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T lymphocyte autoimmunity in peripheral nervous system autoimmune disease

  • T Cells in Chronic Inflammation
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Conclusion

Autoaggressive T cells specific for the PNS myelin P2 protein play a central role in the initiation of EAN in the Lewis rat, although there is as yet no direct experimental evidence that the T cells can themselves mediate demyelination in vivo. However, the striking similarities in the pathogenesis of EAN and the Guillain-Barré syndrome suggest that T cell mediated EAN provides an excellent model to study the immunological mechanisms of inflammation and demyelination that are relevant to human PNS disease.

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References

  1. B. H. Waksman and R. D. Adams,Allergic neuritis: An experimental disease of rabbits induced by injection of peripheral nervous tissue and adjuvants. J. Exp. Med.102, 213–234 (1955).

    Article  PubMed  Google Scholar 

  2. B. H. Waksman and R. D. Adams,A comparative study of experimental allergic neuritis in rabbit, guinea pig and mouse. J. Neuropath. Exp. Neurol.15, 293–314 (1956).

    PubMed  Google Scholar 

  3. P. W. Lampert,Mechanisms of demyelination in experimental allergic neuritis.—Electron microscopic studies. Lab. Invest.20, 127–138 (1969).

    PubMed  Google Scholar 

  4. R. H. M. Ballin and P. K. Thomas,Electron-microscopic observations on demyelination and remyelination in experimental allergic neuritis. I. Demyelination., J. Neurol. Sci.8, 1–18 (1969).

    Article  PubMed  Google Scholar 

  5. B. G. W. Arnason, Inflammatory polyradiculoneuritis. In:Peripheral Neuropathy, Vol. 2 (Eds P. J. Dyck, P. K. Thomas and E. H. Lambert). Saunders, Philadelphia 1975.

    Google Scholar 

  6. J. W. Prineas,Pathology of the Guillain-Barré Syndrome. Ann. Neurol. [Suppl.]9, 6–19 (1981).

    Article  PubMed  Google Scholar 

  7. A. Iqbal, J. J. F. Oger and B. G. W. Arnason,Cell mediated immunity in idiopathic polyneuritis. Ann. Neurol.9, 65–69 (1981).

    Article  PubMed  Google Scholar 

  8. B. Zweiman, A. Rostami, R. P. Lisak, A. R. Moskovitz and D. E. Pleasure,Immune reactions to P2 protein in human inflammatory demyelinative neuropathies. Neurology33, 234–237 (1983).

    PubMed  Google Scholar 

  9. C. Linington, S. Izumo, M. Suzuki, K. Uyemura, R. Meyermann and H. Wekerle,A permanent rat T-cell line that mediates experimental allergic neuritis in the Lewis rat in vivo. J. Immunol.133, 1946–1951 (1984).

    PubMed  Google Scholar 

  10. S. Izumo, C. Linington, H. Wekerle and R. Meyermann,A morphological study on experimental allergic neuritis mediated by a T-cell line specific for bovine P2 protein in the Lewos rat. Lab. Invest.53, 209–218 (1985).

    PubMed  Google Scholar 

  11. K. Heininger, G. Stoll, C. Linington, K. V. Toyka and H. Wekerle,Conduction failure and nerve conduction slowing in experimental allergic neuritis induced by P2-specific T-cell lines. Ann. Neurol.19, 44–49 (1986).

    Article  PubMed  Google Scholar 

  12. H. Wekerle, M. Schwab, C. Linington and R. Meyermann,Antigen presentation in the peripheral nervous system: Schwann cells present endogenous myelin autoantigens to lymphocytes. Submitted.

  13. M. E. Smith, L. S. Forno and W. W. Hofmann,Experimental neuritis in the Lewis rat. J. Neuropathol. Exp. Neurol.38, 377–391 (1979).

    PubMed  Google Scholar 

  14. M. Kablubowski and R. A. C. Hughes,Identification of the neuritogen responsible for EAN, Nature277, 140–141 (1979).

    PubMed  Google Scholar 

  15. M. Kablubowski, R. A. C. Hughes and N. A. Gregson,Experimental allergic neuritis in the Lewis rat: characterisation of the activity of peripheral myelin and its major basic protein, P2. Brain Res.184, 439–454 (1980).

    Article  PubMed  Google Scholar 

  16. K. Saida, T. Saida, D. E. Pleasure and H. Nishitani,P2 protein induced experimental allergic neuritis—an ultrastructural study. J. Neurol. Sci.62, 77–93 (1983).

    Article  PubMed  Google Scholar 

  17. D. J. Mikek, H. O. Sarvas, S. Greenfield and S. W. Brostoff,An immunological characterisation of the basic proteins of rodent sciatic nerve myelin. Brain Res.208, 387–396 (1981).

    Article  PubMed  Google Scholar 

  18. R. A. C. Hughes, M. Kablubowski, I. A. Gray and S. Leibowitz,Immune responses in experimental allergic neuritis. J. Neurol. Neurosurg. Psych.44, 565–569 (1981).

    Google Scholar 

  19. I. Szymanska, J. Ramvani and E. H. Eylar,The passive transfer of severe experimental allergic neuritis in the Lewis rat with lymphoid cells preincubated with P2 protein. Cell Immunol.82, 422–425 (1983).

    Article  PubMed  Google Scholar 

  20. A. Ben Nun, H. Wekerle and I. R. Cohen,The rapid isolation of antigen specific T lymphocyte lines capable of mediating experimental autoimmune encephalomyelitis. Eur. J. Immunol.114, 1537–1540 (1981).

    Google Scholar 

  21. C. Linington, A. Mann, S. Izumo, K. Uyemura, R. Meyermann and H. Wekerle,Induction of experimental allergic neuritis in the BN rat: P2 protein specific T cells overcome resistance to disease. Submitted.

  22. P. M. Hoffman, J. M. Powers, M. J. Weise and S. W. Brostoff,Experimental allergic neuritis. I. Rat strain differences in the response to bovine myelin antigens. Brain Res.195, 355–362 (1980).

    Article  PubMed  Google Scholar 

  23. K. Uyemura, M. Suzuki, K. Kitamura, K. Horie, Y. Ogawa, H. Matsuyama, S. Nozaki and I. Muramatsu,Neuritogenic determinant of bovine P2 protein in peripheral nerve myelin. J. Neurochem.39, 895–898 (1982).

    PubMed  Google Scholar 

  24. R. M. Williams and M. J. Moore,Linkage of susceptibility to experimental allergic encephalomyelitis to the major histocompatibility complex in the rat. J. Exp. Med.138, 775–783 (1973).

    Article  PubMed  Google Scholar 

  25. Y. Olsson,Studies on vascular permeability in peripheral nerves. IV. Distribution of intravenously injected protein tracers in the peripheral nervous system of various species. Acta Neuropathol.10, 26–37 (1971).

    Article  Google Scholar 

  26. E. R. Unanue, D. I. Beller, C. Y. Lu and P. M. Allen,Antigen presentation: Comments on its regulation and mechanisms. J. Immunol.132, 1–5 (1984).

    PubMed  Google Scholar 

  27. B. D. Trapp, M. Dubois-Dalcq and R. H. Quarles,Ultrastructural localisation of P2 protein in actively myelinating Schwann cells. J. Neurochem.43, 944–948 (1984).

    PubMed  Google Scholar 

  28. H. Wekerle, C. Linington, H. Lassmann and R. Meyermann,Cellular immune reactivity within the central nervous system. TINS.9, 271–277 (1986).

    Google Scholar 

  29. R. Meyermann, P. W. Lampert, H. Korr and H. Wekerle,T line mediated EAE. A morphological study of the developing lesion. (Abstract). J. Neuropathol. Exp. Neurol.44, 320–321 (1985).

    Google Scholar 

  30. H. Hirschberg, O. J. Bergh and E. Thorsby,Antigen presenting properties of human vascular endothelial cells. J. Exp. Med.152, 249–255 (1980).

    Article  PubMed  Google Scholar 

  31. G. Nunez, E. J. Ball and P. Stastny,Accessory function of human endothelial cells. I. A subpopulation of Ia positive cells is required for antigen presentation. J. Immunol.131, 666–673 (1983).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  34. R. I. Craggs and H. de F. Webster,Ia antigens in the normal rat nervous system and in lesions of experimental allergic encephalomyelitis. Acta Neuropathol.68, 263–272 (1985).

    Article  PubMed  Google Scholar 

  35. H. Lassmann, K. Vass, C. Brunner and H. Wisniewski,Peripheral nervous system lesions in experimental allergic encephalomyelitis. Acta Neuropathol.69, 193–204 (1986).

    Article  PubMed  Google Scholar 

  36. R. A. Sobel, B. W. Blanchette, A. K. Bhan and R. B. Colvin,The immunopathology of experimental allergic encephalomyelitis. II. Endothelial cell Ia increases prior to inflammatory cell infiltration. J. Immunol.132, 2402–2407 (1984).

    PubMed  Google Scholar 

  37. K. A. Brown and D. C. Dumonde, The immunopathological significance of leucocyte-endothelial interactions. InThe blood-brain barrier in health and disease (Eds A. J. Suckling, M. G. Rumsby and M. W. B. Bradbury). Ellis Horwood, Chichester, England 1986.

    Google Scholar 

  38. N. Savion, I. Vlodavsky and Z. Fuks,Interaction of T lymphocytes and macrophages with cultured vascular endothelial cells: Attachment, invasion and subsequent degradation of the subendothelial extracellular matrix. J. Cell. Physiol.118, 169–178 (1984).

    Article  PubMed  Google Scholar 

  39. R. P. Lisak, M. Hirayama, D. Kuchmy, A. Rosenzweig, S. U. Kim, D. E. Pleasure and D. H. Silverberg,Cultured human and rat oligodendrocytes and rat Schwann cells do not have immune response gene-associated antigen (Ia) on their surface. Brain Res.289, 285–292 (1983).

    Article  PubMed  Google Scholar 

  40. J. H. Meador-Woodruff, J. E. Yoshino, J. W. Bigbee, B. L. Lewis and G. Devries,Differential proliferation responses of cultured Schwann cells to axolemme and myelin-enriched fractions. J. Neurocytol.14, 619–628 (1985).

    Article  PubMed  Google Scholar 

  41. J. Winter, R. Mirsky and M. Kablubowski,Immunocytochemical study of the appearance of P2 in developing rat peripheral nerve: comparison with other myelin components. J. Neurocytol.11, 351–362 (1982).

    Article  PubMed  Google Scholar 

  42. J. N. Whitaker,The protein antigens of peripheral nerve myelin. Ann. Neurol. [Suppl]9, 421–444 (1981).

    Article  Google Scholar 

  43. K. Saida, T. Saida, M. J. Brown, D. H. Silverberg and A. K. Asbury,Antiserum mediated demyelination in vivo. A sequential study using intraneural injection of experimental allergic neuritis serum. Lab. Invest.39, 449–462 (1978).

    PubMed  Google Scholar 

  44. A. F. Hahn, J. J. Gilbert and T. E. Feasby,Passive transfer of demyelination by experimental allergic neuritis serum. Acta Neuropathol. (Berlin)49, 189–196 (1980).

    Article  Google Scholar 

  45. T. Yonezawa, Y. Ishihara and H. Matsuyama,Studies on experimental allergic peripheral neuritis. I. Demyelinating patterns studied in vitro. J. Neuropath. Exp. Neurol.27, 453–463 (1968).

    Google Scholar 

  46. H. C. Agrawal, H. B. Clark, D. Agrawal, F. J. Seil and R. H. Quarles,Identification of antibodies in anti-CNS and anti-PNS myelin sera by immunoblot, characterisation by immunohistochemistry and their effect in tissue culture. Brain Res.307, 191–200 (1984).

    Article  PubMed  Google Scholar 

  47. K. Saida, T. Saida, M. J. Brown and D. H. Silverberg,In vivo demyelination induced by intraneural injection of antigalactocerebroside serum. A morphological study. Am. J. Pathol.95, 99–110 (1979).

    PubMed  Google Scholar 

  48. W. M. Carroll, A. R. Jennings and F. L. Mastaglia,Experimental demyelinating optic neuropathy induced by intraneural injection of galactocerebroside antiserum. J. Neurol. Sci.65, 125–135 (1984).

    Article  PubMed  Google Scholar 

  49. T. Saida, K. Saida, S. Dorfman, D. H. Silverberg, A. J. Sumner, M. C. Manning, R. P. Lisak and M. J. Brown,Experimental allergic neuritis induced by sensitization with galactocerebroside. Science204, 1103–1106 (1979).

    PubMed  Google Scholar 

  50. R. A. C. Hughes and H. C. Powell,Experimental allergic neuritis: Demyelination induced by P2 alone and non-specific enhancement by cerebroside. J. Neuropathol. Exp. Neurol.43, 154–161 (1984).

    PubMed  Google Scholar 

  51. C. L. Koski, P. Vanguri and M. L. Shin,Activation of the alternative pathway of complement by human peripheral nerve myelin. J. Immunol.134, 1810–1814 (1985).

    PubMed  Google Scholar 

  52. D. Sun and H. Wekerle,Ia-restricted encephalitogenic T lymphocytes mediating EAE lyse autoantigen-presenting astrocytes. Nature320, 70–72 (1986).

    Article  PubMed  Google Scholar 

  53. D. W. Mason, R. P. Arthur, M. J. Dallman, J. R. Green, G. P. Spickett and M. L. Thomas,Functions of rat T cell subsets isolated by means of monoclonal antibodies. Immunol. Rev.74, 57–82 (1983).

    PubMed  Google Scholar 

  54. B. G. W. Arnason and E. Chelmicka-Szorc,Passive transfer of EAN in Lewis rats by direct injection of sensitised lymphocytes into the sciatic nerve. Acta Neuropath. (Berlin)22, 1–6 (1972).

    Article  Google Scholar 

  55. J. J. Gilbert, T. E. Feasby and A. F. Hahn,Intraneural injection of lymphocytes in experimental allergic neuritis. Acta Neuropathol. (Berlin)61, 61–64 (1983).

    Article  Google Scholar 

  56. B. G. W. Arnason, G. F. Winkler and N. M. Hadler,Cell-mediated demyelination of peripheral nerve in culture. Lab. Invest.21, 1–10 (1969).

    PubMed  Google Scholar 

  57. H. M. Wisniewski and B. R. Bloom,Primary demyelination as a non-specific consequence of a cell mediated immune response. J. Exp. Med.141, 346–359 (1975).

    Article  PubMed  Google Scholar 

  58. R. A. C. Hughes and H. C. Powell,Experimental allergic neuritis: Demyelination induced by P2 alone and non-specific enhancement by cerebroside. J. Neuropathol. Exp. Neurol.43, 154–161 (1984).

    PubMed  Google Scholar 

  59. H. C. Powell, S. L. Brahney, R. R. Myers, M. Rodriguez and P. W. Lampert,Early changes in experimental allergic neuritis. Lab. Invest.48, 332–338 (1983).

    PubMed  Google Scholar 

  60. M. Dal Canto, H. M. Wisniewski, A. B. Johnson, S. W. Brostoff and C. S. Raine,Vesicular disruption of myelin in autoimmune demyelination. J. Neurol. Sci.24, 313–319 (1975).

    Article  PubMed  Google Scholar 

  61. F. A. Tansey and C. F. Brosnan,Protection against experimental allergic neuritis with silica quartz dust. J. Neuroimmunol.3, 169–179 (1983).

    Article  Google Scholar 

  62. R. I. Craggs, R. H. M. King and P. K. Thomas,The effect of suppression of macrophage activity on the development of experimental allergic neuritis. Acta Neuropathol.62, 316–323 (1984).

    Article  PubMed  Google Scholar 

  63. Y. Yarom, Y. Naparstek, V. Lev-Ram, J. Holoshitz, A. Ben-Nun and I. R. Cohen,Immunospecific inhibition of nerve conduction by T lymphocytes reactive to basic protein of myelin. Nature303, 246–247 (1983).

    Article  PubMed  Google Scholar 

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Linington, C., Wekerle, H. & Meyermann, R. T lymphocyte autoimmunity in peripheral nervous system autoimmune disease. Agents and Actions 19, 256–265 (1986). https://doi.org/10.1007/BF01971223

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