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. 2002 Nov 13;24(1):105–112. doi: 10.1016/0165-5728(89)90104-5

Early major histocompatibility complex (MHC) class I antigen induction in hypothalamic supraoptic and paraventricular nuclei in trypanosome-infected rats

M Schultzberg 1,∗, T Olsson 2, E-B Samuelsson 1, J Maehlen 1, K Kristensson 1
PMCID: PMC7119864  PMID: 2681260

Abstract

Sprague-Dawley rats were injected intraperitoneally with a suspension of Trypanosoma brucei. An early induction of major histocompatibility complex (MHC) class I antigens as well as an infiltration of macrophage-like and cytotoxic T-cells was detected with immunohistochemical techniques in circumventricular organs, such as the median eminence, neurohypophosis, subformical organ, pineal gland and area postrema. These areas, which lack a blood-brain barrier, correspond to those showing early invasion of trypanosomes. In addition, there was a marked induction of MHC class I in neurons in two hypothalamic nuclei, The paraventricular and supraoptic nuclei. Neurons in these two nuclei are located behind the blood-brain, but project to the neurohypophysis and to the medain eminence, thereby exposing their axon terminals to factors circulating in the blod or released locally from invading trypanosomes or from macrophages or cytotoxic T-cells. It is suggested that the alteration in the nerve cell bodies in the hypothalamic nuclei is caused by retrograde axonal signals from these target areas.

Sleeping sickness; Trypanosomes; Paraventricular nucleus; Major histocompatibility complex classI

References

  1. Armstrong W. Hypothalamic supraoptic and paraventricular nuclei. In: Paxinos G., editor. The Rat Nervous Systmem. Academic Press; Sydney: 1985. pp. 119–128. [Google Scholar]
  2. Askonas A.B., Bancroft G.J. Interacation of African trypasomes with the immune system. Philos. Trans. R. Soc. Lond. (Biol.) 1984;307:41–50. doi: 10.1098/rstb.1984.0107. [DOI] [PubMed] [Google Scholar]
  3. Barclay A.N. The localization of populations of lymphocytes by monoclonal antiobodies in rat lymphoid tissues. Immunology. 1981;42:593–600. [PMC free article] [PubMed] [Google Scholar]
  4. Berkenbosch F., van Oers J., del Rey A., Tilders F., Besedovsky H. Corticotropin-releasing factor-producing neurons in the rat activated by interleukin-1. Science. 1987;258:524–526. doi: 10.1126/science.2443979. [DOI] [PubMed] [Google Scholar]
  5. Blalock J.E. Opinion. The immune system as a sensory organ. Immunology. 1984;132:1067–1970. [PubMed] [Google Scholar]
  6. Brideau R.J., Cancer P.B., McMaster W.r., Mason D.W., Williams A.f. Two subsets of rat T lymphocytes defined with monoclonal antibodies. Eur. J. Immunol. 1980;10:609–614. doi: 10.1002/eji.1830100807. [DOI] [PubMed] [Google Scholar]
  7. Dallman M.J., Thomas M.L., Green J.R. MRC Ox19: a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur. J. Immunol. 1984;14:260–267. doi: 10.1002/eji.1830140311. [DOI] [PubMed] [Google Scholar]
  8. Dausset J., Contu L. Hum. Immunol.Is the MHC a general self-recognition system playing a major unifying role in an organism? 1980;1:5–17. doi: 10.1016/0198-8859(80)90004-x. [DOI] [PubMed] [Google Scholar]
  9. Doherty P.C. T cells and viral infections. Br. Med. Bull. 1985;41:7–14. doi: 10.1093/oxfordjournals.bmb.a072028. [DOI] [PubMed] [Google Scholar]
  10. Frierz W., Endler B., Reske K., Wekerle H, Fontana A. Astrocytes as antigen-presenting cells. I. Induction of Ia antigen expresion on astrocytes by T cells via immune interferon and its effect on antigen presentation. J. Immunol. 1985;134:3785–3793. [PubMed] [Google Scholar]
  11. Fontana A., Frei K, Bodmer K., Hofer E. Immune-mediating encephalitis: on the role of antigen-presenting cells in brain tissue. Immunol. Rev. 1987;100:185–201. doi: 10.1111/j.1600-065X.1987.tb00532.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fukumoto T., McMaster W.R., Williams a.F. Mouse monoclonal antibodies against rat major histocompatibility antigens. Two Ia antigens in rat thymus. Eur. J. Immunol. 1982;12:237–243. doi: 10.1002/eji.1830120313. [DOI] [PubMed] [Google Scholar]
  13. Hirsch M.-R., Wietzerbvin J., Pierres M., Goridis C. Expression of Ia antigens by cultur4ed astrocytes treated with gamma-interferon. Neurosci. Lett. 1983;41:199–204. doi: 10.1016/0304-3940(83)90247-1. [DOI] [PubMed] [Google Scholar]
  14. Holmdahl R., Olsson T., Moran T., Moran T., Klareskog L. Scand. J. Immunol. 1985;22:157–169. doi: 10.1111/j.1365-3083.1985.tb01868.x. [DOI] [PubMed] [Google Scholar]
  15. Kaplow L.S. Substitute for benzidine in myeloleroxidase strains. Am. J. Clin. Pathol. 1975;63:451. doi: 10.1093/ajcp/63.3.451. [DOI] [PubMed] [Google Scholar]
  16. Kriegler M., Perez C., Defay K., Albert I., Lu S.D. A novel form of TNF/cachetin is a cell surface cvytotoxic trsndmembrane protein: ramificatins for the complex physiology of TNF. Cell. 1988;53:45–53. doi: 10.1016/0092-8674(88)90486-2. [DOI] [PubMed] [Google Scholar]
  17. Kristensson K. Retrograde signaling after nerve injury. In: Elam J.S., Calcalon P., editors. Axonal Transport in Neuronal Growth and Regeneration. Plenum Press; New York: 1984. pp. 31–43. [Google Scholar]
  18. Lampson L.A. Molecular basis of the immune response to neural antigens. Trends Neurosci. 1987;10:211–216. [Google Scholar]
  19. Lavi E., Suzumura A., Zoltick P., Murasko D.M., Silberberg D.H., Weiss S.R. Tumor necrosis factor induces MHC class I antigen expression on mouse astrocytes. J. Neuroimmunol. 1987;16:102. doi: 10.1016/0165-5728(88)90102-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Le J., Vilček J. Biology of disease. Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities. Lab. Invest. 1987;56:234. [PubMed] [Google Scholar]
  21. Lindholm D., Heumann R., Meyer M., Thoenen H. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciateic nerve. Nature. 1987;330:658–659. doi: 10.1038/330658a0. [DOI] [PubMed] [Google Scholar]
  22. Maehlen J., Daa Schröder H., Klareskog L., Olsson T., Kristensson K. Axotomy induces MHC class I antigen expression on rat nerve cells. Neurosci. Lett. 1988;92:8–13. doi: 10.1016/0304-3940(88)90733-1. [DOI] [PubMed] [Google Scholar]
  23. Massa P.T., Dörres R., ter Meulen V. Vol. 84. 1987. Tumor necrosis factor amplifies measles virus-mediated Ia induction on astrocytes; pp. 7242–7245. (Proc. Natl. Acad. Sci. U.S.A.). [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McMaster W.R., Williams A.F. Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur. J. Immunol. 1979;9:426–433. doi: 10.1002/eji.1830090603. [DOI] [PubMed] [Google Scholar]
  25. Olsson T., Maehlen J., Löve A., Klareskog L., Norrby E., Kristensson K. Induction of class I and class II transplantation antigens in rat brain during fata andl non-fatal measles virus infection. J. Neuroimmunol. 1987;16:215–224. doi: 10.1016/0165-5728(87)90076-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Poltera A.A., Hochmann A.A., Rudin W., Lambert P.H. Trypanosoma brucei brucei: a model for cerabral trypanosomiasis in mice — an immunological, histological and electronmicroscopic study. Clin. Exp. Immunol. 1980;40:496–507. [PMC free article] [PubMed] [Google Scholar]
  27. Schutzberg M., Svensson S.B., Undén A., Bartfai T. Interleukin-1-like immunoreactivity in peripheral tissues. J. Neurosci. Res. 1987;18:184–189. doi: 10.1002/jnr.490180126. [DOI] [PubMed] [Google Scholar]
  28. Schultzbert M., Ambatsis M., Samuelsson E.-B., Kristensson K., van Meirvenne N. Spread of Trypanosoma brucei to the nervous system: early attack on circumventricular organs and sensory ganglia. J. Neurosci. Res. 1988;21:56–61. doi: 10.1002/jnr.490210109. [DOI] [PubMed] [Google Scholar]
  29. Silverman A.-J., Pickard G.E. The hypothalamus. In: Emson P.C., editor. Chemical Neuroanatomy. Raven Press; New York: 1983. pp. 295–336. [Google Scholar]
  30. Suzumura A., Lavi E., Weiss S.R., Silberberg D.H. Coronavirus infection induces H-2 antigen expression on oligodendrocytes and astrocytes. Science. 1986;232:991–993. doi: 10.1126/science.3010460. [DOI] [PubMed] [Google Scholar]
  31. Thoenen H., Barde Y.-A. Physiology of nerve growth factor. Physiol. Rev. 1980;60:1284–1335. doi: 10.1152/physrev.1980.60.4.1284. [DOI] [PubMed] [Google Scholar]
  32. Williams A.F., Galfré G., Milstein C. Analysis of cell surfaces by xenogeneic myeloma-hybrid antibodies: differentiation antigens of rat lymphocytes. Cell. 1977;12:663. doi: 10.1016/0092-8674(77)90266-5. [DOI] [PubMed] [Google Scholar]
  33. Wong G.H.W., Bartlett P., Clark-Lewis I., Battye F., Schrader J.W. Inducible expression of H-2 and Ia antigens on brain cells. Nature. 1984;310:688–691. doi: 10.1038/310688a0. [DOI] [PubMed] [Google Scholar]

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