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N-acetylated alpha-linked acidic dipeptidase is expressed by non-myelinating Schwann cells in the peripheral nervous system

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Journal of Neurocytology

Summary

n-acetylated alpha-linked acidic dipeptidase is a membrane-bound brain peptidase which cleaves the neuropeptiden-acetyl-aspartyl-glutamate ton-acetyl-aspartate and glutamate. In the present study, we have determined the localization ofn-acetylated alpha-linked acidic dipeptidase in the peripheral nervous system. Using enzyme assays and immunoblotting, we demonstrate that sciatic nerve, phrenic nerve, cervical dorsal root ganglion and superior cervical ganglion containn-acetylated alpha-linked acidic dipeptidase activity as well as ann-acetylated alpha-linked acidic dipeptidase-like protein. Furthermore, we show thatn-acetylated. alpha-linked acidic dipeptidase-like immunoreactivity is extensively co-localized in peripheral nerves with immunoreactivity for glial fibrillary acidic protein, a known marker for non-myelinating Schwann cells. Using electron microscopy, we demonstraten-acetylated alpha-linked acidic dipeptidase-like immunoreactivity in cell membranes of non-myelinating Schwann cells in the superior cervical ganglion. These results show thatn-acetylated alpha-linked acidic dipeptidase is expressed in the peripheral nervous system by non-myelinating Schwann cells. This cellular localization suggests thatn-acetylated alpha-linked acidic dipeptidase may be involved in the signalling between axons and Schwann cells, for example during development or regeneration.

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References

  • Berger, U. V., Carter, R. E. &Coyle, J. T. (1993) Distribution ofn-acetyl-aspartyl-glutamate (NAAG)- and NAALADase-immunoreactivities in peripheral nervous system.Society for Neuroscience Abstracts 9, 920.

    Google Scholar 

  • Blakely, R. D., Ory Lavollee, L., Thompson, R. C. &Coyle, J. T. (1986) Synaptosomal transport of radiolabel fromn-acetyl-aspartyl-[3H]glutamate suggests a mechanism of inactivation of an excitatory neuropeptide.Journal of Neurochemistry 47, 1013–19.

    Google Scholar 

  • Blakely, R. D., Robinson, M. B., Thompson, R. C. &Coyle, J. T. (1988) Hydrolysis of the brain dipeptiden-acetyl-l-aspartyl-l-glutamate: subcellular and regional distribution, ontogeny, and the effect of lesions onn-acetylated-alpha-linked acidic dipeptidase activity.Journal of Neurochemistry 50, 1200–9.

    Google Scholar 

  • Cangro, C. B., Namboodiri, M. A., Sklar, L. A., Corigliano Murphy, A. &Neale, J. H. (1987) Immunohistochemistry and biosynthesis ofn-acetylaspartylglutamate in spinal sensory ganglia.Journal of Neurochemistry 49, 1579–88.

    Google Scholar 

  • Cassidy, M. &Neale, J. H. (1993)n-acetylaspartylglutamate catabolism is achieved by an enzyme on the cell surface of neurons and glia.Neuropeptides 24, 271–8.

    Google Scholar 

  • Coggeshall, R. E., Appelbaum, M. L., Fazen, M., Stubbs, T. B. I. &Sykes, M. T. (1975) Unmyelinated axons in human ventral roots, a possible explanation for the failure of dorsal rhizotomy to relieve pain.Brain 98, 157–66.

    Google Scholar 

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

    Google Scholar 

  • 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 

  • Dyck, P. J. &Hopkins, A. P. (1972) Electron microscopic observations on degeneration and regeneration of unmyelinated fibers.Brain 95, 223–34.

    Google Scholar 

  • Fuhrman, S., Palkovits, M., Cassidy, M. &Neale, J. H. (1994) The regional distribution ofn-acetyl-aspartylglutamate (NAAG) and peptidase activity against NAAG in the rat nervous system.Journal of Neurochemistry 62, 275–81.

    Google Scholar 

  • Jessen, K. R., Morgan, L., Stewart, H. J. &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 

  • Kioussi, C., Crine, P. &Matsas, R. (1992) Endopeptidase-24.11 is suppressed in myelin-forming but not in non-myelin-forming Schwann cells during development of the rat sciatic nerve.Neuroscience 50, 69–83.

    Google Scholar 

  • 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 

  • Meyerhoff, J. L., Carter, R. E., Yourick, D. L., Slusher, B. S. &Coyle, J. T. (1992) Genetically epilepsy-prone rats have increased brain regional activity of an enzyme which liberates glutamate fromn-acetyl-aspartyl-glutamate.Brain Research 593, 140–3.

    Google Scholar 

  • Ory-Lavollee, L., Blakely, R. D. &Coyle, J. T. (1987) Neurochemical and immunocytochemical studies on the distribution ofn-acetyl-aspartylglutamate andn-acetyl-aspartate in rat spinal cord and some peripheral nervous tissues.Journal of Neurochemistry 48, 895–9.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. de F. (1991) The cellular sheaths of neurons. InThe Fine Structure of the Nervous System, pp. 212–72. New York: Oxford University Press.

    Google Scholar 

  • Reynolds, M. L. &Woolf, C. J. (1993) Reciprocal Schwann cell-axon interactions.Current Opinion in Neurobiology 3, 683–93.

    Google Scholar 

  • Robinson, M. B., Blakely, R. D., Couto, R. &Coyle, J. T. (1987) Hydrolysis of the brain dipeptiden-acetyl-l-aspartyl-l-glutamate. Identification and characterization of a noveln-acetylated alpha-linked acidic dipeptidase activity from rat brain.Journal of Biological Chemistry 262, 14498–506.

    Google Scholar 

  • Serval, V., Barbeito, L., Pittaluga, A., Cheramy, A., Lavielle, S. &Glowinski, J. (1990) Competitive inhibition ofn-acetylated-alpha-linked acidic dipeptidase activity byn-acetyl-l-aspartyl-beta-linkedl-glutamate.Journal of Neurochemistry 55, 39–46.

    Google Scholar 

  • Slusher, B. S., Robinson, M. B., Tsai, G., Simmons, M. L., Richards, S. S. &Coyle, J. T. (1990) Rat brainn-acetylated alpha-linked acidic dipeptidase activity. Purification and immunologic characterization.Journal of Biological Chemistry 265, 21297–301.

    Google Scholar 

  • Slusher, B. S., Tsai, G., Yoo, G. &Coyle, J. T. (1992) Immunocytochemical localization of then-acetylaspartyl-glutamate (NAAG) hydrolyzing enzymen-acetylated alpha-linked acidic dipeptidase (NAALA-Dase).Journal of Comparative Neurology 315, 217–29.

    Google Scholar 

  • Stauch, B. L., Robinson, M. B., Forloni, G., Tsai, G. &Coyle, J. T. (1989) The effects ofn-acetylated alphalinked acidic dipeptidase (NAALADase) inhibitors on [3H]NAAG catabolismin vivo. Neuroscience Letters 100, 295–300.

    Google Scholar 

  • Tsai, G., Forloni, G., Robinson, M. B., Stauch, B. L. &Coyle, J. T. (1988) Calcium-dependent evoked release ofn-[3H]acetylaspartylglutamate from the optic pathway.Journal of Neurochemistry 51, 1956–9.

    Google Scholar 

  • Turner, A. J., Matsas, R. &Kenny, A. J. (1985) Are there neuropeptide-specific peptidases?Biochemical Pharmacology 34, 1347–56.

    Google Scholar 

  • Zollinger, M., Amsler, U., Do, K. Q., Streit, P. &Cuenod, M. (1988) Release ofn-acetylaspartylglutamate on depolarization of rat brain slices.Journal of Neurochemistry 51, 1919–23.

    Google Scholar 

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Berger, U.V., Carter, R.E., McKee, M. et al. N-acetylated alpha-linked acidic dipeptidase is expressed by non-myelinating Schwann cells in the peripheral nervous system. J Neurocytol 24, 99–109 (1995). https://doi.org/10.1007/BF01181553

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  • DOI: https://doi.org/10.1007/BF01181553

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