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Delayed astrocyte reaction following facial nerve axotomy

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Journal of Neurocytology

Summary

Transection of the facial nerve causes a rapid increase of glial fibrillary acidic protein in reactive astrocytes and a proliferation of local microglial cells. The latter is associated with a detachment of synaptic terminals from the regenerating motor neurons. About 3 weeks following axotomy the reactive astrocytes begin to form thin, sheet-like lamellar processes which cover virtually all neuronal surfaces. A high 5′-nucleotidase enzymic activity can be demonstrated in the plasma membrane of these thin cell processes. Subsequently, the lamellar processes become arranged in stacks which persist for several months and thus isolate the regenerating motor neurons from their afferent synaptic input. It is speculated that the process may protect the motor neurons during regeneration.

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References

  • ALDSKOGIUS, H. (1982) Glial cell responses in the adult rabbit dorsal motor vagal nucleus during axon reaction.Journal of Neuropathology and Applied Neurobiology 8, 341–9.

    Google Scholar 

  • AMANO, S., KREUTZBERG, G. W. & REDDINGTON, M. (1983) 5′-Nucleotidase activity in human astrocytomas.Acta neuropathologica (Berlin) 59, 145–9.

    Google Scholar 

  • BARRON, K. D., CHIANG, T. Y., DANIELS, A. C. & DOOLIN, P. F. (1971) Subcellular accompaniments of axon reaction in cervical motoneurons of the cat. InProgress in Neuropathology, Vol. 1 (edited by ZIMMERMAN, H. M.), pp. 255–80. New York, London: Grune & Stratton.

    Google Scholar 

  • BERNE, R. M., WINN, H. R., KNABB, R. M., ELY, S. W. & RUBIO, R. (1983) Blood flow regulation by adenosine in heart, brain, and skeletal muscle. InRegulatory Function of Adenosine (edited by BERNE, R. M., RALL, T. W. & RUBIO, R.), pp. 293–317. The Hague, Boston, London: Martinus Nijhoff.

    Google Scholar 

  • BERNSTEIN, J. J., WELLS, M. R. & BERNSTEIN, M. E. (1975) Dendrites and neuroglia following hemisection of rat spinal cord: effects of puromycin. InAdvances in Neurology, Vol. 12,Physiology and Pathology of Dendrites (edited by KREUTZBERG, G. W.), pp. 439–51. New York: Raven Press.

    Google Scholar 

  • BIGNAMI, A. & DAHL, D. (1977) Specificity of the glial fibrillary acidic protein for astroglia.Journal of Histochemistry and Cytochemistry 25, 466–9.

    Google Scholar 

  • BIGNAMI, A., ENG, L. F., DAHL, D. & UYEDA, C. T. (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence.Brain Research 43, 429–35.

    Google Scholar 

  • BLINZINGER, K. & KREUTZBERG, G. (1968) Displacement of synaptic terminals from regenerating motoneurons by microglial cells.Zeitschrift für Zellforschung und mikroskopische Anatomie 85, 145–57.

    Google Scholar 

  • CAMMERMEYER, J. (1955) Astroglial changes during retrograde atrophy of nucleus facialis in mice.Journal of Comparative Neurology 102, 133–50.

    Google Scholar 

  • CAMMERMEYER, J. (1965) Juxtavascular karyokinesis and microglia cell proliferation during retrograde reaction in the mouse facial nucleus.Ergebnisse der Anatomie und Entwicklungsgeschichte 38, 1–22.

    Google Scholar 

  • CARRAWAY, K. L., DOSS, C. R., HUGGINS, J. W., CHESNUT, R. W. & CAROTHERS CARRAWAY, C. A. (1979) Effects of cytoskeletal perturbant drugs on ecto 5′-nucleotidase, a conacavalin A receptor.Journal of Cell Biology 83, 529–43.

    Google Scholar 

  • CHEN, D. H. (1978) Qualitative and quantitative study of synaptic displacement in chromatolyzed spinal motoneurons of the cat.Journal of Comparative Neurology 177, 635–64.

    Google Scholar 

  • CONNOR, J. R. & BERKOWITZ, E. M. (1985) A demonstration of glial filament distribution in astrocytes isolated from rat cerebral cortex.Neuroscience 16, 33–44.

    Google Scholar 

  • COTMAN, C. W., NIETO-SAMPEDRO, M. & HARRIS, E. W. (1981) Synapse replacement in the nervous system of adult vertebrates.Physiological Reviews 61, 684–784.

    Google Scholar 

  • DAHL, D. & BIGNAMI, A. (1985) Intermediate filaments in nervous tissue. InCell and Muscle Motility, Vol. 6 (edited by SHAY, J. W.), pp. 75–96. New York: Plenum Press.

    Google Scholar 

  • DEPIERRE, J. W. & KARNOVSKY, M. L. (1974a) Ectoenzymes of the guinea pig polymorphonuclear leukocyte I. Evidence for an ecto-adenosine monophosphatase,-adenosine tri-phosphatase, and -p-nitrophenyl phosphatase.Journal of Biological Chemistry 249, 7111–20.

    Google Scholar 

  • DEPIERRE, J. W. & KARNOVSKY, M. L. (1974b) Ectoenzyme of granulocytes: 5′-nucleotidase.Science 183, 1096–8.

    Google Scholar 

  • DIECKHOFF, J., HEIDEMANN, M., LIETZKE, R. & MANNHERZ, H. G. (1986) Isolation and characterization of 5′-nucleotidase from avian muscle sources and its interaction with filamentous actin. InCellular Biology of Ectoenzymes (edited by KREUTZBERG, G. W., REDDINGTON, M. & ZIMMERMANN, H.), pp. 133–46. Berlin, Heidelberg: Springer.

    Google Scholar 

  • ENG, L. F. (1980) The glial fibrillary acidic (GFA) protein. InProteins of the Nervous System, 2nd edn (edited by BRADSHAW, R. A. & SCHNEIDER, D. M.), pp. 85–117. New York: Raven Press.

    Google Scholar 

  • ENG, L. F. (1985) Glial fibrillary acidic protein (GFAP): the major protein of glial intermediate filaments in differentiated astrocytes.Journal of Neuroimmunology 8, 203–14.

    Google Scholar 

  • ENG, L. F., VANDERHAEGHEN, J. J., BIGNAMI, A. & GERSTL, B. (1971) An acidic protein isolated from fibrous astrocytes.Brain Research 28, 351–4.

    Google Scholar 

  • FRIEDE, R. L. & JOHNSTONE, M. A. (1967) Responses of thymidine labelling of nuclei in gray matter and nerve following sciatic transection.Acta neuropathologica (Berlin) 7, 218–31.

    Google Scholar 

  • GEIGER, B., KREIS, T. E., GIGI, O., SCHMID, E., MITTNACHT, S., JORCANO, J. L., BASSEWITZ, D. B. VON & FRANKE, W. W. (1984) Dynamic rearrangements of cytokeratins in living cells. InCancer Cells. Proceedings of the 1. Cancer Cell Conference, Cold Spring Harbor, 1983. The Transformed Phenotype, Vol. 1 (edited by LEVINE, A. J., VANDE WOUDE, G. F., TOPP, W. C. & WATSON, J. D.), pp. 201–15. Cold Spring Harbor: Cold Spring Harbor Laboratory.

    Google Scholar 

  • GERLACH, E. & BECKER, B. F. (1987)Topics and Perspectives in Adenosine Research. Berlin, Heidelberg, New York: Springer.

    Google Scholar 

  • GRAEBER, M. B. & KREUTZBERG, G. W. (1986) Astrocytes increase in glial fibrillary acidic protein during retrograde changes of facial motor neurons.Journal of Neurocytology 15, 363–73.

    Google Scholar 

  • HOLGATE, S. T., CUSHLEY, M. J., RAFFERTY, P., BEASLEY, R., PHILLIPS, G. & CHURCH, M. K. (1987) The bronchoconstrictor activity of adenosine in asthma. InTopics and Perspectives in Adenosine Research (edited by GERLACH, E. & BECKER, B. F.), pp. 614–24. Berlin, Heidelberg, New York: Springer.

    Google Scholar 

  • HOLLÄNDER, H. (1981) Target preparation for histochemical studies with the electron microscope.Science Tools 28, 8–10.

    Google Scholar 

  • IANNONE, M. A., ZIMMERMAN, T. P., REYNOLDS-VAUGHN, R. & WOLBERG, G. (1987) Effects of adenosine on human neutrophil function and cyclic AMP content. InTopics and Perspectives in Adenosine Research (edited by GERLACH, E. & BECKER, B. F.), pp. 286–98. Berlin, Heidelberg, New York: Springer.

    Google Scholar 

  • KALNINS, V. I., SUBRAHMANYAN, L. & OPAS, M. (1986) The cytoskeleton. InAstrocytes. Cell Biology and Pathology of Astrocytes, Vol. 3 (edited by FEDOROFF, S. & VERNADAKIS, A.), pp. 27–60. New York, London, Tokyo: Academic Press.

    Google Scholar 

  • KARLSSON, U. & SCHULTZ, R. L. (1965) Fixation of the central nervous system for electron microscopy by aldehyde perfusion.Journal of Ultrastructure Research 12, 160–86.

    Google Scholar 

  • KERNS, J. M. & HINSMAN, E. J. (1973) Neuroglial response to sciatic neurectomy. II. Electron microscopy.Journal of Comparative Neurology 151, 255–80.

    Google Scholar 

  • KIRKPATRICK, J. B. (1968) Chromatolysis in the hypoglossal nucleus of the rat: an electron microscopic analysis.Journal of Comparative Neurology 132, 189–212.

    Google Scholar 

  • KREUTZBERG, G. W. (1966) Autoradiographische Untersuchung über die Beteiligung von Gliazellen an der axonalen Reaktion im Facialiskern der Ratte.Acta neuropathologica (Berlin) 7, 149–61.

    Google Scholar 

  • KREUTZBERG, G. W. (1967) DNA metabolism in glial cells during retrograde changes. InMacromolecules and the Function of the Neuron (edited by LODIN, Z. & ROSE, S. P. R.), pp. 51–7. Amsterdam: Excerpta Medica.

    Google Scholar 

  • KREUTZBERG, G. W. (1968) Über perineuronale Mikrogliazellen (Autoradiographische Untersuchungen).Acta neuropathologica (Berlin), Suppl.4, 141–5.

    Google Scholar 

  • KREUTZBERG, G. W. & BARRON, K. D. (1978) 5′-Nucleotidase of microglial cells in the facial nucleus during axonal reaction.Journal of Neurocytology 7, 601–10.

    Google Scholar 

  • KREUTZBERG, G. W., BARRON, K. D. & SCHUBERT, P. (1978) Cytochemical localization of 5′-nucleotidase in glial plasma membranes.Brain Research 158, 247–57.

    Google Scholar 

  • KUNO, M. & LLINAS, R. (1970) Alterations of synaptic action in chromatolysed motoneurones of the cat.Journal of Physiology 210, 823–38.

    Google Scholar 

  • LONDOS, C. (1987) On multiple targets for fat cell receptors. InTopics and Perspectives in Adenosine Research (edited by GERLACH, E. & BECKER, B. F.), pp. 239–48. Berlin, Heidelberg, New York: Springer.

    Google Scholar 

  • LUX, H. D. & SCHUBERT, P. (1975) Some aspects of the electroanatomy of dendrites. InAdvances in Neurology, Vol. 12,Physiology and Pathology of Dendrites (edited by KREUTZBERG, G. W.), pp. 29–44. New York: Raven Press.

    Google Scholar 

  • MATTHEWS, M. R. & NELSON, V. H. (1975) Detachment of structurally intact nerve endings from chromatolytic neurones of rat superior cervical ganglion during the depression of synaptic transmission induced by postganglionic axotomy.Journal of Physiology 245, 91–135.

    Google Scholar 

  • MESCHER, M. F., JOSE, M. J. L. & BALK, S. P. (1981) Actin-containing matrix associated with the plasma membrane of murine tumour and lymphoid cells.Nature 289, 139–44.

    Google Scholar 

  • NISSL, F. (1894) Über eine neue Untersuchungsmethode des Centralorgans speziell zur Feststellung der Lokalisation der Nervenzellen.Zentralblatt für Nervenheilkunde und Psychiatrie 17, 337–44.

    Google Scholar 

  • PURVES, D. (1975) Functional and structural changes in mammalian sympathetic neurones following interruption of their axons.Journal of Physiology 252, 429–63.

    Google Scholar 

  • REISERT, I., WILDEMANN, G., GRAB, D. & PILGRIM, Ch. (1984) The glial reaction in the course of axon regeneration: a stereological study of the rat hypoglossal nucleus.Journal of Comparative Neurology 229, 121–8.

    Google Scholar 

  • RIESKE-SHOWS, E., TETZLAFF, W., CZLONKOWSKA, A., GRAEBER, M. & KREUTZBERG, G. W. (1987) Microglia in culture. InGlial-Neuronal Communication in Development and Regeneration (edited by ALTHAUS, H. H. & SEIFERT, W.) NATO ASI Series H, Vol. 2, pp. 41–51. Heidelberg, New York: Springer.

    Google Scholar 

  • RODAN, G. A., BOURRET, L. A. & CUTLER, L. S. (1977) Membrane changes during cartilage maturation. Increase in 5′-nucleotidase and decrease in adenosine inhibition of adenylate cyclase.Journal of Cell Biology 72, 493–501.

    Google Scholar 

  • SCHOEN, S. W., GRAEBER, M. B., TOTH, L. & KREUTZBERG, G. W. (1988) 5′-Nucleotidase in postnatal ontogeny of rat cerebellum: a marker for migrating nerve cells?Developmental Brain Research 39, 125–36.

    Google Scholar 

  • SCHUBERT, P., LEE, K., REDDINGTON, M. & KREUTZBERG, G. W. (1983) Synaptic modulation by adenosine: electrophysiological and biochemical characteristics. InRegulatory Function of Adenosine (edited by BERNE, R. M., RALL, T. W. & RUBIO, R.), pp. 439–54. The Hague, Boston, London: Martinus Nijhoff.

    Google Scholar 

  • SJÖSTRAND, J. (1965) Proliferative changes in glial cells during nerve regeneration.Zeitschrift für Zellforschung und mikroskopische Anatomie 68, 481–93.

    Google Scholar 

  • SJÖSTRAND, J. (1971) Neuroglial proliferation in the hypoglossal nucleus after nerve injury.Experimental Neurology 30, 178–89.

    Google Scholar 

  • STEFANOVIC, V., MANDEL, P. & ROSENBERG, A. (1976) Ecto-5′-nucleotidase of intact cultured C6 rat glioma cells.Journal of Biological Chemistry 251, 3900–5.

    Google Scholar 

  • STREIT, W. J. & KREUTZBERG, G. W. (1987) Lectin binding by resting and reactive microglia.Journal of Neurocytology 16, 249–60.

    Google Scholar 

  • STREIT, W. J. & KREUTZBERG, G. W. (1988) The response of endogenous glial cells to motor neuron degeneration induced by toxic ricin.Journal of Comparative Neurology,268, 248–63.

    Google Scholar 

  • SUMNER, B. E. H. & SUTHERLAND, F. I. (1973) Quantitative electron microscopy on the injured hypoglossal nucleus in the rat.Journal of Neurocytology 2, 315–28.

    Google Scholar 

  • TETZLAFF, W., GRAEBER, M. B., BISBY, M. A. & KREUTZBERG, G. W. (1988) Increased glial fibrillary acidic protein synthesis in astrocytes during retrograde reaction of the rat facial nucleus.Glia 1, 90–5.

    Google Scholar 

  • TORVIK, A. & SKJÖRTEN, F. (1971) Electron microscopic observations on nerve cell regeneration and degeneration after axon lesions. II. Changes in the glial cells.Acta neuropathologica (Berlin) 17, 265–81.

    Google Scholar 

  • TORVIK, A. & SÖREIDE, A. J. (1972) Nerve cell regeneration after axon lesions in newborn rabbits.Journal of Neuropathology and Experimental Neurology 31, 683–95.

    Google Scholar 

  • UUSITALO, R. J. & KARNOVSKY, M. J. (1977) Surface localization of 5′-nucleotidase on the mouse lymphocyte.Journal of Histochemistry and Cytochemistry 25, 87–96.

    Google Scholar 

  • WACHSTEIN, M. & MEISEL, E. (1957) Histochemistry of hepatic phosphatases at a physiologic pH with special reference to the demonstration of bile canaliculi.American Journal of Clinical Pathology 27, 13–23.

    Google Scholar 

  • WATSON, W. E. (1965) An autoradiographic study of the incorporation of nucleic-acid precursors by neurones and glia during nerve regeneration.Journal of Physiology 180, 741–53.

    Google Scholar 

  • WIDNELL, C. C., SCHNEIDER, Y. J., PIERRE, B., BAUDHUIN, P. & TROUET, A. (1982) Evidence for a continual exchange of 5′-nucleotidase between the cell surface and cytoplasmic membranes in cultured rat fibroblasts.Cell 28, 61–70.

    Google Scholar 

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  1. Department of Neuromorphology, Max Planck Institute for Psychiatry, Am Klopferspitz 18a, 8033, Martinsried-Munich, Germany

    Manuel B. Graeber & Georg W. Kreutzberg

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  1. Manuel B. Graeber
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  2. Georg W. Kreutzberg
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Graeber, M.B., Kreutzberg, G.W. Delayed astrocyte reaction following facial nerve axotomy. J Neurocytol 17, 209–220 (1988). https://doi.org/10.1007/BF01674208

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