Summary
We have usedin situ hybridization with a digoxigenin-labelled probe for tenascin-C mRNA and immunocytochemistry with antibodies against tenascin-C, glial fibrillary acidic protein, OX-42 and the 200 kDa neurofilament protein to study the expression, distribution and cellular relationships of tenascin-C mRNA and protein in the developing (postnatal) and adult spinal cord of rat, and the effects thereon of dorsal root, ventral root and sciatic nerve injuries. The most interesting finding was that on postnatal day 7 (P7), P14 and in the adult, but not on P0 or P3, a group of neurons in the lumbar ventral horn expressed the tenascin-C mRNA gene. They represented about 5% of ventral horn neurons in the adult and were among the smaller such neurons. Since 40–60% of such cells were lost at P13 following sciatic nerve crush on P0, some were almost certainly motor neurons. In addition, we found that at P0 and P3, mRNA-containing glial cells were widespread in grey and white matter but sparse in the developing dorsal columns; tenascin-C immunofluorescence showed a similar distribution. By P7 there were fewer mRNA-containing cells in the ventral horns and in the area of the dorsal columns containing the developing corticospinal tract where immunofluorescence was also weak. At P14 there were no glial-like mRNA-containing cells in the grey matter; such cells were confined to the periphery of the lateral and ventral white columns but were present throughout the dorsal columns where tenascin-C immunofluorescence was also strong. No glial-like mRNA-containing cells were present in the adult lumbar spinal cord and tenascin-C immunofluorescence was confined to irregular patches in the ventral horn, especially around immunonegative cell bodies of small neurons, a zone around the central canal, and a thin zone adjacent to the glia limitans. Thus the expression of tenascin-C is differentially developmentally regulated in the grey matter and in different parts of the white matter. Three days after injury of dorsal roots L4–6, many cells containing tenascin-C mRNA, some identified as glial fibrillary acidic protein-positive astrocytes, were present in the ipsilateral dorsal column, but were rare after longer survivals. Immunoreactivity, however, was elevated in the ipsilateral dorsal column at 3 days, remained high for several months and disappeared at 6.5 months. Dorsal root injury had no effect on tenascin-C mRNA or protein in the grey matter. Sciatic nerve or ventral root injury had no effect on these molecules in any part of the spinal cord.
Similar content being viewed by others
References
Ajemian, A., Ness, R. &David, S. (1994) Tenascin in the injured rat optic nerve and in non-neuronal cellsin vitro: potential role in neural repair.Journal of Comparative Neurology 340, 233–42.
Balice-Gordon, R. J. &Thompson, W. J. (1988) Synaptic rearrangements and alterations in motor unit properties in neonatal rat extensor digitorum longus muscle.Journal of Physiology 398, 191–210.
Bartsch, U., Bartsch, S., Dörries, U. &Schachner, M. (1992) Immunohistological localization of tenascin in the developing and lesioned mouse optic nerve.European Journal of Neuroscience 4, 338–52.
Bartsch, S., Bartsch, U., Dörries, U., Faissner, A., Weller, A., Ekblom, P. &Schachner, M. (1992) Expression of tenascin in the developing and adult cerebellar cortex.Journal of Neuroscience 12, 736–49.
Bertolotto, A., Rocca, G., Canavese, G., Migheli, A. &Schiffer, D. (1991) Chondroitin sulfate proteoglycan surrounds a subset of human and rat CNS neurons.Journal of Neuroscience Research 29, 225–34.
Bignami, A., Asher, R., Perides, G. &Rahemtulla, F. (1992) The extracellular matrix of cerebral grey matter; Golgi's pericellular net and Nissl's nervösen grau revisited.International Journal of Developmental Neuroscience 10, 291–9.
Bronner-Fraser, M. (1988) Distribution and function of tenascin during cranial neural crest development in the chick.Journal of Neuroscience Research 21, 135–47.
Carlstedt, T. (1985) Regenerating axons form nerve terminals at astrocytes.Brain Research 347, 188–91.
Celio, M. R. &Chiquet-Ehrismann, R. (1993) “Perineuronal nets” around cortical interneurons are rich in tenascin.Neuroscience Letters 162, 137–40.
Crossin, K. L., Hoffman, S., Tan, S.-S. &Edelman, G. M. (1989) Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse.Developmental Biology 136, 381–92.
Cummings, J. P. &Stelzner, D. J. (1984) Prenatal and postnatal development of lamina IX neurons in the rat thoracic spinal cord.Experimental Neurology 83, 155–66.
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.
Dörries, U., Bartsch, U., Nolte, C., Roth, J. &Schachner, M. (1993) Adaptation of a non-radioactivein situ hybridization method to electron microscopy: detection of tenascin mRNA in mouse cerebellum with digoxigenin-labelled probes and gold-labelled antibodies.Histochemistry 99, 251–62.
Erickson, H. P. &Bourdon, M. A. (1989) Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors.Annual Review of Cell Biology 5, 71–92.
Faissner, A. &Kruse, J. (1990) J1/tenascin is a repulsive substrate for central nervous system neurons.Neuron 5, 627–37.
Faissner, A., Kruse, J., Chiquet-Ehrismann, R. &Mackie, E. (1988) The high-molecular-weight J1 glycoproteins are immunochemically related to tenascin.Differentiation 37, 104–14.
Fruttiger, M., Schachner, M. &Martini, R. (1995) Tenascin-C expression during Wallerian degeneration in C57BL/Wlds mice: possible implications for axonal regeneration.Journal of Neurocytology 24, 1–14.
Fuss, B., Wintergerst, E. S., Bartsch, U. &Schachner, M. (1993) Molecular characterization andin situ mRNA localization of the neural recognition molecule J1 160/180: a modular structure similar to tenascin.Journal of Cell Biology 120, 1237–49.
Gonzalez, M. De L., Malemud, C. J. &Silver, J. (1993) Role of astroglial extracellular matrix in the formation of rat olfactory bulb glomeruli.Experimental Neurology 123, 91–105.
Gribnau, A. A., De Kort, E. J., Dederen, P. J. &Nieuwenhuys, R. (1986) On the development of the pyramidal tract in the rat. II. An anterograde tracer study of the outgrowth of the corticospinal fibers.Anatomy and Embryology,175, 101–10.
Grierson, J. P., Petroski, R. E., Ling, D. S. &Geller, H. M. (1990) Astrocyte topography and tenascin/cytotactin expression: correlation with the ability to support neuritic outgrowth.Developmental Brain Research 55, 11–19.
Gulcher, J. R., Nies, D. E., Marton, L. S. &Stefansson, K. (1989) An alternatively spliced region of the human hexabrachion contains a repeat of potential N-glycosylation sites.Proceedings of the National Academy of Sciences (USA) 86, 1588–92.
Irintchev, A., Salvini, T. F., Faissner, A. &Wernig, A.(1993) Differential expression of tenascin after denervation, damage or paralysis of mouse soleus muscle.Journal of Neurocytology 22, 955–65.
Jansen, J. K. S. &Fladby, T. (1990) The perinatal reorganization of the innervation of skeletal muscle in mammals.Progress in Neurobiology 34, 39–90.
Jones, F. S., Hoffman, S., Cunningham, B. A. &Edelman, G. M. (1989) A detailed structural model of cytotactin: protein homologies, alternative RNA splicing, and binding regions.Proceedings of the National Academy of Sciences (USA) 86, 1905–9.
Joosten, E. A., Gribnau, A. A. &Dederen, P. J. (1987) An anterograde tracer study of the developing cortico-spinal tract in the rat: three components.Brain Research 433, 121–30.
Kruse, J., Keilhauer, G., Faissner, A. &Schachner, M. (1985) The J1 glycoprotein — a novel nervous system cell adhesion molecule of the L2/HNK-1 family.Nature 316, 146–8.
Langenfeld-Oster, B., Faissner, A., Irintchev, A. &Wernig, A. (1994) Polyclonal antibodies against N-CAM and tenascin delay endplate reinnervation.Journal of Neurocytology 23, 591–604.
Laywell, E. D., Dörries, U., Bartsch, U., Faissner, A., Schachner, M. &Steindler, D. A. (1992) Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury.Proceedings of the National Academy of Sciences (USA) 89, 2634–8.
Liuzzi, F. J. &Lasek, R. J. (1987) Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway.Science 237, 642–5.
Lochter, A. &Schachner, M. (1993) Tenascin and extracellular matrix glycoproteins: from promotion to polarization of neurite growthin vitro.Journal of Neuroscience 13, 3986–4000.
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.
Lowrie, M. B. &Vrbova, G. (1992) Dependence of postnatal motoneurones on their targets: review and hypothesis.Trends in Neurosciences 15, 80–4.
Lowrie, M. B., Krishnan, S. &Vrbova, G. (1987) Permanent changes in muscle and motoneurons induced by nerve injury during a critical period of development of the rat.Developmental Brain Research 31, 91–107.
Mackie, E. J., Tucker, R. P., Halfter, W., Chiquet-Ehrismann, R. &Epperlein, H. H. (1988) The distribution of tenascin coincides with pathways of neural crest cell migration.Development 102, 237–50.
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. &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.
Mckeon, R. J., Schreiber, R. C., Rudge, J. S. &Silver, J. (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes.Journal of Neuroscience 11, 3398–411.
Mege, R. M., Nicolet, S., Pincon-Raymond, M., Murawsky, M. &Rieger, F. (1992) Cytotactin is involved in synaptogenesis during regeneration of the frog neuromuscular system.Developmental Biology 149, 381–94.
Miragall, F., Kadmon, G., Faissner, A., Antonicek, H. &Schachner, M. (1990) Retention of J1/tenascin and the polysialylated form of the neural cell adhesion molecule (N-CAM) in the adult olfactory bulb.Journal of Neurocytology 19, 899–914.
Mitrovic, N., Dörries, U. &Schachner, M. (1994) Expression of the extracellular matrix glycoprotein tenascin in the somatosensory cortex of the mouse during postnatal development: an immunocytochemical andin situ hybridization analysis.Journal of Neurocytology 23, 364–78.
Perides, G., Erickson, H. P., Rahemtulla, F. &Bignami, A. (1993) Colocalization of tenascin with versican, a hyaluronate-binding chrondroitin sulfate proteoglycan.Anatomy and Embryology 188, 467–79.
Pesheva, P., Spiess, E. &Schachner, M. (1989) J-160 and J-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion.Journal of Cell Biology 109, 1765–78.
Pindzola, R. R., Doller, C. &Silver, J. (1993) Putative inhibitory extracellular matrix molecules at the dorsal root entry of the spinal cord during development and after root and sciatic nerve lesions.Developmental Biology 156, 34–48.
Prieto, A. L., Jones, F. S., Cunningham, B. A., Crossin, K. L. &Edelman, G. M. (1990) Localization during development of alternatively spliced forms of cytotactin mRNA byin situ hybridization.Journal of Cell Biology 111, 685–98.
Rettig, W. J., Hoffman, S., Su, S. L. &Garin-Chesa, P. (1992) Species diversity of neuronectin and cytotactin expression patterns in the vertebrate central nervous system.Brain Research 590, 219–28.
Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T. &Aizawa, S. (1992) Mice develop normally without tenascin.Genes and Development 6, 1821–31.
Sanes, J. R., Schachner, M. &Covault, J. (1986) Expression of several adhesion macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle.Journal of Cell Biology 102, 420–31.
Spring, J., Beck, K. &Chiquet-Ehrismann, R. (1989) Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments.Cell 59, 325–34.
Steindler, D. A., Cooper, N. G. F., Faissner, A. &Schachner, M. (1989) Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field.Developmental Biology 131, 243–60.
Tan, S.-S., Crossin, K. L., Hoffman, S. &Edelman, G. M. (1987) Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution.Proceedings of the National Academy of Sciences (USA) 84, 7977–81.
Tan, S.-S., Prieto, A. L., Newgreen, D. F., Crossin, K. L. &Edelman, G. M. (1991) Cytotactin expression in somites after dorsal neural tube and neural crest ablation in chicken embryos.Proceedings of the National Academy of Sciences (USA) 88, 6393–402.
Taylor, J., Pesheva, P. &Schachner, M. (1993) Influence of janusin and tenascin on growth cone behaviourin vitro.Journal of Neuroscience Research 35, 347–62.
Tsukamoto, T., Kusakabe, M. &Saga, Y. (1991)In situ hybridization with non-radioactive digoxigenin-11-UTP-labeled cRNA probes: localization of developmentally regulated mouse tenascin mRNAs.International Journal of Developmental Biology 35, 25–32.
Tucker, R. P. (1991) The distribution of tenascin and its transcript in the developing avian central nervous system.Journal of Experimental Zoology 259, 78–91.
Wehrle, B. &Chiquet, M. (1990) Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowthin vitro.Development 110, 401–15.
Weller, A., Beck, S. &Ekblom, P. (1991) Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis.Journal of Cell Biology 112, 355–62.
Wintergerst, E. S., Fuss, B. &Bartsch, U. (1993) Localization of janusin mRNA in the central nervous system of the developing and adult mouse.European Journal of Neuroscience 5, 299–310.
Wintergerst, E. S., Bartsch, U., Bartini, C. &Schachner, M. (1995) Changes in the expression of the extracellular matrix molecules tenascin and janusin after 3-acetylpyridine-induced lesion of the olivocerebellar system of the adult rat. Submitted for publication.
Zhang, Y., Anderson, P. N., Winterbottom, J., Lieberman, A. R., Campbell, G., Martini, R. &Schachner, M. (1994) Neurons in the rat spinal cord synthesize tenascin.Society for Neuroscience Abstracts 20, 46.
Zhang, Y., Campbell, G., Anderson, P. N., Martini, R. Schachner, M. &Lieberman, A. R. (1995a) The molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts. I. Cell adhesion molecules.Journal of Comparative Neurology, in Press.
Zhang, Y., Campbell, G., Anderson, P. N., Martini, R., Schachner, M. &Lieberman, A. R. (1995b) The molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts. II. Tenascin.Journal of Comparative Neurology, in Press.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Zhang, Y., Anderson, P.N., Campbell, G. et al. Tenascin-C expression by neurons and glial cells in the rat spinal cord: Changes during postnatal development and after dorsal root or sciatic nerve injury. J Neurocytol 24, 585–601 (1995). https://doi.org/10.1007/BF01257374
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01257374