Journal of Neurocytology

, Volume 23, Issue 1, pp 1–28

Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves

  • Rudolf Martini


By combining both immunocytochemical and functional investigations, a hypothetical framework will be developed for the molecular mechanisms underlying neuron-glia interactions during development and regeneration of peripheral nerves. In particular, the immunoglobulin-like molecules L1, N-CAM, MAG and PO, the extracellular matrix molecules laminin and tenascin, and the carbohydrates PSA and L2/HNK-1 will be considered. During early stages of limb bud innervation in embryos, L1 and N-CAM are expressed on axons and Schwann cells and are involved in axonal fasciculation, whereas tenascin is thought to be involved in forming a scaffold around the nerve possibly preventing axons and/or Schwann cells from leaving the nerve. PSA has been shown to be involved in pathway selection at initial stages of limb bud innervation. Later on, when motor axons enter muscles, the carbohydrates determine the branching pattern of the nerves. During myelination, L1 appears to play a pivotal role during the formation of the first Schwann cell loops around the prospective myelin-containing axons. MAG and PO appear also to be functionally involved at initial stages of myelin formation. Additionally, MAG may contribute to the formation and maintenance of non-compacted myelin and axon-Schwann cell apposition whereas PO is involved in myelin compaction. Under regenerative conditions, L1, N-CAM, laminin, and tenascin are strongly up-regulated by denervated Schwann cells.In vitro observations strongly suggest that these molecules might foster axonal regeneration. The carbohydrate PSA is confined to regrowing axons and is also a candidate to support axonal regrowth. L2/HNK-1, which is found on motor axon-associated Schwann cells, may provide regenerating motor axons with a selective advantage over others resulting in appropriate reinnervation of motor pathways. Since many of the functional studies this review refers to have been performedin vitro, some of the conclusions drawn need reexaminationin vivo. Gene manipulations, such as the generation of null mutants followed by a thorough morphological and immunocytochemical investigation may be a powerful tool to resolve this problem.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abo, T. &Balch, C. M. (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1).Journal of Immunology 127, 1024–9.Google Scholar
  2. Aguayo, A. J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. InSynaptic Plasticity (ed.Cotman, C. W.) pp. 457–84 New York: The Guilford Press.Google Scholar
  3. Aguayo, A. J., Charron, L. &Bray, G. M. (1976) Potential of Schwann cells from unmyelinated nerves to produce myelin: a quantitative ultrastructural and radiographic study.Journal of Neurocytology 5, 565–73.Google Scholar
  4. Ariga, T., Kohriyama, T., Freddo, L., Latov, N., Saito, M., Kon, K., Ando, S., Suzuki, M., Hemling, M. E., Rinehart, K. L., Kusunoki, S. &Yu, R. K. (1987) Characterization of sulfated glucuronic acid containing glycolipids reacting with IgM M-proteins in patients with neuropathy.Journal of Biological Chemistry 262, 848–53.Google Scholar
  5. Arquint, M., Roder, J., Chia, L.-S., Down, J., Wilkinson, D., Bayley, H., Braun, P. &Dunn, R. (1987) Molecular cloning and primary structure of myelinassociated glycoprotein.Proceedings of the National Academy of Sciences (USA) 84, 600–4.Google Scholar
  6. Baron-Vanevercooren, A., Kleinmann, H. K., Ohno, S. Marangos, P., Schwartz, J. P. &Dubois-Daecq, M. E. (1982) Nerve growth factor, laminin, and fibronectin promote neurite growth in human fetal sensory ganglia cultures.Journal of Neuroscience Research 8, 179–93.Google Scholar
  7. Barthels, D., Santoni, N. -J., Wille, W., Ruppert, C., Chaix, J.-C., Hirsch, R., Fontecilla-Camps, J. C. &Goridis, C. (1987) Isolation and nucleotide sequence of mouse N-CAM cDNA that codes for a Mr 79000 polypeptide without a membrane-spanning region.EMBO Journal 6, 907–14.Google Scholar
  8. 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.Google Scholar
  9. Bartsch, U., Kirchhoff, F. &Schachner, M. (1989) Immunohistological localization of the adhesion molecules L1, N-CAM, and MAG in the developing and adult optic nerve of mice.Journal of Comparative Neurology 284, 451–62.Google Scholar
  10. 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.Google Scholar
  11. Bhattacharyya, A., Frank, E., Ratner, N. &Brackenbury, R. (1991) P0 is an early marker of the Schwann cell lineage in chickens.Neuron 7, 831–44.Google Scholar
  12. 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.Google Scholar
  13. Bock, E., Richter-Landsberg, C., Faissner, A. &Schachner, M. (1985) Demonstration of immunochemical identity between the nerve growth factorinducible large external (NILE) glycoprotein and the cell adhesion molecule L1.EMBO Journal 4, 2765–8.Google Scholar
  14. Boisseau, S., Nedelec, J., Poirier, V., Rougon, G. &Simonneau, M. (1991) Analysis of high PSA N-CAM expression during mammalian spinal cord and peripheral nervous system development.Development 112, 69–82.Google Scholar
  15. Von Bohlen Und Halbach, F., Taylor, J. &Schachner, M. (1992) Cell type-specific effects of the neural adhesion molecules L1 and N-CAM on diverse second messenger systems.European Journal of Neuroscience 4, 896–909.Google Scholar
  16. Brümmendorf, T., Wolff, J. M., Frank, R. &Rathjen, F. G. (1989) Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains.Neuron 2, 1351–61.Google Scholar
  17. Brushart, T. M. (1988) Preferential reinnervation of motor nerves by regenerating motor axons.Journal of Neuroscience 8, 1026–31.Google Scholar
  18. Brushart, T. M. (1990) Preferential motor reinnervation: a sequential double-labelling study.Restorative Neurology and Neuroscience 1, 281–7.Google Scholar
  19. Brushart, T. M. (1993) Motor axons preferentially reinnervate motor pathways.Journal of Neuroscience,13, 2730–8.Google Scholar
  20. Brushart, T. M., Martini, R. &Schachner, M. (1992) Expression of L2/HNK-1 in reinnervated peripheral nerve.Society for Neuroscience Abstracts 18, 1462.Google Scholar
  21. Bunge, R. P., Bunge, M. B. &Eldridge, C. F. (1986) Linkage between axonal ensheathment and basal lamina production by Schwann cells.Annual Review of Neuroscience 9, 305–28.Google Scholar
  22. Bunge, R. P., Bunge, M. B. &Bates, M. (1989) Movements of the Schwann cell nucleus implicate progession of the inner (axon-related) Schwann cell process during myelination.Journal of Cell biology 109, 273–84.Google Scholar
  23. Capecchi, M. R. (1989) Altering the genome by homologous recombination.Science 244, 1288–92.Google Scholar
  24. Carpenter, E. M. &Hollyday, M. (1992) The location and distribution of neural crest-derived Schwann cells in developing peripheral nerves in the chick forelimb.Developmental Biology 150, 144–59.Google Scholar
  25. Chiquet, M. (1989) Tenascin/J1/cytotactin: the potential function of hexabrachion proteins in neural development.Developmental Neuroscience 11, 266–75.Google Scholar
  26. Chiquet-Ehrismann, R. (1990) What distinguishes tenascin from fibronectin?FASEB Journal 4, 2598–604.Google Scholar
  27. Chou, D. K. H., Ilyas, A. A., Evans, J. E., Costello, C., Quarles, R. H. &Jungalwala, F. B. (1986) Structure of sulfated glucuronyl glycolipids in the nervous system reacting with HNK-1 antibody and some IgM paraproteins in neuropathy.Journal of Biological Chemistry 261, 11717–25.Google Scholar
  28. Chou, K. H., Ilyas, A. A., Evans, J. E., Quarles, R. H. &Jungalwala, F. B. (1985) Structure of a glycolipid reacting with monoclonal IgM in neuropathy and with HNK-1.Biochemical and Biophysical Research Communication 128, 383–8.Google Scholar
  29. Cravioto, H. (1965) The role of Schwann cells in the development of human peripheral nerves. An electron microscopic study.Journal of Ultrastructure Research 12, 634–51.Google Scholar
  30. Cunningham, B. A. &Edelman, G. M. (1990) Structure, expression, and cell surface modulation of cell adhesion molecules. InMorphoregulatory molecules (ed. byEdelman, G. M., Cunningham, B. A. &Thiery, J.-P.), pp. 9–40. New York: John Wiley & Sons.Google Scholar
  31. Cunningham, B. A., Hoffman, S., Rutishauser, U., Hemperly, J. J. &Edelman, G. M. (1983) Molecular topography of the neural cell adhesion molecule N-CAM: surface orientation and location of sialic acid-rich and binding regions.Proceedings of the National Academy of Sciences (USA) 80, 3116–20.Google Scholar
  32. Cunningham, B. A., Hemperly, J. J., Murray, B. A., Prediger, E. A., Brackenbury, R. &Edelman, G. M. (1987) Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing.Science 236, 799–806.Google Scholar
  33. Dahm, L. M. &Landmesser, L. T. (1988) The regulation of intramuscular nerve branching during normal development and following activity blockade.Developmental Biology 130, 621–44.Google Scholar
  34. Daniloff, J. K., Levi, G., Grumet, M., Rieger, F. &Edelman, G. M. (1986) Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair.Journal of Cell Biology 103, 929–45.Google Scholar
  35. 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.Google Scholar
  36. Davies, J. A., Cook, G. M. W., Stern, C. D. &Keynes, R. J. (1990) Isolation from chick somites of a glycoprotein fraction that causes collapse of dorsal root ganglion growth cones.Neuron 2, 11–20.Google Scholar
  37. D'Urso, D., Brophy, P. J., Staugaitis, S. M., Gillespie, C. S., Frey, A. B., Stempak, J. G. &Colman, D. R. (1990) Protein zero of peripheral nerve myelin: biosynthesis, membrane insertion, and evidence for homotypic interaction.Neuron 2, 449–60.Google Scholar
  38. Engvall, E., Earwicker, D., Haaparanta, T., Ruoslahti, E. &Sanes, J. R. (1990) Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits.Cell Regulation 1, 731–40.Google Scholar
  39. 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.Google Scholar
  40. Fawcett, J. W. &Keynes, R. J. (1990) Peripheral nerve regeneration.Annual Review of Neuroscience 13, 43–60.Google Scholar
  41. Filbin, M. T., Walsh, F. S., Trapp, B. D., Pizzey, J. A. &Tennekoon, G. I. (1990) Role of myelin P0 protein as a homophilic adhesion molecule.Nature 344, 871–2.Google Scholar
  42. Finne, J. (1990) The carbohydrate units of nervous tissue glycoproteins: Structural properties and role in cell interactions. InMorphoregulatory Molecules (ed.Edelman, G. M., Cunningham, B. A. &Thiery, J.-P.), pp. 81–116. New York: John Wiley & Sons.Google Scholar
  43. Fischer, G., Künemund, V. &Schachner, M. (1986) Neurite outgrowth in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1.Journal of Neuroscience 6, 602–12.Google Scholar
  44. Frail, D. E. &Braun, P. E. (1984) Two developmentally regulated messenger RNAs differing in their coding region may exist for the myelin-associated glycoprotein.Journal of Biological Chemistry 259, 14857–62.Google Scholar
  45. Frail, D. E., Webster, H. Def. &Braun, P. E. (1985) Developmental expression of the myelin-associated glycoprotein in the peripheral nervous system is different from that in the central nervous system.Journal of Neurochemistry 45, 1308–10.Google Scholar
  46. Galileo, D. S., Majors, J., Horwitz, A. F. &Sanes, J. R. (1992) Retrovirally introduced antisense integrin RNA inhibits neuroblast migrationin vivo.Neuron 9, 1117–31.Google Scholar
  47. 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.Google Scholar
  48. Goridis, C., Hirn, M., Santoni, M.-J., Gennarini, G., Deagostini-Bazin, H., Jordan, B. R., Kiefer, M. &Steinmetz, M. (1985) Isolation of mouse N-CAM-related cDNA: detection and cloning using monoclonal antibodies.EMBO Journal 4, 631–35.Google Scholar
  49. Greenfield, S., Brostoff, S., Eylar, E. H. &Morell, P. (1973) Protein composition of myelin in the peripheral nervous system.Journal of Neurochemistry 20, 1207–16.Google Scholar
  50. Grumet, M. &Edelman, G. M. (1984) Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific neuron-glia cell adhesion molecule.Journal of Cell Biology 98, 1746–56.Google Scholar
  51. Grumet, M., Hoffman, S., Chuong, C.-M. &Edelman, G. M. (1984) Polypeptide components and binding functions of neuron-glia cell adhesion molecules.Proceedings of the National Academy of Sciences (USA) 81, 7989–93.Google Scholar
  52. 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.Google Scholar
  53. Gupta, S. K., Poduslo, J. F., Dunn, R., Roder, J. &Mezei, C. (1990) Myelin-associated glycoprotein gene expression in the presence and absence of Schwann cell-axonal contact.Developmental Neuroscience 12, 22–33.Google Scholar
  54. Hahn, A. F., Whitaker, J. N., Kachar, B. &Webster, H. Def. (1987) P2, P1, and P0 myelin protein expression in developing rat sixth nerve: a quantitative immunocyto-chemical study.Journal of Comparative Neurology 260, 501–12.Google Scholar
  55. Hall, S. M. (1989) Regeneration in the peripheral nervous system.Neuropathology and Applied Neurobiology 15, 513–29.Google Scholar
  56. Hlavin, M. L. &Lemmon, V. (1991) Molecular structure and functional testing of human L1CAM: an interspecies comparison.Genomics 11, 416–23.Google Scholar
  57. Hoffman, S. &Edelman, G. M. (1983) Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule.Proceedings of the National Acadenty of Sciences (USA) 80, 5762–6.Google Scholar
  58. Hunter, D. D., Porter, B. E., Bulock, J. W., Adams, S. P., Merlie, J. P. &Sanes, J. R. (1989a) Primary sequence of a motor neuron-selective adhesive site in the synaptic basal lamina protein s-laminin.Cell 59, 905–13.Google Scholar
  59. Hunter, D. D., Shah, V., Merlie, J. P. &Sanes, J. R. (1989b) A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction.Nature 338, 229–34.Google Scholar
  60. Hunter, D. D., Cashman, N., Morris-Valero, R., Bulock, J. W., Adams, S. P. &Sanes, J. R. (1991) An LRE (leucine-arginine-glutamate)-dependent mechanism for adhesion of neurons to S-laminin.Journal of Neuroscience 11, 3960–71.Google Scholar
  61. Husmann, K., Faissner, A. &Schachner, M. (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in fibronectin type III repeats.Journal of Cell Biology 116, 1475–86.Google Scholar
  62. Ide, C., Tohyama, K., Yokota, R., Nitatori, T. &Onodera, S. (1983) Schwann cell basal lamina and nerve regeneration.Brain Research 288, 61–75.Google Scholar
  63. Ilyas, A. A., Quarles, R. H. &Brady, R. O. (1984) The monoclonal antibody HNK-1 reacts with a human peripheral nerve ganglioside.Biochemical and Biophysical Research Communication 122, 1206–11.Google Scholar
  64. Inuzuka, T., Fujita, N., Sato, S., Baba, H., Nakano, R., Ishiguro, H. &Miyyatake, T. (1991) Expression of the large myelin-associated glycoprotein in the mouse peripheral nervous system.Brain Research 562, 173–5.Google Scholar
  65. Jessell, T. M., Hynes, M. A. &Dodo, J. (1990) Carbohydrates and carbohydrate-binding proteins in the nervous system.Annual Review of Neuroscience 13, 227–55.Google Scholar
  66. Jessen, K. R. &Mirsky, R. (1991) Schwann cell precursors and their development.Glia 4, 185–94.Google Scholar
  67. Jessen, K. R. &Mirsky, R. (1992) Schwann cells: early lineage, regulation of proliferation and control of myelin formation.Current Opinion in Neurobiology 2, 575–81.Google Scholar
  68. Jessen, K. R., Mirsky, R. &Morgan, L. (1987) Myelinated, but not unmyelinated axons, reversibly down-regulate N-CAM in Schwann cells.Journal of Neurocytology 16, 681–8.Google Scholar
  69. Jessen, K. R., Morgan, L., Stewart, H. J. S. &Mirsky, R. (1990) Three markers of adult non-myelin-forming Schwann cells, 217c (Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions.Development 109, 91–103.Google Scholar
  70. Johnson, P. W., Abramow-Newerly, W., Seilheimer, B., Sadoul, R., Tropak, M. B., Arquint, M., Dunn, R. J., Schachner, M. &Roder, J. C. (1989) Recombinant myelin-associated glycoprotein confers neural adhesion and neurite outgrowth function.Neuron 3, 377–85.Google Scholar
  71. 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.Google Scholar
  72. Kioussi, C., Crine, P. &Matsas, R. (1992) Endopeptidase-24.11. is suppressed in myelin-forming but not in nonmyelin forming Schwann cells during development of the rat sciatic nerve.Neuroscience 50, 69–83.Google Scholar
  73. Kücherer-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.Google Scholar
  74. Künemund, V., Jungalwala, F. B., Fischer, G., Chou, D. K. H., Keilhauer, G. &Schachner, M. (1988) The L2/HNK-1 carbohydrate of neural cell adhesion molecules is involved in cell interactions.Journal of Cell Biology 106, 213–23.Google Scholar
  75. Kuffler, D. P. (1986) Accurate reinnervation of motor end plates after disruption of sheath cells and muscle fibers.Journal of Comparative Neurology 250, 228–35.Google Scholar
  76. Lai, C., Brow, M. A., Nave, K.-A., Noronha, A. B., Quarles, R. H., Bloom, F. E., Milner, R. J. &Sutcliffe, J. G. (1987a) Two forms of 1B236/myelinassociated glycoprotein, a cell adhesion molecule for postnatal neural development, are produced by alternative splicing.Proceedings of the National Academy of Sciences (USA) 84, 4337–41.Google Scholar
  77. Lai, C., Watson, J. B., Bloom, F. E., Sutcliffe, J. G. &Milner, R. J. (1987b) Neural protein 1B236/myelinassociated glycoprotein (MAG) defines a subgroup of the immunoglobulin superfamily.Immunological Reviews 100, 129–51.Google Scholar
  78. Lander, A. D. (1989) Understanding the molecules of neural cell contacts: emerging patterns of structure and function.Trends in Neurosciences 12, 189–95.Google Scholar
  79. Landmesser, L. T., Dahm, L., Schultz, K. &Rutishauser, U. (1988) Distinct roles for adhesion molecules during innervation of embryonic chick muscle.Developmental Biology 130, 645–70.Google Scholar
  80. Landmesser, L., Dahm, L., Tang, J. &Rutishauser, U. (1990) Polysialic acid as a regulator of intramuscular nerve branching during embryonic development.Neuron 4, 655–67.Google Scholar
  81. 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.Google Scholar
  82. Lemke, G. (1986) Molecular biology of the major myelin genes.Trends in Neurosciences 9, 266–70.Google Scholar
  83. Lemke, G. (1988) Unwrapping the genes of myelin.Neuron 1, 535–43.Google Scholar
  84. Lemke, G. &Axel, R. (1985) Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin.Cell 40, 501–8.Google Scholar
  85. Lemke, G., Lamar, E. &Patterson, J. (1988) Isolation and analysis of the gene encoding peripheral myelin protein zero.Neuron 1, 73–83.Google Scholar
  86. Lemmon, V. &Mcloon, S. C. (1986) The appearance of an L1-like molecule in the chick primary visual pathway.Journal of Neuroscience 6, 2987–94.Google Scholar
  87. 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.Google Scholar
  88. Manthorpe, M., Engvall, E., Ruoslahti, E., Longo, F. M., Davis, G. E. &Varon, S. (1983) Laminin promotes neuritic regeneration from cultured peripheral and central neurons.Journal of Cell Biology 97, 1882–90.Google Scholar
  89. Marinkovich, M. P., Lunstrum, G. P., Keene, D. R. &Burgeson, R. E. (1992) The dermal-epidermal junction of human skin contains a novel laminin variant.Journal of Cell Biology 119, 695–703.Google Scholar
  90. Martin, J. R. &Webster, H. Def. (1973) Mitotic Schwann Cells in developing nerve: their changes in shape, fine structure, and axon relationships.Developmental Biology 32, 417–31.Google Scholar
  91. 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.Google Scholar
  92. 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.Google Scholar
  93. Martini, R. &Schachner, M. (1991) Complex expression pattern of tenascin during innervation of the posterior limb buds of the developing chicken.Journal of Neuroscience Research 28, 261–79.Google Scholar
  94. 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.Google Scholar
  95. 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.Google Scholar
  96. 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.Google Scholar
  97. 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.Google Scholar
  98. Mirsky, R., Jessen, K. R., Schachner, M. &Goridis, C. (1986) Distribution of the adhesion molecules N-CAM and L1 on peripheral neurons and glia in adult rats.Journal of Neurocytology 15, 799–815.Google Scholar
  99. Mitchell, L. S., Griffiths, I. R., Morrison, S., Barrie, J. A., Kirkham, D. &Mcphilemy, K. (1990) Expression of myelin protein gene transcripts by Schwann cells of regenerating nerve.Journal of Neurosdence Research 21, 125–35.Google Scholar
  100. Miura, M., Kobayashi, M., Asou, H. &Uyemura, K. (1991) Molecular cloning of cDNA encoding the rat neural cell adhesion molecule L1. Two L1 isoforms in the cytoplasmic region are produced by differential splicing.FEBS Letters 289, 91.Google Scholar
  101. Moos, M., Tacke, R., Scherer, H., Teplow, D., Früh, K. &Schachner, M. (1988) Neural adhesion molecule L1 is a member of the immunoglobulin superfamily with binding domains similar to fibronectin.Nature 334, 701–3.Google Scholar
  102. Murray, B. A., Hemperly, J. J., Prediger, E. A., Edelman, G. M. &Cunningham, B. A. (1986) Alternatively spliced mRNAs code for different polypeptide chains of the chicken neural cell adhesion molecule (N-CAM).Journal of Cell Biology 102, 189–93.Google Scholar
  103. Nathaniel, E. J. H. &Pease, D. C. (1963) Regenerative changes in rat dorsal roots following Wallerian degeneration.Journal of Ultrastructure Research 9, 533–49.Google Scholar
  104. 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 transsection of mouse sciatic nerve.Differentiation 30, 141–51.Google Scholar
  105. Noakes, P. G. &Bennett, M. R. (1987) Growth of axonsinto developing muscles of the chick forelimb is preceded by cells that stain with Schwann cell antibodies.Journal of Comparative Neurology 259, 330–47.Google Scholar
  106. Noakes, P. G., Bennett, M. R. &Stratford, J. (1988) Migration of Schwann cells and axons into developing chick forelimb muscles following removal of either the neural tube or the neural crest.Journal of Comparative Neurology 277, 214–33.Google Scholar
  107. Noronha, A., Ilyas, A., Antonicek, H., Schachner, M. &Quarles, R. H. (1986) Molecular specificity of L2 monoclonal antibodies that bind to carbohydrate determinants of neural cell adhesion molecules and their resemblance to other monoclonal antibodies recognizing the myelin-associated glycoprotein.Brain Research 385, 237–44.Google Scholar
  108. Oakley, R. A. &Tosney, K. W. (1991) Peanut agglutinin and chondroitin-6-sulfate are molecular markers for tissues that act as barriers to axon advance in the avian embryo.Developmental Biology 147, 187–206.Google Scholar
  109. Onda, H., Poulin, M. L., Tassava, R. A. &Chili, I.-M. (1991) Characterization of a newt tenascin cDNA and localization of tenascin mRNA during newt limb regeneration by in situ hybridization.Developmental Biology 148, 219–32.Google Scholar
  110. Owens, G. C. &Bunge, R. P. (1989) Evidence for an early role for myelin-associated glycoprotein in the process of myelination.Glia 2, 119–28.Google Scholar
  111. Owens, G. C. &Bunge, R. P. (1990) Schwann cells depleted of galactocerebroside express myelin-associated glycoprotein and initiate but do not continue the process of myelination.Glia 3, 118–24.Google Scholar
  112. Owens, G. C. &Bunge, R. P. (1991) Schwann cells infected with a recombinant retrovirus expressing myelin-associated glycoprotein antisense RNA do not form myelin.Neuron 7, 565–75.Google Scholar
  113. Owens, G. C., Boyd, C. J., Bunge, R. P. &Salzer, J. L. (1990) Expression of recombinant myelin-associated glycoprotein in primary Schwann cells promotes the initial investment of axons by myelinating Schwann cells.Journal of Cell Biology 111, 1171–82.Google Scholar
  114. Perry, V. H. &Brown, M. C. (1992) Role of macrophages in peripheral nerve degeneration and repair.BioEssays 14, 401–6.Google Scholar
  115. Peters, A. &Muir, A. R. (1959) The relationship between axons and Schwann cells during development of peripheral nerves in the rat.Quarterly Journal of Experimental Physiology 44, 117–30.Google Scholar
  116. Peters, A., Palay, S. L. &Webster, H. Def. (1991)The Fine Structure of the Nervous System. New York, Oxford. Oxford University Press.Google Scholar
  117. Poltorak, M., Sadoul, R., Keilhauer, G., Landa, C., Fahrig, T. &Schachner, M. (1987) Myelin-associated glycoprotein, a member of the L2/HNK-1 family of neural cell adhesion molecules, is involved in neuron-oligodendrocyte and oligodendrocyte-oligodendrocyte interaction.Journal of Cell Biology 105, 1893–9.Google Scholar
  118. Prieto, A. L., Jones, F. S., Cunningham, B. A., Crossin, K. L. &Edeeman, G. M. (1990) Localization during development of alternatively spliced forms of cytotactin mRNA byin situ hybridization.Journal of Cell Biology 111, 685–98.Google Scholar
  119. Prince, J. T., Aeberti, L., Healy, P. A., Nauman, S. J. &Stallcup, W. B. (1991) Molecular cloning of NILE glycoprotein and evidence for its continued expression in mature rat CNS.Journal of Neuroscience Research 30, 567–81.Google Scholar
  120. Quarles, R. H. (1984) Myelin-associated glycoprotein in development and disease.Developmental Neuroscience 6, 285–303.Google Scholar
  121. Quarles, R. H. &Trapp, B. D. (1984) Localization of myelin-associated glycoprotein.Journal of Neurochemistry 43, 1773–4.Google Scholar
  122. Quarles, R. H., Barbarash, G. R., Figlewicz, D. A. &Mcintyre, L. J. (1983) Purification and partial characterization of the myelin-associated glycoprotein from adult rat brain.Biochimica Biophysica Acta 757, 140–3.Google Scholar
  123. Ramon Y Cajal, S. (1928)Degeneration and Regeneration of the Nervous System Vol. 1. translated by R. M. May, London: Oxford University Press.Google Scholar
  124. Ranscht, B. &Bronner-Fraser, M. (1991) T-cadherin expression alternates with migrating neural crest cells in the trunk of the avian embryo.Development 111, 15–22.Google Scholar
  125. Rathjen, F. G. (1988) A neurite outgrowth-promoting molecule in developing fiber tracts.Trends in Neurosciences 11, 183–4.Google Scholar
  126. 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.Google Scholar
  127. Rathjen, F. G., Wolff, J. M., Frank, R., Bonhöfer, F. &Rutishauser, U. (1987) Membrane glycoproteins involved in neurite fasciculation.Journal of Cell Biology 104, 343–53.Google Scholar
  128. Reichardt, L. F. &Tomaselli, K. J. (1991) Extracellular matrix molecules and their receptors: functions in neural development.Annual Review of Neuroscience 14, 531–70.Google Scholar
  129. Remsen, L. G., Strain, G. M., Newman, M. J., Satterlee, N. &Daniloff, J. K. (1990) Antibodies to the neural cell adhesion molecule disrupt functional recovery in injured nerves.Experimental Neurology 110, 268–73.Google Scholar
  130. 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.Google Scholar
  131. Rogers, S. L., Letourneau, P. C., Palm, S. L., Mccarthy, J. &Furcht, L. T. (1983) Neurite extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin.Developmental Biology 98, 212–20.Google Scholar
  132. Rutishauser, U. &Goridis, C. (1986) NCAM: the molecule and its genetics.Trends in Genetics 2, 72–6.Google Scholar
  133. Rutishauser, U. &Jessell, T. M. (1988) Cell adhesion molecules in vertebrate neural development.Physiological Reviews 68, 819–57.Google Scholar
  134. Rutishauser, U. &Landmesser, L. (1991) Polysialic acid on the surface of axons regulates patterns of normal and activity-dependent innervation.Trends in Neurosciences 14, 528–32.Google Scholar
  135. Sadoul, R., Hirn, M., Deagostini-Bazin, H., Rougon, G. &Goridis, C. (1983) Adult and embryonic mouse neural cell adhesion molecules have different binding properties.Nature 304, 347–9.Google Scholar
  136. Sadoul, R., Fahrig, T., Bartsch, U. &Schachner, M. (1990) Binding properties of liposomes containing the myelin-associated glycoprotein MAG to neural cell cultures.Journal of Neuroscience Research 25, 1–13.Google Scholar
  137. Saga, Y., Tsukamoto, T., Jing, N., Kusakabe, M. &Sakakura, T. (1991) Murine tenascin: cDNA cloning, structure and temporal expression of isoforms.Gene 104, 177–85.Google Scholar
  138. Salzer, J. L., Holmes, W. P. &Colman, D. R. (1987) The amino acid sequences of the myelin-associated glycoproteins: homology to the immunoglobulin gene superfamily.Journal of Cell Biology 104, 957–65.Google Scholar
  139. Sandrock, A. W. &Matthew, W. D. (1987a) Identification of a peripheral nerve neurite growth-promoting activity by development and use of anin vitro bioassay.Proceedings of the National Academy of Sciences (USA) 84, 6934–8.Google Scholar
  140. Sandrock, A. W. &Matthew, W. D. (1987b) Anin vitro neurite promoting antigen functions in axonal regenerationin vivo.Science 237, 1605–8.Google Scholar
  141. Sanes, J. R. (1989) Extracellular matrix molecules that influence neural development.Annual Review of Neuroscience 12, 491–516.Google Scholar
  142. Sanes, J. R. (1993) Topographic maps and molecular gradients.Current Opinion in Neurobiology 3, 67–74.Google Scholar
  143. Sanes, J. R., Engvall, E., Butkowski, R. &Hunter, D. D. (1990) Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere.Journal of Cell Biology 111, 1685–99.Google Scholar
  144. Schachner, M. (1990) Functional implications of glial cell recognition molecules.Seminars in the Neurosciences 2, 497–507.Google Scholar
  145. Schachner, M., Antonicek, H., Fahrig, T., Faissner, A., Fischer, G., Künemund, V., Martini, R., Meyer, A., Persohn, E., Pollerberg, E., Probstmeier, R., Sadoul, K., Sadoul, R., Seilheimer, B. &Thor, G. (1990) Families of cell adhesion molecules. InMorphoregulatory Molecules (edited byEdelman, G. M., Cunningham, B. A. &Thiery, J.-P.), pp. 443–68. New York: J. Wiley & Sons.Google Scholar
  146. Scherer, S. S. &Easter, S. S. (1984) Degenerative and regenerative changes in the trochlear nerve of goldfish.Journal of Neurocytology 13, 519–65.Google Scholar
  147. Schneider-Schaulies, J., Brunn, A.Von &Schachner, M. (1990) Recombinant peripheral myelin protein P0 confers both adhesion and neurite outgrowth-promoting properties,Journal of Neuroscience Research 27, 286–97.Google Scholar
  148. Schnell, L. &Schwab, M. E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors.Nature 343, 269–72.Google Scholar
  149. Schuch, U., Lohse, M. J. &Schachner, M. (1989) Neural cell adhesion molecules influence second messenger systems.Neuron 3, 13–20.Google Scholar
  150. Schwab, M. E., Kapfhammer, J. P. &Bandtlow, C. E. (1993) Inhibitors of neurite growth.Annual Reviews of Neuroscience 16, 565–95.Google Scholar
  151. Schwarting, G. A., Jungalwala, F. B., Chou, D. K. H., Boyer, A. M. &Yamamoto, M. (1987) Sulfated glucuronic acid-containing glycoconjugates are temporally and spatially regulated antigens in the developing mammalian nervous system.Developmental Biology 120, 65–76.Google Scholar
  152. 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.Google Scholar
  153. Seilheimer, B., Persohn, E. &Schachner, M. (1989) Antibodies to the L1 adhesion molecule inhibit Schwann cell ensheathment of neuronsin vitro.Journal of Cell Biology 109, 3095–103.Google Scholar
  154. Small, S. J., Shull, G. E., Santoni, M.-J. &Akeson, R. (1987) Identification of a cDNA clone that contains the complete coding sequence for a 140-kD rate N-CAM polypeptide.Journal of Cell Biology 105, 2335–45.Google Scholar
  155. 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.Google Scholar
  156. Stappert, J. &Kemler, R. (1993) Intracellular associations of adhesions molecules.Current Opinion in Neurobiology 3, 60–6.Google Scholar
  157. Stemple, D. L. &Anderson, D. J. (1991) A Schwann cell antigen recognized by monoclonal antibody 217c is the rat low-affinity nerve growth factor receptor.Neuroscience Letters 124, 57–60.Google Scholar
  158. Tacke, R. &Martini, R. (1990) Changes in expression of mRNA specific for cell adhesion molecules (L1 and NCAM) in the transected peripheral nerve of the adult rat.Neuroscience Letters 120, 227–30.Google Scholar
  159. Takeichi, M. (1990) Cadherins: a molecular family important in selective cell-cell adhesion.Annual Review of Biochemistry 59, 237–52.Google Scholar
  160. Tanaka, H., Agata, A. &Obata, K. (1989) A new membrane antigen revealed by monoclonal antibodies is associated with motoneuron axonal pathways.Developmental Biology 132, 419–35.Google Scholar
  161. Tang, J., Landmesser, L. &Rutishauser, U. (1992) Polysialic acid influences specific pathfinding by avian motoneurons.Neuron 8, 1031–44.Google Scholar
  162. Tosney, K. W. (1991) Cells and cell-interactions that guide motor axons in the developing chick embryo.BioEssays 13, 17–23.Google Scholar
  163. Tosney, K. W. &Landmesser, L. T. (1985) Development of the major pathways for neurite outgrowth in the chick hindlimb.Developmental Biology 109, 193–214.Google Scholar
  164. Tosney, K. W. &Oakley, R. A. (1990) The perinotochordal mesenchyme acts as a barrier to axon advance in the chick embryo: implications for a general mechanism of axonal guidance.Experimental Neurology 109, 75–89.Google Scholar
  165. Trapp, B. D. &Quarles, R. H. (1984) Immunocytochemical localization of the myelin-associated glycoprotein: Fact or artifact?Journal of Neuroimmunology 6, 231–49.Google Scholar
  166. Trapp, B. D., O'connell, M. F. &Andrews, S. B. (1986) Ultrastructural immunolocalization of MAG and P0 proteins in cryosections of peripheral nerve.Journal of Cell Biology 103, 228a.Google Scholar
  167. Wang, G.-Y., Hirai, K.-I. &Shimada, H. (1992) The role of laminin, a component of Schwann cell lamina, in rat sciatic nerve regeneration within antiserum-treated nerve grafts.Brain Research 570, 116–25.Google Scholar
  168. Webster, H. Def., Martin, J. R. &O'connell, M. F. (1973) The relationships between interphase Schwann cells and axons before myelination: a quantitative electron microscopic study.Developmental Biology 32, 401–16.Google Scholar
  169. Wehrle, B. &Chiquet, M. (1990) Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowthin vitro.Development 110, 401–15.Google Scholar
  170. 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.Google Scholar
  171. Weinberg, H. J. &Spencer, P. S. (1975) Studies on the control of myelinogenesis. I. Myelination of regenerating axons after entry into a foreign unmyelinated nerve.Journal of Neurocytology 4, 395–418.Google Scholar
  172. 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.Google Scholar
  173. Williams, L. R., Longo, F. M., Powell, H. C., Lungborg, G. &Varon, S. (1983) Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: parameters for a bioassay.Journal of Comparative Neurology 218, 460–70.Google Scholar
  174. Willison, H. J., Trapp, B. D., Bacher, J. D. &Quarles, R. H. (1988) The expression of myelin-associated glycoprotein in regenerating cat sciatic nerve.Brain Research 444, 10–16.Google Scholar
  175. Wood, P. M., Schachner, M. &Bunge, R. P. (1990) Inhibition of Schwann cell myelinationin vitro by antibody to the L1 adhesion molecule.Journal of Neuroscience 10, 3635–45.Google Scholar
  176. Yip, J. W. &Yip, Y. P. L. (1992) Laminin-developmental expression and role in axonal outgrowth in the peripheral nervous system of the chick.Developmental Brain Research 68, 23–33.Google Scholar
  177. Zhang, H., Miller, R. H. &Rutishauser, U. (1992) Polysialic acid is required for optimal growth of axons on a neuronal substrate.Journal of Neuroscience 12, 3107–14.Google Scholar
  178. Zhang, Y., Campbell, G., Anderson, P. A., 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 13, 1509.Google Scholar
  179. Ziskind-Conhaim, L. (1988) Physiological and morphological changes in developing peripheral nerves of rat embryos.Developmental Brain Research 42, 15–28.Google Scholar

Copyright information

© Chapman and Hall Ltd 1994

Authors and Affiliations

  • Rudolf Martini
    • 1
  1. 1.Department of NeurobiologySwiss Federal Institute of Technology Zürich, HönggerbergZürichSwitzerland

Personalised recommendations