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Schwann cells responding to primary demyelination in vivo express p75NTR and c-erbB receptors: a light and electron immunohistochemical study

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Journal of Neurocytology

Abstract

We have used quantitative and qualitative light microscope immunohistochemistry to examine the expression of p75NTR and c-erbB receptors in Schwann cells in a demyelinating lesion induced by the intraneural injection of lysophosphatidyl choline (LPC). We report that levels of p75NTR, c-erbB2 and c-erbB4, as assessed using image analysis of immuno-peroxidase labelled sections, and c-erbB3, as assessed by eye, increased within each lesion site soon after the initiation of myelinolysis, peaked between 5 and 8 days after induction of demyelination and fell to undetectable levels at the onset of remyelination. Pre-embedding immunoelectron microscopy confirmed that Schwann cells ensheathing demyelinated axons were p75NTR positive. Immunolabel decorated overlapping processes of neighbouring Schwann cells, suggesting that in this context p75NTR could play a role in juxtacrine signalling between reacting cells. We conclude that upregulation of p75NTR and c-erbB receptors is a constitutive Schwann cell response to an acute disruption of the axon–Schwann cell relationship.

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References

  • Anton, E. S., Weskamp, G. Reichardt, L. F. & Matthew, W. D. (1994) Nerve growth factor and its low affinity receptor promote Schwann cell migration. Proceedings of the National Academy of Sciences, USA 91, 2795–9.

    Google Scholar 

  • Banerjee, A., Roach, M. C., Trcka, P. Luduena, R. F. (1992) Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of beta-tubulin. Journal of Biological Chemistry 265, 1794–9.

    Google Scholar 

  • Bannerjee, S. A. & Patterson, P. H. (1995) Schwann cell CD9 expression is regulated by axons. Molecular and Cellular Neuroscience 6, 462–73.

    PubMed  Google Scholar 

  • Benedetti, M., Levi, A. & Chao, M. V. (1993) Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proceedings of the National Academy of Sciences, USA 90, 7859–63.

    Google Scholar 

  • Bolin, L. M. & Shooter, E. M.(1993) Neurons regulate Schwann cell genes by diffusible molecules. Journal of Cell Biology 123, 237–43.

    PubMed  Google Scholar 

  • Bravo, R. & Macdonald-Bravo, H. (1987) Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. Journal of Cell Biology 105, 1549–54.

    PubMed  Google Scholar 

  • Byers, M. R., Kvinnsland, I. & Bothwell, M. (1992) Analysis of low affinity nerve growth factor receptor during pulpal healing and regeneration of myelinated and unmyelinated axons in replanted teeth. Journal of Comparative Neurology 326, 470–84.

    PubMed  Google Scholar 

  • Carraway III, K. L. & Cantley, L. C. (1994) A neu acquaintance for erbB3 and erbB4: a role for receptor heterodimerization in growth signalling. Cell 78, 5–8.

    PubMed  Google Scholar 

  • Carraway III, K. L. & Burden, S. J. (1995) Neuregulins and their receptors. Current Opinion in Neurobiology 5, 606–12.

    PubMed  Google Scholar 

  • Carroll, S. L., Miller, M. L., Frohnert, P. W., Kim, S. S. & Corbett, J. A. (1997) Expression of neuregulins and their putative receptors, erbB2 and erbB3, is induced during Wallerian degeneration. Journal of Neuroscience 17, 1642–59.

    PubMed  Google Scholar 

  • Cassacia-Bonnefil, P., Carter, B. D., Dobrowsky, R. T. & Chao, M. V. (1996) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383, 716–19.

    PubMed  Google Scholar 

  • Clark, M. B., Zeheb, R., White, T. K., & Bunge, R. P. (1991) Schwann cell plasminogen activator is regulated by neurons. Glia 4, 514–28.

    PubMed  Google Scholar 

  • Cohen, J. A., Yachnis, A. T., Arai, M., Davis, J. G. & Scherer, S. S. (1992) Expression of the neu protooncogene by Schwann cells during peripheral nerve development and Wallerian degeneration. Journal of Neuroscience Research 31, 622–34.

    PubMed  Google Scholar 

  • Conti, G., Baron, P. L., Scarpini, E., Vedeler, C., Rostami, A., Pleasure, D. & Scarlato, G. (1995) Low-affinity nerve growth factor receptor expression in sciatic nerve during P2-peptide induced experimental allergic neuritis. Neuroscience Letters 199, 135–8.

    PubMed  Google Scholar 

  • Curtis, R., Stewart, H. J. S., Hall, S. M., Wilkin, G. P., Mirsky, R. & Jessen, K. R. (1992) GAP-43 is expressed by nonmyelin-forming Schwann cells of the peripheral nervous system. Journal of Cell Biology 116, 1455–64.

    PubMed  Google Scholar 

  • Curtis, R., Adryan, K. M., Stark, J. L., Park, J. S., Compton, D. L., Weskamp, G., Huber, L, J., Chao, M. V., Jaenisch, R., et al. (1995) Differential role of the low affinity neurotrophin receptor (p75) in retrograde axonal transport of the neurotrophins. Neuron 14, 1201–11.

    PubMed  Google Scholar 

  • Dobrowsky, R. T., Werner, M. H., Castellino, A. M., Chao, M. V. & Hannun, Y. A. (1994) Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 265, 15–9.

    PubMed  Google Scholar 

  • Dong, Z., Brennan, A., Liu, N., Yarden, Y., Lefkowitz, G., Mirsky, R. & Jessen, K. R. (1995) Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15, 585–96.

    PubMed  Google Scholar 

  • Doyu, M., Sobue, G., Ken, E., Kimata, K.

  • Shinomura, T., Yamada, Y., Mitsuma, T. & Takahashi, A. (1993) Laminin A, B1, and B2 chain gene expression in transected and regenerating nerves: regulation by axonal signals. Journal of Neurochemistry 60, 543–51.

    PubMed  Google Scholar 

  • Ekstrom, P. A. (1995) Neurones and glial cells of the mouse sciatic nerve undergo apoptosis after injury in vivo and in vitro. Neuroreport 6, 1029–32.

    PubMed  Google Scholar 

  • Falls, D. L., Rosen, K. M., Corfas, G., Lane, W. S. & Fischbach, G. D. (1993) ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72, 801–15.

    PubMed  Google Scholar 

  • Fann, X. & Gelman, B. B. (1992) Schwann cell nerve growth factor receptor expression during initiation of remyelination. Journal of Neuroscience Research 31, 58–67.

    PubMed  Google Scholar 

  • Frade, J. M., Rodriguez-Tebar, A. & Barde, Y. A. (1996) Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 383, 166–8.

    PubMed  Google Scholar 

  • Geisert, E. E. Jr. & Frankfurter, A. (1989) The neuronal response to injury as visualised by immuno-staining of class III b-tubulin in the rat. Neuroscience Letters 102, 137–41.

    PubMed  Google Scholar 

  • Gregson, N. A. & Hall, S. M. (1973) A quantitative analysis of the effects of the intraneural injection of lysophosphatidyl choline. Journal of Cell Science 13, 257–77.

    PubMed  Google Scholar 

  • Griffin, J. W., Stocks, E. A., Fahnestock, M., Van Praagh, A. & Trapp, B. D. (1990) Schwann cell proliferation following lysolecithin-induced demyelination. Journal of Neurocytology 19, 367–84.

    PubMed  Google Scholar 

  • Grinspan, J. B., Marchionni, M. A., Reeves, M., Coulaloglou, M. & Scherer, S. S. (1996) Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. Journal of Neuroscience 16, 6107–118.

    PubMed  Google Scholar 

  • Hall, S. M. (1988) Neurotoxic effects of lysolecithin, mouse, rat. In Monographs on Pathology of Laboratory Animals. Nervous System (edited by Jones, T. C., Mohr, U. & Hunt, R. D.) pp. 63–73. Berlin: Springer-Verlag.

    Google Scholar 

  • Hall, S. M. & Gregson, N. A. (1971) The in vivo and ultrastructural effects of injection of lysophosphatidyl choline into myelinated peripheral nerve fibres of the adult mouse. Journal of Cell Science 9, 769–89.

    PubMed  Google Scholar 

  • Hempstead, B. L., Martin-Zanca, D., Kaplan, D. R., Parada, L. F. & Chao, M. V. (1991) Coexpression of the trk proto-oncogene and the low-affinity NGF receptor required for high-affinity NGF binding. Nature 350, 678–83.

    PubMed  Google Scholar 

  • Heumann, R., Korsching, S., Bandtlow, C. & Thoenen, H. (1986) Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. Journal of Cell Biology 104, 1623–31.

    Google Scholar 

  • Heumann, R., Lindholm, D., Bandtlow, C., Meyer, M., Radeke, M. E., Misko, T. P., Shooter, E. M. & Thoenen, H. (1987) Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerves during development, degeneration and regeneration. Proceedings of the National Academy of Sciences, USA 84, 8735–9.

    Google Scholar 

  • Holmes, W. E., Sliwkowski, M. X., Akita, R. W., Henzel, W. J., Lee, J., Park, J. W., Yansura, D., Abadi, N., Raab, H., Lewis, G. D., Shepard, M., Kuang, W. J., Wood, W. I., Goeddel, D. V. & Vandlen, R. L. (1992) Identification of heregulin, a specific activator of p185erbB2. Science 256, 1205–10.

    PubMed  Google Scholar 

  • JESSEN, K. R., BRENNAN, A., MORGAN, L., MIRSKY, R., KENT, A., HASHIMOTO,Y. & GAVRILOVIC, J. (1994) The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron 12, 509–27.

    PubMed  Google Scholar 

  • Jessen, K. R., Mirsky, R. & Morgan, L. (1987) Axonal signals regulate the differentiation of nonmyelin-forming Schwann cells: an immunohistochemical study of galactocerebroside in transected and regenerating nerves. Journal of Neuroscience 7, 3362–9.

    PubMed  Google Scholar 

  • Jessen, K. R., Morgan, L., Stewart, H. J. S. & Mirsky, R. (1990) Three markers of adult nonmyelin-forming Schwann cells, (Ran-1), A5E3 and GFAP: development and regulation by neuron- Schwann cell interactions. Development 109, 91–103.

    PubMed  Google Scholar 

  • Jing, S., Tapley, P. & Barbacid, M. (1992) Nerve growth factor mediates signal transduction through trk homodimer receptors. Neuron 9, 67–79.

    Google Scholar 

  • Korsching, S. (1993) The neurotrophic factor concept: a re-examination. Journal of Neuroscience 13, 2739–48.

    PubMed  Google Scholar 

  • Kuecherer-ehret, A., Graeber, M. B., Edgar, D., Thoenen, H. & Kreutzberg, G. W. (1990) Immunoelectron microscopic localization of laminin in normal and regenerating mouse sciatic nerve. Journal of Neurocytology 19, 101–9.

    PubMed  Google Scholar 

  • Lefcort, F., Venstrom, K., Mcdonald, J. A. & Reichardt, L. F. (1992) Regulation of expression of fibronectin and its receptor alpha 5 beta 1, during development and regeneration of peripheral nerve. Development 116, 767–82.

    PubMed  Google Scholar 

  • Lemke, G. & Chao, M. (1988) Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development 102, 499–504.

    PubMed  Google Scholar 

  • Levi, A. D. O., Bunge, R. P., Lofgren, J. A., Meima, L., Hefti, F., Nikolics, K. & Sliwkowski, M. X. (1995) The influence of heregulins on human Schwann cell proliferation. Journal of Neuroscience 15, 1329–40.

    PubMed  Google Scholar 

  • Levi-montalcini, R., Skaper, S. D., Toso, R. D., Petrelli, L. & Leon, A. (1996) Nerve growth factor: from neurotrophin to neurokin. Trends in Neuroscience 19, 514–20.

    Google Scholar 

  • Li, H., Newcombe, J. & Cuzner, M. L. (1993) Characterization and distribution of phagocytic macrophages in multiple sclerosis plaques. Neuropathology and Applied Neurobiology 19, 214–23.

    PubMed  Google Scholar 

  • Li, H., Terenghi, G. & Hall, S. M. (1997) The effects of delayed re-innervation on the expression of c-erbB receptors by chronically denervated rat Schwann cells in vivo. Glia 20, 333–47.

    PubMed  Google Scholar 

  • Mahanthappa, N. K., Anton, E. S. & Matthew, W. D. (1996) Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. Journal of Neuroscience 16, 4673–83.

    PubMed  Google Scholar 

  • Marchionni, M. A., Goodearl, A. D. J., Chen, M. S., Bermingham-mcdonogh, O., Kirk, C., Hendricks, M., Danehy, F., Misumi, D., Sudhalter, J., Kobayashi, K., Wroblewski, D., Lynch, C., Baldassare, M., Hiles, I., Davis, J. B., Hsuan, J. J., Totty, N. F., Otsu, M., Mcburney, R. N., Waterfield, M. D., Stroobant, P. & Gwynne, D. (1993) Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362, 312–18.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Mason, P., Neuberger, T., Attema, B. & De vries, G. (1993) Regulation of neu expression in Schwann celldorsal root ganglion co-cultures. Society of Neuroscience Abstracts 19, 540.8.

    Google Scholar 

  • Matsuoka, I., Meyer, M. & Thoenen, H. (1991) Celltype-specific regulation of nerve growth factor synthesis in non-neuronal cells: comparison with other cell types. Journal of Neuroscience 11, 3165–77.

    PubMed  Google Scholar 

  • Mccormick, D. & Hall, P. A. (1992) The complexities of proliferating cell nuclear antigen. Histopathology 21, 591–4.

    PubMed  Google Scholar 

  • Meyer, D. & Birchmeier, C. (1994) Distinct isoforms of neuregulin are expressed in mesenchymal and neuronal cells during mouse development. Proceedings of the National Academy of Sciences, USA 91, 1064–8.

    Google Scholar 

  • Meyer, D. & Birchmeier, C. (1995) Multiple essential functions of neuregulin in development. Nature 378, 386–90.

    PubMed  Google Scholar 

  • Meyer, M., Matsuoka, I., Wetmore, C. & Thoenen, H. (1992) Enhanced synthesis of brainderived 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.

    PubMed  Google Scholar 

  • Mitchell, L. S., Griffiths, I. R., Morrison, S., Barrie, J. A., Kirkham, A. & Mcphilmey, K. (1990) Expression of myelin protein gene transcripts by Schwann cells of regenerating nerve. Journal of Neuroscience 27, 125–35.

    Google Scholar 

  • Morris, R. J., Barber, P. C., Beech, J. & Raisman, G. (1983) The distribution of Thy-1 antigen in the P.N.S. of the adult rat. Journal of Neurocytology 12, 1017–39.

    PubMed  Google Scholar 

  • Morrissey, T. K., Levi, A. D. O., Nuijens, A., Sliwkowski, M. X. & Bunge, R. P. (1995) Axon-induced mitogenesis of human Schwann cells involves heregulin and p185erbB2. Proceedings of the National Academy of Sciences, USA 92, 1431–5. 688

    Google Scholar 

  • Plowman, G. D., Culouscou, J-M., Whitney, G. S., Green, J. M., Carlton, G. W., Foy, L., Neubauer, M. G. & Shoyab, M. (1993a) Ligandspecific activation of HER4/p180erbB4, a fourth member of the epidermal growth factor receptor family. Proceedings of the National Academy of Sciences, USA 90, 1746–50.

    Google Scholar 

  • Plowman, G. D. Green, J. M. Culouscou, J. M., Carlton, G. W., Rothwell, V. M. & Buckley, S. (1993b) Heregulin induces tyrosine phosphorylation of HER4/p185erbB4. Nature 366, 473–75.

    Article  PubMed  Google Scholar 

  • Raabe, T. D., Clive, D. R., Neuberger, T. J., Wen, D. & Devries, G. H. (1996) Cultured neonatal Schwann cells contain and secrete neuregulins. Journal of Neuroscience Research 46, 263–70.

    PubMed  Google Scholar 

  • Rabizadeh, S., Oh, J., Zhong, L. T., Yang, J., Bitler, C. M., Butcher, L. L. & Bredesen, D. E. (1993) Induction of apoptosis by the low-affinity NGF receptor. Science 261, 345–8.

    PubMed  Google Scholar 

  • Ratner, N., Hong, D., Lieberman, M. A., Bunge, R. P. & Glaser, L. (1988) The neuronal cell-surface molecule mitogenic for Schwann cells is a heparinbinding protein. Proceedings of the National Academy of Sciences, USA 85, 6992–6.

    Google Scholar 

  • Redd, P. E. & Byers, M. R. (1994) Regeneration of junctional epithelium and its innervation in adult rats: a study using immunocytochemistry for p75 nerve growth factor receptor and calcitonin gene-related peptide. Journal of Periodontal Research 29, 214–24.

    PubMed  Google Scholar 

  • Roberson, M. D., Toews, A. D., Bouldin, T. W., Weaver, J., Goines, N. D. & Morell, P. (1995) NGFR-mRNA expression in sciatic nerve: a sensitive indicator of early stages of axonopathy. Molecular Brain Research 28, 231–8.

    PubMed  Google Scholar 

  • Salzer, J. L., Bunge, R. P. & Glaser, L. (1980) Studies of Schwann cell proliferation. III Evidence for the surface localization of the neurite mitogen. Journal of Cell Biology 84, 767–78.

    PubMed  Google Scholar 

  • Schechter, A. L., Hung, M-C., Vaidyanathan, L. & Weinberg, R. A. (1985) The neu gene: An erbB-homologous gene distinct from and unlinked to the gene encoding the EGF receptor. Science 229, 976–78.

    PubMed  Google Scholar 

  • Seilheimer, B. & Schachner, M. (1987) Regulation of neural cell adhesion molecule expression on cultured mouse Schwann cells by nerve growth factor. EMBO Journal 6, 1611–16.

    PubMed  Google Scholar 

  • Shah, N. M., Marchionni, M. A., Isaacs, I., Stroobant, P. & Anderson, D. J. (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349–60.

    PubMed  Google Scholar 

  • Smith, K. J., Bostock, H. & Hall, S. M. (1982) Saltatory conduction precedes remyelination in axons demyelinated with lysophosphatidyl choline. Journal of the Neurological Sciences 54, 13–31.

    PubMed  Google Scholar 

  • Smith, K. J., Hall, S. M. & Schauf, C. L. (1985) Vesicular demyelination induced by raised intracellular calcium. Journal of the Neurological Sciences 71, 19–37.

    PubMed  Google Scholar 

  • Smith, K. J. & Hall, S. M. (1988) Peripheral demyelination and remyelination initiated by the calcium-selective ionophore ionomycin: in vivo observations. Journal of the Neurological Sciences 83, 37–53.

    PubMed  Google Scholar 

  • Steedman, H. F. (1957) Polyester wax. A new ribboning embedding medium for histology. Nature 179, 1345–6.

    PubMed  Google Scholar 

  • Stoll, G., Li, C. Y., Trapp, B. D. & Griffin, J.W. (1993) Expression of NGF receptors during immune-mediated and lysolecithin-induced demyelination of the peripheral nervous system. Journal of Neurocytology 22, 1022–9.

    PubMed  Google Scholar 

  • Sudhalter, J., Whitehouse, L., Rusche, J. R., Marchionni, M. & Mahanthappa, N. K. (1996) Schwann cell heparan sulfate proteoglycans play a critical role in glial growth factor/neuregulin signalling. Glia 17, 28–39.

    PubMed  Google Scholar 

  • Taniuchi, M., Clark, H. B. & Johnson, E. M. (1986) Induction of nerve growth factor receptor in Schwann cells after axotomy. Proceedings of the National Academy of Sciences, USA 83, 4094–8.

    Google Scholar 

  • Thomson, C. E., Griffiths, I. R., Mcullough, M. C., Kyriakides, E., Barrie, J. A. & Montague, P. (1993) In vitro studies of axonally-regulated Schwann cell genes during Wallerian degeneration. Journal of Neurocytology 22, 590–602.

    PubMed  Google Scholar 

  • Toews, A. D., Griffiths, I. R., Kyriakides, E., Goodrum, J. F., Eckermann, C. E., Morell, P. & Thomson, C. E. (1992) Primary demyelination induced by exposure to tellurium alters Schwann cell gene expression: a model for intracellular targeting of NGF receptor. Journal of Neuroscience 12, 3676–87.

    PubMed  Google Scholar 

  • Toma, J. G., Pareek, S., Barker, P., Mathew, T. C., Murphy, R. A., Acheson, A. & Miller, F. D. (1992) Spatiotemporal increases in epidermal growth factor receptors following peripheral nerve injury. Journal of Neuroscience 12, 2504–15.

    PubMed  Google Scholar 

  • Trachtenberg, J. T. & Thompson, W. J. (1995) Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379, 174–7.

    Google Scholar 

  • Tzahar, E., Levkowitz, G., Karunagaran, D., Yi, L., Peles, E., Lavi, S., Chang, D., Liu, N., Yayon, A., Wen, D. & Yarden, Y. (1994) ErbB-3 and erbB-4 function as the respective low and high affinity receptors of all neu differentiation factor/ heregulin isoforms. Journal of Biological Chemistry 269, 25226–33.

    PubMed  Google Scholar 

  • Waseem, N. H., & Lane, P. (1990) Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conservation and the detection of a nucleolar form. Journal of Cell Science 69, 121–9.

    Google Scholar 

  • Wen, D., Peles, E., Cupples, R., Suggs, S. V., Bacus, S. S., Luo, Y., Trail, G., Hu, S., Silbiger, S. M., Levy, R. B., Koski, R. A., Lu, H. S. & Yarden, Y. (1992) Neu differentiation factor: A transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 69, 559–72.

    PubMed  Google Scholar 

  • Whitworth, I. H., Brown, R. A., Dore, C., Green, C. J. & Terenghi, G. (1995) Orientated mats of fibronectin as a conduit material for use in peripheral nerve repair. Journal of Hand Surgery (British Volume) 20, 429–36.

    Google Scholar 

  • Willison, H. J., Trapp, B. D., Bacher, J. D. & Quarles, R. H. (1988) The expression of myelinassociated glycoprotein in regenerating cat sciatic nerve. Brain Research 444, 10–16.

    PubMed  Google Scholar 

  • Wu, W., Mathew, T. C. & Miller, F. D. (1993) Evidence that the loss of homeostatic signals induces regenerationassociated alterations in neuronal gene expression. Developmental Biology 158, 456–66.

    PubMed  Google Scholar 

  • Yamamoto, M., Kondo, H. & Iseki, S. (1992) Nerve growth factor receptor (NGFR)-like immunoreactivity in the perineurial cell in normal and sectioned peripheral nerves of rats. Anatomical Record 233, 301–8.

    PubMed  Google Scholar 

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Hall, S.M., Li, H. & Kent, A.P. Schwann cells responding to primary demyelination in vivo express p75NTR and c-erbB receptors: a light and electron immunohistochemical study. J Neurocytol 26, 679–690 (1997). https://doi.org/10.1023/A:1018502012347

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