulated in the muscle branch (quadriceps) but not in the cutaneous branch (saphenous) of the femoral nerve in 16-week-old animals. In addition myelomonocytic cells displaying endogenous peroxidase activity invaded the muscle branch readily whereas they were absent from the cutaneous branch at this time. We could further show that it is only a subpopulation of axon-Schwann cell units (mainly muscle efferents) in the muscle branch which undergo Wallerian degeneration and upregulate tenascin-C at normal speed and that the remaining axon-Schwann cell units (mainly afferents) displayed delayed Wallerian degeneration and no tenascin-C expression. Regrowing axons could only be found in the tenascin-C-positive muscle branch where they always grew in association with axon-Schwann cell units undergoing Wallerian degeneration. These observations indicate a tight relationship between Wallerian degeneration, upregulation of tenascin-C expression and regrowth of axons, suggesting an involvement of tenascin-C in peripheral nerve regeneration.
- Bedi, K. S., Winter, J., Berry, M. &Cohen, J. (1992) Adult rat dorsal root ganglion neurons extend neurites on predegenerated but not on normal peripheral nervesin vitro.European Journal of Neuroscience 4, 193–200.
- Beuche, W. &Friede, R. L. (1984) The role of non-resident cells in Wallerian degeneration.Journal of Neurocytology 13, 767–96.
- Beuche, W. &Friede, R. L. (1986) Myelin phagocytosis in Wallerian degeneration of peripheral nerves depends on silica-sensitive, bg/bg-negative and Fc-positive monocytes.Brain Research 378, 97–106.
- Bisby, M. A. &Chen, S. (1990) Delayed Wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons.Brain Research 530, 117–20.
- Bixby, J. L., Lilien, J. &Reichardt, L. F. (1988) Identification of the major proteins that promote neuronal process outgrowth on Schwann cellsin vitro.Journal of Cell Biology 107, 353–61.
- Bristow, J., Tee, M. K., Tee S. E., Tee G., Mellon, S. H. &Miller, W. L. (1993) Tenascin-X: a novel extracellular matrix protein encoded by the human XB gene overlapping P450c21B.Journal of Cell Biology 122, 265–78.
- Brown, M. C., Lunn, E. R. &Perry, V. H. (1989) Failure of normal Wallerian degeneration results in very poor regeneration of cutaneous afferent fibres.Journal of Physiology 422, 12P.
- Brown, M. C., Lunn, E. R. &Perry, V. H. (1992) Consequences of slow Wallerian degeneration for regenerating motor and sensory axons.Journal of Neurobiology 23, 521–36.
- Brown, M. C., Perry, V. H., Hunt, S. P. &Lapper, S. R. (1994) Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration.European Journal of Neuroscience 6, 420–8.
- Brown, M. C., Perry, V. H., Lunn, E. R., Gordon, S. &Heumann, R. (1991) Macrophage dependence of peripheral sensory nerve regeneration: possible involvement of nerve growth factor.Neuron 6, 359–70.
- Chen, S. &Bisby, M. A. (1993) Impaired motor axon regeneration in the C57BL/Ola mouse.Journal of Comparative Neurology 333, 449–54.
- Clemence, A., Mirsky, R. &Jessen, K. R. (1989) Nonmyelin-forming Schwann cells proliferate rapidly during Wallerian degeneration in the rat sciatic nerve.Journal of Neurocytology 18, 185–92.
- Daniloff, J. K., Crossin, K. L., Pincon-Raymond, M., Murawsky, M., Rieger, F. &Edelman, G. M. (1989) Expression of cytotactin in the normal and regenerating neuromuscular system.Journal of Cell Biology 108, 625–35.
- Eccleston, P. A. (1992) Regulation of Schwann cell proliferation: mechanisms involved in peripheral nerve development.Experimental Cell Research 199, 1–19.
- Erickson, H. P. (1993) Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions.Current Opinion in Cell Biology 5, 869–76.
- Faissner, A. &Kruse, J. (1990) J1/tenascin is a repulsive substrate for central nervous system neurons.Neuron 5, 627–37.
- Fawcett, J. W. &Keynes, R. J. (1990) Peripheral nerve regeneration.Annual Reviews in Neuroscience 13, 43–60.
- Friede, R. L. &Johnstone, M. (1967) Response of thymidine labeling of nuclei in gray matter and nerve following sciatic nerve transection.Acta Neuropathologica 7, 218–31.
- Giese, K. P., Martini, R., Lemke, G., Soriano, P. &Schachner, M. (1992) Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons.Cell 71, 565–76.
- Hall, S. M. (1986) 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.
- Hall, S. M. (1989) Regeneration in the peripheral nervous system.Neuropathology and Applied Neurobiology 15, 513–29.
- Hall, S. M. (1994) Observations on the progress of Wallerian degeneration in transected peripheral nerves of C57BL/Wlds mice in the presence of recruited macrophages.Journal of Neurocytology 22, 480–90.
- Heumann, R., Korsching, S., Bandtlow, C. &Thoenen, H. (1987) Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection.Journal of Cell Biology 104, 1623–31.
- Johnson, E. J., Taniuchi, M. &Distefano, P. S. (1988) Expression and possible function of nerve growth factor receptors on Schwann cells.Trends in Neuroscience 11, 299–304.
- Kruse, J., Mailhammer, R., Wernecke, H., Faissner, A., Sommer, I., Goridis, C. &Schachner, M. (1984) Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1.Nature 311, 153–5.
- Lochter, A., Vaughan, L., Kaplony, A., Prochiantz, A., Schachner, M. &Faissner, A. (1991) J1/tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth.Journal of Cell Biology 113, 1159–71.
- Lunn, E. R., Perry, V. H., Brown, M. C., Rosen, H. &Gordon, S. (1989) Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve.European Journal of Neuroscience 1, 27–33.
- Lyon, M. F., Ogunkolade, B. W., Brown, M. C., Atherton, D. J. &Perry, V. H. (1993) A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4.Proceedings of the National Academy of Sciences (USA)90, 9717–20.
- Martini, R. (1994) Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves.Journal of Neurocytology 23, 1–28.
- Martini, R. &Schachner, M. (1986) Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve.Journal of Cell Biology 103, 2439–48.
- Martini, R. &Schachner, M. (1988) Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and myelin-associated glycoprotein) in regenerating adult mouse sciatic nerve.Journal of Cell Biology 106, 1735–46.
- Martini, R., Bollensen, E. &Schachner, M. (1988) Immunocytological localization of the major peripheral nervous system glycoprotein P0 and the L2/HNK-1 and L3 carbohydrate structures in developing and adult mouse sciatic nerve.Developmental Biology 129, 330–8.
- Martini, R., Schachner, M. &Faissner, A. (1990) Enhanced expression of the extracellular matrix molecule J1/tenascin in the regenerating adult mouse sciatic nerve.Journal of Neurocytology 19, 601–16.
- Martini, R., Xin, Y., Schmitz, B. &Schachner, M. (1992) The L2/HNK-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves.European Journal of Neuroscience 4, 628–39.
- Martini, R., Schachner, M. &Brushart, T. (1994) The L2/HNK-1 Carbohydrate is preferentially expressed by previously motor axon-associated Schwann Cells in re-innervated peripheral nerves.Journal of Neuroscience, in press.
- Meyer, M., Motsuoka, I., Wetmore, C., Olson, L. &Thoenen, H. (1992) Enhanced synthesis of brain derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA.Journal of Cell Biology 119, 45–54.
- 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.
- Nolte, C. &Martini, R. (1992) Immunocytochemical localization of the L1 and N-CAM cell adhesion molecules and their shared carbohydrate epitope L2/HNK-1 in the developing and differentiated gustatory papillae of the mouse tongue.Journal of Neurocytology 21, 19–33.
- Palay, S. L. &Chan-Palay, V. (1974)Cerebellar Cortex. Cytology and Organization. New York, Heidelberg, Berlin: Springer Verlag.
- Perry, V. H. &Brown, M. C. (1992) Macrophages and nerve regeneration.Current Opinion in Neurobiology 2, 679–82.
- Perry, V. H., Brown, M. C. &Gordon, S. (1987) The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration.Journal of Experimental Medicine 165, 1218–23.
- Perry, V. H., Brown, M. C. &Tsao, J. W. (1992) The effectiveness of the gene which slows the rate of Wallerian degeneration in C57BL/Ola mice declines with age.European Journal of Neuroscience 4, 1000–2.
- Rathjen, F. G. &Schachner, M. (1984) Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion.EMBO Journal 3, 1–10.
- Rieger, F., Daniloff, J. K., Pincon-Raymond, M., Crossin, K. L., Grumet, M. &Edelman, G. M. (1986) Neuronal cell adhesion molecules and cytotactin are colocalized at the node of Ranvier.Journal of Cell Biology 103, 379–91.
- Ruegg, C. R., Chiquet, E. R. &Alkan, S. S. (1989) Tenascin, an extracellular matrix protein, exerts immunomodulatory activities.Proceedings of the National Academy of Sciences (USA)86, 7437–41.
- Sanes, J. R., Schachner, M. &Covault, J. (1986) Expression of several adhesive macromolecules (NCAM, L1, J1, NILE, uvomorulin, laminin, fibronectin and haparan sulfate proteoglycan) in embryonic, adult and denervated adult skeletal muscles.Journal of Cell Biology 102, 420–31.
- Seilheimer, B. &Schachner, M. (1988) Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture.Journal of Cell Biology 107, 341–51.
- Stole, G., Griffin, J. W., Li, C. Y. &Trapp, B. D. (1989) Wallerian degeneration on the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation.Journal of Neurocytology 18, 671–83.
- Taylor, J., Pesheva, P. &Schachner, M. (1993) Influence of janusin and tenascin on growth cone behaviorin vitro.Journal of Neuroscience Research 35, 347–62.
- Wehrle, B. &Chiquet, M. (1990) Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowthin vitro.Development 110, 401–15.
- Wehrle-Haller, B. &Chiquet, M. (1993) Dual function of tenascin-simultaneous promotion of neurite growth and inhibition of glial migration.Journal of Cell Science 106, 597–610.
- Wehrle-Haller, B., Koch, M., Baumgartner, S., Spring, J. &Chiquet, M. (1991) Nerve-dependent and -independent tenascin expression in the developing chick limb bud.Development 112, 627–37.
- Zhang, Y., Campbell, G., Anderson, P. N., Lieberman, A. R., Martini, R. &Schachner, M. (1993) Cell adhesion and extracellular matrix molecules associated with regenerating CNS axons and Schwann cells of peripheral nerve grafts implanted in adult rat thalamus.Society for Neuroscience Abstracts 19, 1509.
- Tenascin-C expression during Wallerian degeneration in C57BL/Wlds mice: possible implications for axonal regeneration
Journal of Neurocytology
Volume 24, Issue 1 , pp 1-14
- Cover Date
- Print ISSN
- Online ISSN
- Kluwer Academic Publishers
- Additional Links