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Bidirectional signals betweenTrypanosoma brucei brucei and dorsal root ganglion neurons

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Journal of Neurocytology

Summary

The extracellular haemoflagellateTrypanosoma brucei brucei releases a factor, which can induce CD8+ T-cells to produce interferon-γ. Interferon-γ derived from these cells promotes proliferation of the trypanosomes. We now report that these trypanosomes can interact with small neurons in cultures of rat dorsal root ganglia, which contain an interferon-γ like immunoreactive molecule. Cultures of dorsal root ganglia were able to promote the proliferation and survival of the trypanosomes and this growth promoting effect was blocked by monoclonal antibodies against the trypanosome-derived lymphocyte triggering factor, interferon-γ and CD8+ and by Fab-fragments of these antibodies. Living trypanosomes and the factor induced an increase in expression of major histocompatibility complex class I antigens in the cultures; this induction was blocked by Fab fragments of the interferon-γ antibody, indicating that it is mediated by release of the neuronal interferon-γ-like immunoreactive molecule. These data suggest, that the interferon-γ-like immunoreactive molecule in small dorsal root ganglion neurons mimicks certain physiological effects of lymphocyte derived interferon-γ. Furthermore, the trypanosomes and small sensory neurons seem to interact bidirectionally by release of the trypanosome-derived lymphocyte triggering factor and the neuronally derived interferon-γ-like molecule, whereby, perhaps, neuronal disturbances may be elicited and trypanosome proliferation regulated.

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References

  • Adams, J. H., Doua, A., Dago-Akribi, A., Boa, Y. &Haller, L. (1986) Human African trypanosomiasis (T.b. Gambiense): a study of 16 fatal cases of sleeping sickness with some observations on acute reactive arsenical encephalopathy.Neuropathology and Applied Neurobiology 12, 81–94.

    Google Scholar 

  • Bakhiet, M., Olsson, T., Van Der Meide, P. &Kristensson, K. (1990) Depletion of CD8+ T cells suppresses growth of Trypanosoma brucei brucei and interferon-gamma production in infected rats.Clinical and Experimental Immunology 81, 195–9.

    Google Scholar 

  • Bakhiet, M., Olsson, T., Edlund, C., Höjeberg, B., Holmberg, K., Lorentzen, K. &Kristensson, K. (1992) A Trypanosoma brucei brucei derived factor that triggers CD8+ lymphocytes to interferon-γ secretion: purification and characterisation.Scandinavian Journal of Immunology, in press.

  • Birecree, E., King, E. L. &Nanney, L. B. (1991) Epidermal Growth factor and its receptor in the developing human nervous system.Developmental Brain Research 60, 145–54.

    Google Scholar 

  • Brun, R., Jenni, L., Schönenberger, M. &Schell, K.-F. (1981) In vitro cultivation of bloodstream forms of Trypanosoma brucei, T. rhodesiense, and T. gambiense.Journal of Protozoology 28, 470–9.

    Google Scholar 

  • Eneroth, A., Kristensson, K., Ljungdahl, Å. &Olsson, T. (1991) Interferon-γ-like immunoreactivity in developing rat spinal ganglia neuronin vivo andin vitro.Journal of Neurocytology 20, 225–31.

    Google Scholar 

  • Giordano, C. (1973) Les signes neurologiques et electrooncephalo-graphiques de la trypanosomiase humaine africaine.Médecine d'Afrique Noire 20, 317–24.

    Google Scholar 

  • 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.

    Google Scholar 

  • Greenwood, B. M. &Whittle, H. C. (1980) The pathogenesis of sleeping sickness.Transaction of the Royal Society of Tropical Medicine and Hygiene 74, 716–23.

    Google Scholar 

  • Hide, G., Gray, A., Harrison, C. M. &Tait, A. (1989) Identification of an epidermal growth factor receptor homologue in trypanosomes.Molecular and Biochemical Parasitology 36, 51–60.

    Google Scholar 

  • Hirumi, H., Doyle, J. J. &Hirumi, K. (1977) African Trypanosomes: cultivation of animal-infective Trypanosoma bruceiin vitro.Science 196, 992–4.

    Google Scholar 

  • Kiefer, R., Haas, C. A. &Kreutzberg, G. W. (1991) Gamma interferon-like immunoreactive material in rat neurons: evidence against a close relationship to gamma Interferon.Neuroscience 45, 551–60.

    Google Scholar 

  • Ljungdahl, A., 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.

    Google Scholar 

  • Losy, J., Maehlen, J., Olsson, T. &Kristensson, K. (1989) Distribution of leukosialin (W3/13)-like immunoreactivity in the rat central nervous system.Journal of Neurocytology 18, 71–6.

    Google Scholar 

  • Mustafa, M. J., Diener, P., Höjeberg, B., Van Der Meide, P. &Olsson, T. (1991) T cell immunity and interferon-γ-secretion during experimental allergic encephalomyelitis in Lewis rats.Journal of Neuroimmunology 31, 165–77.

    Google Scholar 

  • Olsson, T., Bakhiet, M., Edlund, C., Höjeberg, B., Van Der Meide, P. &Kristensson, K. (1991) Bidirectional activating signals between Trypanosome brucei and CD8+ T cells: a trypanosome-released factor triggers interferon-γ production that stimulates parasite growth.European Journal of Immunology 21, 2447–54.

    Google Scholar 

  • Poltera, A. A., Hochmann, A., Rudin, W. &Lambert, P. H. (1980) Trypanosoma brucei brucei: a model for cerebral trypanosomiasis in mice — an immunological, histological and electronmicroscopic study.Clinical Experimental Immunology 40, 496–507.

    Google Scholar 

  • Schultzberg, M., Ambatsis, M., Samuelsson, E.-B., Kristensson, K. &Van Meirvenne, N. (1988) Spread of Trypanosoma brucei to the nervous system: early attack on circumventricular organs and sensory ganglia.Journal of Neuroscience Research 21, 56–61.

    Google Scholar 

  • Schultzberg, M., Olsson, T., Samuelsson, E. -B., Maehlen, J. &Kristensson, K. (1989) Early major histocompatibility complex (MHC) class I antigen induction in hypothalamic supraoptic and paraventricular nuclei in trypanosome-infected rats.Journal of Neuroimmunology 24, 105–12.

    Google Scholar 

  • Stagsted, J., Reaven, G. M., Hansen, T., Goldstein, A. &Olsson, L. (1990) Regulation of insulin receptor functions by a peptide derived from a major histocompatibility complex class I antigen.Cell 62, 297–307.

    Google Scholar 

  • Tanner, M., Jenni, L., Hecker, H. &Brun, R. (1980) Characterization of Trypanosoma brucei isolated from lymph-nodes of rats.Parasitology 80, 383–91.

    Google Scholar 

  • Tanner, M. (1980) Studies on the mechanisms supporting the continuous growth of Trypanosoma (Trypanozoon) brucei as bloodstream-like form in vitro.Acta Tropica 37, 203–20.

    Google Scholar 

  • Wallach, D., Fellous, M. &Revel, M. (1982) Preferential effects of gammainterferon on the synthesis of HLA antigens and their mRNAs in human cells.Nature 299, 883–6.

    Google Scholar 

  • Weber, R. J., Hill, J. M. &Pert, C. B. (1988) Regional distribution and density of Thy. 1.1. in rat brain and its relation to subpopulations of neurons.Journal of Neuroimmunology 17, 137–45.

    Google Scholar 

  • Williams, A. F. &Gagnon, J. (1982) Neuronal cell Thy-1 glycoprotein: homology with immunoglobulin.Science 216, 696–703.

    Google Scholar 

  • Wiesenfeld-Hallin, Z., Kristensson, K., Samuelsson, E. -B. &Schultzberg, M. (1991) Studies of hyperalgesia induced by Trypanosoma brucei brucei infection in rats.Acta Tropica 48, 215–22.

    Google Scholar 

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Eneroth, A., Bakhiet, M., Olsson, T. et al. Bidirectional signals betweenTrypanosoma brucei brucei and dorsal root ganglion neurons. J Neurocytol 21, 846–852 (1992). https://doi.org/10.1007/BF01191682

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  • DOI: https://doi.org/10.1007/BF01191682

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