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. 2002 Nov 11;29(1):139–147. doi: 10.1016/0165-5728(90)90156-H

Characterization of measles virus-induced cellular autoimmune reactions against myelin basic protein in Lewis rats

Uwe G Liebert 1,∗, George A Hashim 2a,2b, ter Meulen Volker 1
PMCID: PMC7119477  PMID: 1698812

Abstract

Subacute encephalomyelitis (SAME) in Lewis rats following infection with a neurotropic measles virus (MV) is associated with a cell-mediated autoimmune response (CMAI) to myelin badic protein (MBP). MBP-selected CD44+ T cell lines both from measles-infected animals as well as from rats challenged with guinea pig MBP (Gp-MBP) had a similar pattern of response in the presence of synthetic peptides to Gp-MBP and specifically responded in vitro only to the encephalitogenic and not the non-encephalitogenic or other control peptides. In primary splenic lymphocyte cultures from SAME animals, however, a low but significant T-cell response was obtained against the non-encephalitogenic peptide S67 (residues 69–81) of the Gp-MBP. Moreover, immunization of MV-infected rats with this peptide induced clinical and histological experimental allergic encephalomyelitis (EAE) in 38% of the animals. The results of the study show that the non-encephalitogenic peptide S67 can be rendered encephalitogenic in rats when an additional stimulus is given in the form of MV infection. The data indicate further that MV infection of the central nervous system (CNS) enhances the susceptibility of the CNS to autoimmune T cell aggression.

Keywords: Measles virus, Myelin basic protein, T cell line, Epitope, Experimental allergic encephalomyelitis, Autoimmunity

References

  1. Behan P.O., Geschwind N., Lamarche J.B., Lisak R.P., Kies M.W. Delayed hypersensitivity to encephalitogenic protein in disseminated encephalomyelitis. Lancet. 1968;ii:1009–1012. doi: 10.1016/s0140-6736(68)91299-3. [DOI] [PubMed] [Google Scholar]
  2. Eylar E.H., Kniskern P.J., Jackson J.J. Myelin basic protein. Methods Enzymol. 1979;32B:323. [PubMed] [Google Scholar]
  3. Fontana A., Fierz W., Wekerle H. Astrocytes present myelin basic protein to encephalitogenic T-cell lines. Nature. 1984;307:273–276. doi: 10.1038/307273a0. [DOI] [PubMed] [Google Scholar]
  4. Gendelman H.E., Wolinsky J.S., Johnson R.T., Pressman N.J., Pezeshkpour G.H., Boisset G.F. Measles encephalomyelitis: lack of evidence of viral invasion of the central nervous system and quantitative study of the nature of demyelination. Ann. Neurol. 1984;15:353–360. doi: 10.1002/ana.410150409. [DOI] [PubMed] [Google Scholar]
  5. Happ M.P., Heber-Katz E. Differences in the repertoire of the Lewis rat T cell response to self and non-self myelin basic protein. J. Exp. Med. 1988;167:502–513. doi: 10.1084/jem.167.2.502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hashim G.A., Day E.D. Role of antibodies in T cell-mediated experimental allergic encephalomyelitis. J. Neurosci. Res. 1988;21:1–5. doi: 10.1002/jnr.490210102. [DOI] [PubMed] [Google Scholar]
  7. Hashim G.A., Day E.D., Fredane L., Intintola P., Carvalho E. Biological activity of region 65–102 of the myelin basic protein. J. Neurosci. Res. 1986;16:467–478. doi: 10.1002/jnr.490160303. [DOI] [PubMed] [Google Scholar]
  8. Hemachudha T., Griffin D.E., Giffels J.J., Johnson R.T., Moser A.B., Phanuphak P. Myelin basic protein as an encephalitogen in encephalomyelitis and polyneuritis following rabies vaccination. New Engl. J. Med. 1987;316:369–374. doi: 10.1056/NEJM198702123160703. [DOI] [PubMed] [Google Scholar]
  9. Hemachudha T., Phanuphak P., Johnson R.T., Griffin D.E., Ratanavongsiri J., Siriprasomsup W. Neurologic complications of Semple-type rabies vaccine: clinical and immunological studies. Neurology. 1987;37:550–556. doi: 10.1212/wnl.37.4.550. [DOI] [PubMed] [Google Scholar]
  10. Jahnke U., Fischer E.H., Alvord E.C., Jr. Sequence homology between certain viral proteins related to encephalomyelitis and neuritis. Science. 1985;229:282–284. doi: 10.1126/science.2409602. [DOI] [PubMed] [Google Scholar]
  11. Johnson R.T., Griffin D.E., Hirsch R.L., Wolinsky J.S., Roedenbeck S., DeSoriano I.L. Measles encephalomyelitis: clinical and immunological studies. New Engl. J. Med. 1984;310:137–142. doi: 10.1056/NEJM198401193100301. [DOI] [PubMed] [Google Scholar]
  12. Kobune K., Kobune F., Yamanouchi M., Nagashima K., Yoshikawa Y., Hayami M. Neurovirulence of rat brain-adapted measles virus. Jpn. J. Exp. Med. 1983;53:177–180. [PubMed] [Google Scholar]
  13. Lassmann H. Springer Verlag; Berlin - Heidelberg - New York -Tokyo: 1983. Comparative Neuropathology of Chronic Experimenall Allergic Encephalomyelitis and Multiple Sclersis. [PubMed] [Google Scholar]
  14. Liebert U.G., ter Meulen V. Virological aspects of measles virus induced encephalomyelitis in Lewis and BN rats. J. Gen. Virol. 1987;68:1715–1722. doi: 10.1099/0022-1317-68-6-1715. [DOI] [PubMed] [Google Scholar]
  15. Liebert U.G., Linington C., ter Meulen V. Induction of autoimmune reactions to myelin basic protein in measles virus encephalitis in Lewis rats. J. Neuroimmunol. 1988;17:103–118. doi: 10.1016/0165-5728(88)90018-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lisak R.P., Behan P.O., Zweiman B., Shetty T. Cell mediated immunity to myelin basic protein in acute disseminated encephalomyelitis. Neurology. 1974;24:560–564. doi: 10.1212/wnl.24.6.560. [DOI] [PubMed] [Google Scholar]
  17. Mannie M.D., Patterson P.Y., U'Prchard D.C., Flouret G. Vol. 82. 1985. Induction of experimental allergic encephalomyelitis in Lewis rats with purified synthetic peptides: delineation of antigenic determinants for encephalitogenicity, in vitro activation of cellular transfer, and proliferation of lymphocytes; pp. 5515–5519. (Proc. Natl. Acad. Sci. U.S.A.). [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Massa P.T., Schimpl A., Wecker E., ter Meulen V. Vol. 84. 1987. Tumor necrosis factor implifies measles virus-mediated Ia induction of astrocytes; pp. 7242–7245. (Proc. Natl. Acad. Sci. U.S.A.). [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Massanari R.M., Paterson P.Y., Lipton H.L. Potentiation of experimental allergic encephalomyelitis in hamsters with persistent encephalitis due to measles virus. Infect. Dis. 1979;139:297–303. doi: 10.1093/infdis/139.3.297. [DOI] [PubMed] [Google Scholar]
  20. Mokhtarian P., Swoveland P. Predisposition to EAE induction in resistant mice by prior infection with Semliki Forest virus. J. Immunol. 1987;138:3264–3268. [PubMed] [Google Scholar]
  21. Notkins A.L., Onodera T., Prabhakar E.L. In: Concepts in Viral Pathogenesis. Notkins A.L., Oldstone M.B.A., editors. Springer; New York - Berlin - Heidelberg - Tokyo: 1984. pp. 210–215. [Google Scholar]
  22. Offner H., Hashim G., Vandenbark A.A. Response of rat encephalitogenic T lymphocyte lines to synthetic peptides of myelin basic protein. J. Neurosci. Res. 1987;17:344–348. doi: 10.1002/jnr.490170404. [DOI] [PubMed] [Google Scholar]
  23. Offner H., Hashim G., Celnik B., Galang A., Li X., Burns E.R., Shen N., Heber-Katz E., Vandenbark A.A. T cell determinants of myelin basic protein include a unique encephalitogenic I-E restricted epitope for Lewis rats. J. Exp. Med. 1989;170:355–367. doi: 10.1084/jem.170.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Richert J.R., Robinson E.D., Deibler G.E., Martenson R.W., Dragovic L.J., Kies M.W. Evidence for multiple human T cell recognition sites on myelin basic protein. J. Neuroimmunol. 1989;23:55–66. doi: 10.1016/0165-5728(89)90073-8. [DOI] [PubMed] [Google Scholar]
  25. Schluesener H., Wekerle H. Autoaggressive T lymphocyte lines recognize the encephalitogenic region of myelin basic protein: in vitro selection from unprimed rat T lymphocyte populations. J. Immunol. 1985;135:3128–3133. [PubMed] [Google Scholar]
  26. Sedgwick J., Brostoff S., Mason D. Experimental allergic encephalomyelitis in the absence of a classical delayed-type hypersensitivity reaction. Severe paralytic disease correlates with the presence of interleukin 2 receptor-positive cells infiltrating the central nervous system. J. Exp. Med. 1987;165:1058–1075. doi: 10.1084/jem.165.4.1058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sun D., Wekerle H. Ia-restricted encephalitogenic T lymphocytes mediating EAE lyse autoantigen presenting astrocytes. Nature. 1986;320:70–72. doi: 10.1038/320070a0. [DOI] [PubMed] [Google Scholar]
  28. Watanabe R., Wege H., ter Meulen V. Adoptive transfer of EAE-like lesions from rats with coronavirus-induced demyelinating encephalomyelitis. Nature. 1983;305:150–153. doi: 10.1038/305150a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zamvil S.S., Nelson P.A., Mitchell D.J., Knobler R.L., Fritz R.B., Steinman L. Encephalitogenic T cell clones specific for myelin basic protein. An unusual bias in antigen recognition. J. Exp. Med. 1985;162:2107–2124. doi: 10.1084/jem.162.6.2107. [DOI] [PMC free article] [PubMed] [Google Scholar]

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