Skip to main content
Log in

Major histocompatibility antigens and lymphocyte subsets during experimental allergic neuritis in the Lewis rat

  • Original Investigations
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Summary

Major histocompatibility antigens were identified in frozen sections of normal Lewis rat peripheral nerve tissue with monoclonal antibodies and an avidin-biotin-peroxidase complex system. Class I antigen is normally required for cytotoxic/suppressor T lymphocyte function and class II antigen for activation of helper T lymphocytes. In the sciatic nerves class I antigen was expressed diffusely by most endoneurial and perineurial cells but class II antigen only by a minority. In the cauda equina class I antigen was expressed by all arachnoid and some endoneurial cells, while class II antigen was expressed by a smaller proportion of arachnoid cells in the endoneurium of spinal roots and interstitial cells surrounding dorsal root ganglion neurons. The endothelium of endoneurial, perineurial and meningeal vessels uniformly expressed class I but not class II antigen. Experimental allergic neuritis was induced in Lewis rats by immunisation with bovine intradural root myelin. Early lesions consisted of multifocal infiltration of the nerve roots by cells expressing leucocyte common antigen. Surrounding endoneurial cells showed markedly increased expression of major histocompatibility antigens. In inflammatory lesions about 10% of the cells were stained with pan T cell antibodies. T lymphocyte subsets were identified with antibody W3/25 for helper cells and MRC OX-8 for cytotoxic/suppressor cells. The W3/25 positive cells were usually slightly in excess of OX-8 positive cells and their relative proportions did not alter during the disease. The presence of class I antigen on normal endothelium and its increased expression on endoneurial cells in the early phase of inflammation suggest an important role for class I restricted lymphocytes in the pathogenesis of the early stages of experimental allergic neuritis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Ballin RHM, Thomas PK (1968) Electronmicroscopic observations on demyelination and remyelination in experimental allergic neuritis. I. Demyelination. J Neurol Sci 8:1–18

    Article  Google Scholar 

  2. Barclay AN (1981) The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology 42:593–600

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Barclay AN, Mason DW (1982) Induction of Ia antigen in rat epidermal cells and gut epithelium by immunological stimuli. J Exp Med 156:1665–1676

    Article  CAS  PubMed  Google Scholar 

  4. Booss J, Esiri MM, Wallace WT, Mason DY (1983) Immunohistochemical analysis of T lymphocyte subsets in the central nervous system in chronic progressive multiple sclerosis. J Neurol Sci 62:219–232

    Article  CAS  PubMed  Google Scholar 

  5. Brideau RJ, Carter PB, McMaster WR, Mason DW, Williams AF (1980) Two subsets of rat T lymphocytes defined with monoclonal antibodies. Eur J Immunol 10:609–615

    Article  CAS  PubMed  Google Scholar 

  6. Brosnan JV, Fellowes R, Craggs RI, King RHM, Bowley TJ, Thomas PK (1985) Changes in lymphocyte subsets during the course of EAN. Brain 108:315–334

    Article  PubMed  Google Scholar 

  7. Cantrell DA, Robins RA, Brooks CG, Baldwin RW (1982) Phenotype of rat natural killer cells defined by monoclonal antibodies marking rat lymphocyte subsets. Immunology 45:97–103

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Dallman MJ, Thomas ML, Green JR (1984) MRC OX-19: a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur J Immunol 14:260–267

    Article  CAS  PubMed  Google Scholar 

  9. Fukumoto T, McMaster WR, Williams AF (1982) Mouse monoclonal antibodies against rat major histocompatibility antigens. Two Ia antigens and expression of Ia and Class I antigens in rat thymus. Eur J Immunol 12:237–243

    Article  CAS  PubMed  Google Scholar 

  10. Gilman SC, Rosenberg JS, Feldman JD (1982) Membrane phenotype of the rat cytotoxic T lymphocyte. J Immunol 129:1012–1016

    CAS  PubMed  Google Scholar 

  11. Hart DNJ, Fabre JW (1981) Demonstration and characterization of Ia-positive dendritic cells in the interstitial connective tissues of rat heart and other tissues but not brain. J Exp Med 153:347–361

    Article  Google Scholar 

  12. Hughes RAC, Powell HC (1984) Experimental allergic neuritis: demyelination induced by P2 alone and non-specific enhancement by cerebroside. J Neuropathol Exp Neurol 43:154–161

    Article  CAS  PubMed  Google Scholar 

  13. Hunt SV, Fowler MH (1981) A repopulation assay for B and T lymphocyte stem cells employing radiation chimeras. Cell Tissue Kinet 14:445

    CAS  PubMed  Google Scholar 

  14. Izumo S, Linington C, Wekerle H, Meyermann R (1985) Morphologic study on experimental allergic neuritis mediated by a T cell line specific for bovine P2 protein in Lewis rats. Lab Invest 53:209–218

    CAS  PubMed  Google Scholar 

  15. Johnson P, Williams AF (1986) Striking similarities between antigen receptor J pieces and sequence in the second chain of the murine CD8 antigen. Nature 323:74–76

    Article  CAS  PubMed  Google Scholar 

  16. Kadlubowski M, Hughes RAC, Gregson NA (1980) Experimental allergic neuritis in the Lewis rat: characterization of the activity of peripheral myelin and its major basic protein P2. Brain Res 184:439–454

    Article  CAS  PubMed  Google Scholar 

  17. Lampert PW (1969) Mechanism of demyelination in experimental allergic neuritis. Electronmicroscopic studies. Lab Invest 20:127–138

    CAS  PubMed  Google Scholar 

  18. Linington C, Izumo S, Suzuki M, Ukemura K, Meyermann R, Wekerle H (1984) A permanent rat T cell line that mediates EAN in the Lewis rat in vivo. J Immunol 133:1946–1950

    CAS  PubMed  Google Scholar 

  19. Matsumoto Y, Fujiwara M (1986) In situ detection of Class I and II major histocompatibility antigens in the rat central nervous system during experimental allergic encephalomyelitis. J Neuroimmunol 12:265–277

    Article  CAS  PubMed  Google Scholar 

  20. Matsumoto Y, Hara N, Tanaka R, Fujiwara M (1986) Immunohistochemical analysis of the rat central nervous system during experimental allergic encephalomyelitis, with special reference to Ia-positive cells with dendritic morphology. J Immunol 136:3668–3676

    CAS  PubMed  Google Scholar 

  21. Mason DW, Arthur RP, Dallman MJ, Green JR, Spickett GP, Thomas ML (1983) Functions of rat T-lymphocyte subsets isolated by means of monoclonal antibodies. Immunol Res 74:57–82

    CAS  Google Scholar 

  22. Mayrhofer G, Pugh CW, Barclay AN (1983) The distribution, ontogeny and origin in the rat of Ia positive cells with dendritic morphology and of Ia antigen in epithelia, with special reference to the intestine. Eur J Immunol 13:112–122

    Article  CAS  PubMed  Google Scholar 

  23. McMaster WR, Williams AF (1979) Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol 9:426–433

    Article  CAS  PubMed  Google Scholar 

  24. Olsson T, Holmdahl R, Klareskog L, Forsum U (1983) Ia expressing cells and T lymphocytes of different subsets in peripheral nerve tissue during experimental allergic neuritis in Lewis rats. Scand J Immunol 18:339–343

    Article  CAS  PubMed  Google Scholar 

  25. Olsson T, Holmdahl R, Klareskog L, Forsum U, Kristennson K (1984) Dynamics of Ia-expressing cells and T-lymphocytes of different subsets during experimental allergic neuritis in Lewis rats. J Neurol Sci 66:141–149

    Article  CAS  PubMed  Google Scholar 

  26. Ota K, Ire H, Takahashi K (1987) T cell subsets and Ia-positive cells in the sciatic nerve during the course of experimental allergic neuritis. J Neuroimmunol 13:283–292

    Article  CAS  PubMed  Google Scholar 

  27. Polman CH, Dijkstra CD, Sminia T, Koetsier JC (1986) Immunohistochemical analysis of macrophages in the central nervous system of Lewis rats with acute allergic encephalomyelitis. J Neuroimmunol 11:215–222

    Article  CAS  PubMed  Google Scholar 

  28. Powell HC, Braheny SL, Myers RR, Rodriguez M, Lampert PW (1983) Early changes in experimental allergic neuritis. Lab Invest 48:332–338

    CAS  PubMed  Google Scholar 

  29. Robins RH, Baldwin RW (1985) T cell subsets in tumour rejection. Immunol Today 6:55–58

    Article  CAS  PubMed  Google Scholar 

  30. Saida K, Saida T, Pleasure DE, Nishitani H (1983) P2 protein induced experimental allergic neuritis. An ultrastructural study. J Neurol Sci 62:77–93

    Article  CAS  PubMed  Google Scholar 

  31. Sobel RA, Blanchette BW, Bhan AK, Colvin RB (1984) The immunopathology of experimental allergic encephalomyelitis. II. Endothelial cell Ia increases prior to inflammatory cell infiltration. J Immunol 132:2402–2407

    CAS  PubMed  Google Scholar 

  32. Sun D, Wekerle H (1986) Ia-restricted encephalitogenic T lymphocytes mediating EAE lyse autoantigen-presenting astrocytes. Nature 320:70–72

    Article  CAS  PubMed  Google Scholar 

  33. Sunderland CA, McMaster WR, Williams AF (1979) Purification with monoclonal antibody of a predominant leukocyte-common antigen and glycoprotein from rat thymocytes. Eur J Immunol 9:155–159

    Article  CAS  PubMed  Google Scholar 

  34. Swain SL (1983) T cell subsets and the recognition of MHC class. Immunol Rev 74:129

    Article  CAS  PubMed  Google Scholar 

  35. Waksman BH, Adams RD (1962) A histologic study of the early lesion in experimental allergic encephalomyelitis in the guinea-pig and rabbit. Am J Pathol 41:135–153

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Wekerle H, Linington C, Lassmann H, Meyermann R (1986) Cellular immune reactivity within the CNS. Trends Neurosci 9:271–277

    Article  Google Scholar 

  37. Williams AF, Galfre G, Milstein C (1977) Analysis of cell surfaces by xenogeneic myeloma-hybrid antibodies: differentiation antigens of rat lymphocytes. Cell 12:663–673

    Article  CAS  PubMed  Google Scholar 

  38. Wood GS, Turner RR, Shiurba RA, Eng L, Warnke RA (1985) Human dendritic cells and macrophages. Am J Pathol 119:73–82

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hughes, R.A.C., Atkinson, P.F., Gray, I.A. et al. Major histocompatibility antigens and lymphocyte subsets during experimental allergic neuritis in the Lewis rat. J Neurol 234, 390–395 (1987). https://doi.org/10.1007/BF00314083

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00314083

Key words

Navigation