Summary
Interferon-γ-like immunoreactivity was observed in a subpopulation of 16-day-old embryonic rat spinal ganglion neurons using two monoclonal antibodies directed against different epitopes of recombinant interferon-γ. During ontogenesis bothin vivo andin vitro, it was found that the strong immunoreactivity was confined to small neurons when neurons become morphologically distinct on the basis of size.In vivo, the interferon-γ-immunoreactive neurons started to express major histocompatibility complex class I antigens after the first postnatal week, whilein vitro no such antigen could be detected. A quantitative Elisa method was developed to determine the levels of major histocompatibility complex class I and interferon-γin vitro, whereby increased amounts of major histocompatibility complex class I antigen was detected after exposing the cultures to recombinant interferon-γ and Sendai virus. Sendai virus also caused a small increase in interferon-γ with a peak about 12 hours after infection. Thein vitro system will be used to study further the role of the putative neuronal interferon-γ-like molecule in the regulation of cell growth, for induction of major histocompatibility complex antigens and in virus infection of sensory neurons.
Similar content being viewed by others
References
Babbitt, B. P., Allen, P. M., Matsueda, G., Haber, E. &Unanue, E. R. (1985) Binding of immunogenic peptides to la histocompatibility molecules.Nature 317, 359–61.
Brain, S. D. &Williams, T. J. (1988) Substance P regulates the vasodilator activity of calcitonin gene-related peptide.Nature 335, 73–75.
Collart, M. A., Belin, D., Vassali, J.-D., De Korsado, S. &Vassali, P. (1986) Gamma-interferon enhances macrophage transcription of the tumor necrosis factor/cachectin, interleukin-1, and urokinase genase, which are controlled by short-lived repressors.Journal of Experimental Medicine 164, 2113–18.
De Maeyer, E. &De Maeyer-Guignard, J. (1988)Interferons and other Regulatory Cytokines. New York: John Wiley.
Eccleston, P. A., Jessen, K. R. &Mirsky, R. (1989) Transforming growth factor-β and-γ-interferon have dual effects on growth of peripheral glia.Journal of Neuroscience Research 24, 524–30.
Erkman, I., Wuarin, I., Cadell, D. &Kato, A. C. (1989) Interferon induces astrocyte maturation causing an increase in cholinergic properties of cultured human spinal cord cells.Developmental Biology 132, 375–88.
Frei, K. &Fontana, A. (1989) Immune regulatory functions of astrocytes and microglial cells within the central nervous system. InNeuroimmune Networks: Physiology and Diseases (edited byGoetyl, E. J. &Spector, N. H.) pp. 127–36. New York: Alan R. Liss.
Goldberg, M., Belkowski, L. S. &Bloom, B. R. (1989) Regulation of macrophage growth and antiviral activity by Interferon-γ.Journal of Cell Biology 109, 1331–40.
Goldberg, M., Belkowski, L. S. &Bloom, B. R. (1990) Regulation of macrophage function by interferon-γ. Somatic cell genetic approaches in murine macrophage cell lines to mechanisms of growth inhibition, the oxidative burst, and expression of the chronic granulomatous disease gene.Journal of Clinical Investigation 85, 563–9.
Hökfelt, T., Elde, R., Johansson, O., Luft, R., Nilsson, G. &Arimura, A. (1976) Immunohistochemical evidence for separate populations of somatostatincontaining and substance P-containing primary afferent neurons in the rat.Neuroscience 1, 131–6.
Johnson, E. M., Gorin, P. D., Brandeis, L. D. &Pearson, J. (1980) Dorsal root ganglion neurons are destroyed by exposurein utero to maternal antibody to nerve growth factor.Science 210, 916–18.
Kiefer, R. &Kreutzberg, G. W. (1990) Gamma interferonlike immunoreactivity in the rat nervous system.Neuroscience 37, 725–34.
Kingston, A. E., Bergsteinsdottir, K., Jessen, K. R., Van Der Meide, P. H., Colston, M. J. &Mirsky, R. (1989) Schwann cells co-cultured with stimulated T cells and antigen express major histocompatibility complex (MHC) class II determinants without interferon-γ pretreatment: synergistic effects of interferon-γ and tumor necrosis factor on MHC class II induction.European Journal of'Immunology 19, 177–83.
Lampson, L. A. (1987) Molecular basis of the immune response to neural antigens.Trends in Neurosciences 10, 211–16.
Ljungdahl, Å., Olsson, T., Van Der Meide, P. H., Holmdahl, R., Klareskog, L. &Höjeberg, B. (1989) Interferon-gamma-like immunoreactivity in certain neurons of the central and peripheral nervous system.Journal of Neuroscience Research 24, 451–6.
Maehlen, J., Nennesmo, I., Olsson, A-B., Olsson, T., Schröder, H. D. &Kristensson, K. (1989) Peripheral nerve injury causes transient expression of MHC class I antigens in rat motor neurons and skeletal muscles.Brain Research 481, 368–72.
Maehlen, J., Schröder, H. D., Klareskog, L., Olsson, T. &Kristensson, K. (1988) Axotomy induces MHC class I antigen expression on rat nerve cells.Neuroscience Letters 92, 8–13.
Nilsson, J., Von Euler A. M. &Dalsgaard, C-J. (1985) Stimulation of connective tissue cell growth by substance P and substance K.Nature 315, 61–3.
Olsson, T., Kristensson, K., Ljungdahl, A., Maehlen, J., Holmdahl, R. &Klareskog, L. (1989) Gamma-interfer on-like immunoreactivity in axotomized rat motor neurons.Journal of Neuroscience 9, 3870–6.
Oppenheimer-Marks, N. &Ziff, M. (1988) Migration of lymphocytes through endothelial cell monolayers: augmentation by interferon-γ.Cellular Immunology 114, 307–23.
Rosa, F. &Fellous, M. (1984) The effect of gamma interferon on MHC antigens.Immunology Today 5, 261–2.
Sanceau, J., Sondermeyer, P., Beranger, F., Falcoff, R. &Vaquero, C. (1987) Intracellular human γ-interferon triggers an antiviral state in transformed murine L cells.Proceedings of the National Academy of Sciences (USA) 84, 2906–10.
Sotelo, S., Gibbs, C. J., Gajdusek, D. C., Toh, B. H. &Wurth, M. (1980) Method for preparing cultures of central neurons: cytochemical and immunochemical studies.Proceedings of the National Academy of Sciences (USA) 77, 653–7.
Stevens, J. G. (1978) Latent characteristics of selected herpes-viruses.Advances in Cancer Research 26, 227–56.
Streit, W. J., Graeber, M. B. &Kreutzberg, G. W. (1989) Expression of la antigen on perivascular and microglial cells after sublethal and lethal motor neuron injury.Experimental Neurology 105, 115–26.
Tedeshi, B., Barett, J. N. &Keane, R. W. (1986) Astrocytes produce interferon that enhances the expression of H-2 antigens on a subpopulation of brain cells.Journal of Cell Biology 102, 2244–53.
Tirone, F. &Shooter, E. M. (1989) Early gene regulation by nerve growth factor in PC12 cells: Induction of an interferon-related gene.Proceedings of the National Academy of Sciences (USA) 86, 2088–92.
Van Der Meide, P. H., Borman, H. G., Dubbeld, M. A., Botman, C. A. D. &Schellekens, H. (1989) Isolation and characterization of monoclonal antibodies directed to rat interferon-gamma.Eymphokine Research 8, 439–49.
Wong, G. H. W., Bartlett, P. F., Clark-Lewis, I., Battye, F. &Schrader, J. W. (1984) Inducible expression of H-2 and la antigens on brain cells.Nature 310, 688–91.
Wong, G. H. W., Bartlett, P. F., Clark-Lewis, I., McKimm-Breschkin, J. L. &Schrader, J. W. (1985) Interferon-γ induces the expression of H-2 and Ia antigens on brain cells.Journal of Neuroimmunology 7, 255–78.
Yamaguchi, T., Handa, K., Shimizu, Y., Abo, T. &Kumagai, K. (1977) Target cells for interferon production in human leukocytes stimulated by Sendai virus.Journal of Immunology 118, 1931–5.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Eneroth, A., Kristensson, K., Ljungdahl, Å. et al. Interferon-γ-like immunoreactivity in developing rat spinal ganglia neuronsin vivo andin vitro . J Neurocytol 20, 225–231 (1991). https://doi.org/10.1007/BF01186995
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01186995