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.
Similar content being viewed by others
References
Ballin RHM, Thomas PK (1968) Electronmicroscopic observations on demyelination and remyelination in experimental allergic neuritis. I. Demyelination. J Neurol Sci 8:1–18
Barclay AN (1981) The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology 42:593–600
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
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
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
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
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
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
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
Gilman SC, Rosenberg JS, Feldman JD (1982) Membrane phenotype of the rat cytotoxic T lymphocyte. J Immunol 129:1012–1016
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
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
Hunt SV, Fowler MH (1981) A repopulation assay for B and T lymphocyte stem cells employing radiation chimeras. Cell Tissue Kinet 14:445
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
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
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
Lampert PW (1969) Mechanism of demyelination in experimental allergic neuritis. Electronmicroscopic studies. Lab Invest 20:127–138
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
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
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
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
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
McMaster WR, Williams AF (1979) Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol 9:426–433
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
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
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
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
Powell HC, Braheny SL, Myers RR, Rodriguez M, Lampert PW (1983) Early changes in experimental allergic neuritis. Lab Invest 48:332–338
Robins RH, Baldwin RW (1985) T cell subsets in tumour rejection. Immunol Today 6:55–58
Saida K, Saida T, Pleasure DE, Nishitani H (1983) P2 protein induced experimental allergic neuritis. An ultrastructural study. J Neurol Sci 62:77–93
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
Sun D, Wekerle H (1986) Ia-restricted encephalitogenic T lymphocytes mediating EAE lyse autoantigen-presenting astrocytes. Nature 320:70–72
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
Swain SL (1983) T cell subsets and the recognition of MHC class. Immunol Rev 74:129
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
Wekerle H, Linington C, Lassmann H, Meyermann R (1986) Cellular immune reactivity within the CNS. Trends Neurosci 9:271–277
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
Wood GS, Turner RR, Shiurba RA, Eng L, Warnke RA (1985) Human dendritic cells and macrophages. Am J Pathol 119:73–82
Author information
Authors and Affiliations
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF00314083