Summary
Tenascin-C, an extracellular matrix glycoprotein that exhibits both growth-promoting and growth-inhibiting properties, is produced in the CNS mainly by astrocytes. In the present study we show that kainate-induced seizures result in an increased expression of tenascin-C in rat brain. Tenascin-C mRNA was increased mainly in the granule cell layer of the hippocampal complex, but tenascin-C mRNA expression was also observed in the pyriform cortex and amygdalo-cortical nucleus. Double labelling experiments using tenascin-C probes and MAP2 (a neuronal microtubule associated protein) antibodies revealed many neurons in these layers that express tenascin-C mRNA. These results support our previous findings of an increased tenascin-C immunoreactivity associated with the axons of granule cells. Tenascin-C expression is rapidly induced by seizures (6h), preceding any lesion and glial reaction. In this pathological condition tenascin-C appears to be produced by both glia and neurons. The functional repercussions on the scarring and remodelling processes are also discussed.
Similar content being viewed by others
References
Armstrong, R. C., Harvarth, L. &Dubois-Dalcq, M. (1990) Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules.Journal of Neuroscience Research 27, 400–7.
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.
Ben-Ari, Y. (1985) Limbic seizures and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy.Neuroscience 14, 375–403.
Brodkey, J. A., Laywell, E. D., O'Brien, T. F., Faissner, A., Stefansson, K., Dörries, H. U., Schachner, M. &Steindler, D. A. (1995) Focal brain injury and upregulation of a developmentally regulated extracellular matrix protein.Journal of Neurosurgery 82, 106–12.
Bugra, K., Pollard, H., Charton, G., Moreau, J., Ben-Ari, Y. &Khrestchatisky, M. (1994) aFGF, bFGF and flg mRNAs show distinct patterns of induction in the hippocampus following kainate-induced seizures.Eurepean Journal of Neuroscience 6, 58–66.
Chomczynski, P. &Sacchi, H. (1987) Single-step method of RNA isolation by guanidinium thiocyanate-phenolchloroform extraction.Annals of Biochemistry 162, 156–9.
Chuong, C.-M., Crossin, K. L. &Edelman, G. M. (1987) Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers.Journal of Cell Biology 104, 331–42
Edelman, G. M. (1986) Cell adhesion molecules in neuronal histogenesis.Annual Review of Physiology 48, 417–30.
Faissner, A. &Kruse, J. (1990) J1/Tenascin is a repulsive substrate for central nervous system neurons.Neuron 5, 627–37.
Faissner, A. &Steindler, D. (1995) Boundaries and inhibitory molecules in developing neural tissues.Glia 13, 233–54.
Faissner, A. Kruse, J., Chiquet-Ehrismann, R. &Mackie, E. (1988) The high-molecular-weight J1 glycoproteins are immunocytochemically related to tenascin.Differentiation 37, 104–14.
Ferhat, L., Khrestchatisky, M., Roisin, M. P. &Barbin, G. (1993). bFGF-induced increase in Zif/268 anc c-fos mRNA levels is Ca2+ dependent in primary cultures of hippocampal neurons.Journal of Neurochemistry 61, 1105–12.
Ferhat, L., Chevassus Au Louis, N., Jorquera, I., Niquet, J., Khrestchatisky, M., Ben-Ari, Y. &Represa, A. (1995) Transient increase of tenascin-C in immature hippocampus: astroglial and neuronal expression.Journal of Neurocytology 25, 53–66.
Gall, C. M., Berschauer, R. &Isackson, P. J. (1994) Seizures increase basic fibroblast growth factor mRNA in adult rat forebrain neurons and glia.Molecular Brain Research 21, 190–205.
Goetschy, J. F., Ulrich, G., Aunis, D. &Ciesielskitreska, J. (1987) Fibronectin and collagen modulate the proliferation and morphology of astroglial cells in culture.International Journal of Developmental Neuroscience 5, 63–70.
Grumet, M., Hoffman, S., Crossin, K. L. &Edelman, G. M. (1985) Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction.Proceedings of the National Academy of Science USA 82, 8075–9.
Husmann, K., Faissner, A. &Schachner, M. (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type 3 repeats.Journal of Cell Biology 116, 1475–86.
Khrestchatisky, M., Ferhat, L., Charton, G., Bernard, A., Pollard, H., Represa, A. &Ben-Ari, Y. (1995) Molecular correlates between reactive and developmental plasticity in the rat hippocampus.Journal of Neurobiology 26, 426–36.
Kruse, J., Keilhauer, 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.
Laywell, E. D., Dörries, U., Bartsch, U., Faissner, A., Schachner, M. &Steindler, D. A. (1992) Enhanced expression of the developmentally regulated extrecellular matrix molecule tenascin following adult brain injury.Proceeding of the National Academy of Science USA 89, 2634–8.
Letourneau, P. C., Condic, M. L. &Snow, D. M. (1994) Interactions of developing neurons with the extracellular matrix.The Journal of Neuroscience. 14, 915–28.
Lindholm, D., Castren, E., Kiefer, R., Zafra, F. &Thoenen, H. (1992) Transforming growth factor-β1 in the rat brain: increase after injury and inhibition of astrocyte proliferation.Journal of Cell Biology 117, 395–400.
Lochter, A. &Schachner, M., (1993) Tenascin and extracellular matrix glycoproteins: from promotion to polarization of neurite growthin vitro.Journal of Neuroscience 13, 3986–4000.
McKeon, R. J., Schreiber, R. C., Rudge, J. C. &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.
Meiners, S., Marone, M., Rittenhouse, J. L. &Geller, H. M. (1993) Regulation of astrocytic tenascin by basic fibroblast growth factor.Developmental Biology 160, 480–93.
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.
Nadler, J. V. (1981) Kainic acid as a tool for the study of temporal lobe epilepsy.Life Sciences 29, 2031–42.
Nagano, N., Aoyagi, M. &Hirakawa, K. (1993) Extracellular matrix modulates the proliferation of rat astrocytes in serum-free culture.Glia 8, 71–6.
Nedivi, E., Hevroni, D., Naot, D., Israeli, D. &Citri, Y. (1993) Numerous candidate plasticity-related genes revealed by differential cDNA cloning.Nature 363, 718–22.
Nichols, N. R., Osterburg, H. H., Masters, J. N., Millar, S. L. &Finch, C. E. (1990) Messenger RNA for glial fibrillary acidic protein is decreased in rat brain following acute chronic cortiscosterone treatment.Molecular Brain Research 7, 1–7.
Niquet, J., Jorquera, I., Ben-Ari, Y. &Represa, A. (1993) NCAM immunoreactivity on mossy fibers and reactive astrocytes in the hippocampus of epileptic rats.Brain Research 626, 106–16.
Niquet, J., Ben-Ari, Y. &Represa, A. (1994a) Glial reaction after seizure induced hippocampal lesion: immunohistochemical characterization of proliferating glial cells.Journal of Neurocytology 23, 641–56.
Niquet, J., Jorquera, I., Ben-Ari, Y. &Represa, A. (1994b) Proliferative astrocytes may express fibronectinlike protein in the hippocampus of epileptic rats.Neuroscience Letters 180, 13–16.
Niquet, J., Jorquera, I., Faissner, A., Ben-Ari, Y. &Represa, A. (1995) Gliosis and axonal sprouting in the hippocampus of epileptic rats are associated with an increase of tenascin-C immunoreactivity.Journal of Neurocytology 24, 611–24.
Pearson, C. A., Pearson, D., Shibahara, S., Hofsteenge, J. &Chiquet-Ehrismann, R. (1988) Tenascin: cDNA cloning and induction by TGF-β.EMBO Journal 7, 2977–82.
Pollard, H., Khrestchatisky, M., Moreau, J., Ben-Ari, Y. &Represa, A. (1994) Correlation between reactive sprouting and microtubule protein expression in epileptic hippocampus.Neuroscience 61, 773–87.
Popovici, T., Represa, A., Crépel, V., Barbin, G., Beaudoin, M. &Ben-Ari, Y. (1990) Effects of kainic acid-induced seizures and ischemia on c-fos-like proteins in rat brain.Brain Research 536, 183–94.
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.
Reichardt, L. F. &Tomaselli, K. J. (1991) Extracellular matrix molecules and their receptors: functions in neural development.Annual Review of Neuroscience 14, 531–70.
Represa, A., Tremblay, E. &Ben-Ari, Y. (1987) Kainate binding sites in the hippocampal mossy fibers: localization and plasticity.Neuroscience 20, 739–48.
Represa, A., Jorquera, I., Le Gal La Salle, G. &Ben-Ari, Y. (1993) Epilepsy induced collateral sprouting of hippocampal mossy fibers: does it induce the development of ectopic synapses with granule cell dendrites?Hippocampus 3, 257–68.
Represa, A., Niquet, J., Charriaut-Marlangue, C. &Ben-Ari, Y. (1993b) Reactive astrocytes in the kainic acid-damaged hippocampus have the phenotypic features of type-2 astrocytes.Journal of Neurocytology 22, 299–310.
Represa, A., Niquet, J., Pollard, H. &Ben-Ari, Y. (1995) Cells death, gliosis, and synaptic remodeling in the hippocampus of epileptic rats.Journal of Neurobiology 26, 413–25.
Rutishauser, D. E. &Jessel, T. M. (1988) Cell adhesion molecules in vertebrate neural development.Physiological Reviews 68, 810–57.
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.
Steindler, D. A., Settles, D., Erickson, H. P. Laywell, E. D., Yoshiki, A., Faissner, A. &Kusakabe, M. (1995) Tenascin knockout mice: barrels, boundary molecules, and glial scars.Journal of Neuroscience 15, 1971–83.
Tauck, D. L. &Nadler, J. V. (1985) Evidence for functional mossy fiber sprouting in hippocampal formation of kainic acid treated rats.Journal of Neuroscience 5, 1016–22.
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.
Weller, A., Beck, S. &Ekblom, P. (1992) Aminoacid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis.Journal of Cell Biology 112, 355–62.
Zhang, Y., Anderson, P. N., Campbell, G., Mohajeri, H., Schachner, M. &Lieberman, A. R. (1995) 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.Journal of Neurocytology 24, 585–601.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ferhat, L., Chevassus-Au-Louis, N., Khrestchatisky, M. et al. Seizures induce tenascin-C mRNA expression in neurons. J Neurocytol 25, 535–546 (1996). https://doi.org/10.1007/BF02284821
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02284821