Skip to main content
NCBI home page
Wiley - PMC COVID-19 Collection logoLink to Wiley - PMC COVID-19 Collection
. 2006 Apr 28;100(1):185–201. doi: 10.1111/j.1600-065X.1987.tb00532.x

Immune‐Mediated Encephalitis: On the Role of Antigen‐Presenting Cells in Brain Tissue

Adriano Fontana 1, Karl Frei 1, Stefan Bodmer 1, Erhard Hofer 2
PMCID: PMC7165561  PMID: 3326820

The content is available as a PDF (5.9 MB).

REFERENCES

  1. Anjeszky, A. (1900) Ueber Immunisierung gegen Wut mit normaler Nervensubstanz. Zentralbl. Bakteriol. (Naturwiss.) 27, 5. [Google Scholar]
  2. Ben‐Nun, A. , Eisenstein, S. & Coben J. R. (1982) Experimental autoimmune encephalomyelitis (EAE) in genetically resistant rats: PVG rats resist active induction of EAE but are susceptible to and can generate EAE effector T cell lines. J. Immunol. 129, 918. [PubMed] [Google Scholar]
  3. Ben‐Nun, A. , Wekerle, H. & Cohen, J. R. (1981) The rapid isolation of clonable antigen‐specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur. J. Immunol. 11, 195. [DOI] [PubMed] [Google Scholar]
  4. Berand, E. , Resbef, T. Vandenbark, A. A. , Offner, H. , Friz, R. , Chou, C.‐H.J. , Bernard, D. & Cohen, J. R. (1986) Experimental autoimmune encephalomyelitis mediated by T lymphocyte lines: genotype of antigen‐presenting cells influences immunodominant epitope of basic protein. J. Immunol. 136, 511. [PubMed] [Google Scholar]
  5. Carrel, S. , de Tribolet, N. & Gross, N. (1982) Expression of HLA‐DR and common acute lymphoblastic leukemia antigens on glioma cells. Eur. J. Immunol. 12, 354. [DOI] [PubMed] [Google Scholar]
  6. Cate, R. L. , Mattaliano, R. J. , Hession, C. Tizard, R. , Farber, N. M. , Cheung, A. , Ninfa, E. G. , Frey, A. Z. , Gash, D. J. , Chow, E. P. , Fisher, R. A. , Bertonis, J. M. , Torres, G. , Wallner, B. P. , Ramachandran, K. L. , Ragin, R. C. Manganaro, T. F. , MacLaughlin, D. T. & Donahoe, P. K. (1986) Isolation of the bovine and human genes for Muellerian Inhibiting Substance and expression of the human gene in animal cells. Cell 45, 685. [DOI] [PubMed] [Google Scholar]
  7. Cheifetz, S. , Weatherbee, J. A. , Tsang, M. L. S. , Anderson, J. K. , Mole, J. E. , Lucas, R. & Massagué, J. (1987) The transforming growth factor‐β system, a complex pattern of cross‐reactive ligands and receptors. Cell 48, 409. [DOI] [PubMed] [Google Scholar]
  8. Derynck, R. , Jarrett, J. A. , Chen, E. Y. Eaton, D. H. , Bell, J. R. , Assoian, R. K. , Roberts, A. B. , Sporn, M. B. & Goeddel, D. V. (1985) Human transforming growth factor‐β cDNA sequence and expression in tumor cell lines. Nature 316, 701. [DOI] [PubMed] [Google Scholar]
  9. Erb, P. , Kennedy, M. , Hagmann, I. , Wassmer, P. , Huegli, G. , Fierz, W. & Fontana, A. (1986) Accessory cells and the activation and expression of different T cell functions In: Regulation of immune gene expression., Feldmann M., & McMichael A., eds. The Humana Press, Inc., p. 187. [Google Scholar]
  10. Fierz, W. , Endler, B. , Reske, K. , Wekerle, H. & Fontana, A. (1985) Astrocytes as antigen‐presenting cells. I. Induction of la antigen expression on astrocytes by T cells via immune interferon and its effect on antigen presentation. J. Immunol. 134, 3785. [PubMed] [Google Scholar]
  11. Fierz, W. & Fontana, A. (1986a) An immunological function for astrocytes In: Multiple Sclerosis Research in Europe, Hommes O. R., ed. MTP Press. Lancaster , England . [Google Scholar]
  12. Fierz, W. & Fontana, A. (1986b) The role of astrocytes in the interaction between the immune and nervous system In: Cell. Neurobiol: Astrocytes: Cell Biology and Pathology of Astrocytes., Fedoroff S. & Vernadakis A., eds. Academic Press, Inc. 3, p. 203. [Google Scholar]
  13. Fontana, A. , Bodmer, S. & Frei, K. (1987) Immunoregulatory factors secreted by astrocytes and glioblastoma cells. Lymphokines (in press). [Google Scholar]
  14. Fontana, A. , Erb, P. , Pircher, H. P. , Zinkernagel, R. , Weber, E. & Fierz, W. (1986) Astrocytes as antigen‐presenting cells. II. Unlike H‐2K‐dependent cytotoxic T cells, H‐2I‐restricted T cells are only stimulated in the presence of interfero n‐γ. J. Neuroimmunol. 12, 15. [DOI] [PubMed] [Google Scholar]
  15. Fontana, A. , Fierz, W. & Wekerle, H. (1984c) Astrocytes present myelin basic protein to encephalitogenic T‐cell lines. Nature 307, 273. [DOI] [PubMed] [Google Scholar]
  16. Fontana, A. , Hengartner, H. , de Tribolet, N. & Weber, E. (1984a) Glioblastoma cells release interleukin‐1 and factors inhibiting interleukin‐2 mediated effects. J. Immunol. 132, 1837. [PubMed] [Google Scholar]
  17. Fontana, A. , Kristensen, F. , Dubs, R. , Gemsa, D. & Weber, E. (1982) Production of prostaglandin E and interleukin 1‐like factors by cultured astrocytes and C‐6 glioma cells. J. Immunol. 129, 2419. [PubMed] [Google Scholar]
  18. Fontana, A. , McAdam, K. P. W. J. , Kristensen, F. & Weber, E. (1983) Biological and biochemical characterization of an interleukin 1‐like factor from rat C‐6 glioma cells. Eur. J. Immunol. 13, 689. [DOI] [PubMed] [Google Scholar]
  19. Fontana, A. , Otz, U. , De Week, A. L. & Grob, P. J. (1981) Glia cell stimulating factor (GSF): A new lymphokine. Part 2. Cellular sources and partial purification of human GSF. J Neuroimmunol. 2, 73. [DOI] [PubMed] [Google Scholar]
  20. Fontana, A. , Weber, E. & Dayer, J. M. (1984b) Synthesis of interleukin‐1/endogenous pyrogen in the brain of endotoxin treated mice: A step in fever induction J. Immunol. 133, 1696. [PubMed] [Google Scholar]
  21. Frei, K. , Bodmer, S. , Schwerdel, C. & Fontana, A. (1985) Astrocytes of the brain synthesize interleukin‐3 like factors. J. Immunol. 135, 4044. [PubMed] [Google Scholar]
  22. Frei, K. , Bodmer, S. , Schwerdel, C. & Fontana, A. (1986) Astrocyte‐derived interleukin‐3 as a growth factor for microglia cells and peritoneal macrophages. J. Immunol. 137 3521. [PubMed] [Google Scholar]
  23. Frei, K. , Siepl, C. , Groscurth, P. , Bodmer, S. , Schwerdel, C. & Fontana, A. (1987) Antigen presentation and tumor cytotoxicity by interferon‐γ treated microglial cells. Eur. J. Immunol, (in press). [DOI] [PubMed] [Google Scholar]
  24. Giulian, D. , Baker, T. J. , Shih, L‐C. N. & Lachman, L. B. (1986) Interleukin‐1 of the central nervous system is produced by ameboid microglia. J. Exp. Med. 164, 594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Giulian, D. & Lachman, L. B. (1985) Interleukin‐1 stimulation of astroglial proliferation after brain injury. Science 228, 497. [DOI] [PubMed] [Google Scholar]
  26. Haranaka, K. , Carswell, E. A. , Williamson, B. D. Prendergast, J. S. , Satomi, N. & Old, L. J. (1986) Purification, characterization and antitumor activity of no recombinant mouse tumor necrosis factor. Proc. Nat l. Acad. Sci. USA 83, 3949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hart, D. N. J. & Fabri, J. W. (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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hauser, St. L. , Bhan, A. K. , Gilles, F. H. , Hoban, C. J. , Reinherz, E. L. , Schlossman, St. F. & Weiner, H. L. (1983) Immunohistochemical staining of human brain with monoclonal antibodies that identify lymphocytes, monocytes and the la antigen. J. Neuroimmunol 5, 197. [DOI] [PubMed] [Google Scholar]
  29. Hickey, W. F. , Osborn, J. P. & Kirby, W. M. (1985) Expression of la molecules by astrocytes during acute experimental allergic encephalomyelitis in the Lewis rat. Cell. Immunol. 91, 528. [DOI] [PubMed] [Google Scholar]
  30. Hirsch, M. R. , Wietzerbin, J. , Pierres, M. & Goridis, C. (1983) Expression of la antigens by cultured astrocytes treated with Interferon J. Neurosci. Lett. 41, 199. [DOI] [PubMed] [Google Scholar]
  31. Hofman, F. M. , von Hanwehr, R. R. Dinarello, C. A. , Mizel, S. B. , Hinton, D. & Merrill, J. E. (1986) Immunoregulatory molecules and IL‐2 receptors identified in multiple sclerosis brain. J. Immunol. 136, 3279. [PubMed] [Google Scholar]
  32. Itoyama, Y. Ohnishi, A. , Tateishi, J. , Kuroiwa, Y. & Webster, H. de F. (1985) Spinal cord multiple sclerosis lesions in Japanese patients. Schwann cell remyelination occurs in areas that lack glial fibrillary acidic protein. Acta Neuropathol. (Berl.) 65, 217. [DOI] [PubMed] [Google Scholar]
  33. Kabat, E. A. , Wolf, A. & Bezer, A. E. (1946) The rapid production of acute disseminated encephalomyelitis in rhesus monkeys by injection of heterologous and homologous brain tissue with adjuvant. VII. The effect of cortisone. J. Immunol. 68, 265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kehrl, J. H. , Wakefield, L. M. , Roberts, A. B. Jakowlew, S. , Alvarez‐Mon, M. , Derynck, R. , Sporn, M. B. & Fauci, A. S. (1986) The production of TGF‐β by human T lymphocytes and its potential role in the regulation of T cell growth. J. Exp. Med. 163, 1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kim, S. U. , Moretto, G. & Shin, D. H. (1985) Expression of la antigens on the surface of human oligodendrocytes and astrocytes in culture. J. Neuroimmunol. 10, 141. [DOI] [PubMed] [Google Scholar]
  36. Korngold, R. , Feldman, A. , Borke, L. B. , Lublin, F. D. & Doherty, R. C. (1986) Acute experimental allergic encephalomyelitis in radiation bone marrow chimeras between high and low susceptible strains of mice. Immunogenetics 24, 309. [DOI] [PubMed] [Google Scholar]
  37. Lassmann, H. , Vass, K. , Brunner, Ch. & Seitelberger, F (1986) Characterization of inflammatory infiltrates in experimental allergic encephalomyelitis In: Progress in Neuropathology, Zimmermann H. M., ed. Raven Press; N.Y. , Vol. 6, p. 33. [Google Scholar]
  38. Lindsay, R. M. (1986) Reactive gliosis In: Celt Neurobiol. Astrocytes: Cell Biology and Pathology of Astrocytes, Fedoroff S. & Vernadakis A., eds. Academic Press, Inc., 3, 231. [Google Scholar]
  39. Linthicum, D. S. & Frelinger, J. A. (1982) Acute autoimmune encephalomyelitis in mice. II. Susceptibility is controlled by the combination of H‐2 and histamine sensitization genes. J. Exp. Med. 155, 31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lipton, H. L. & Dal Canto, M. C. (1976) Theiler's virus‐induced demyelination: Prevention by immunosuppression. Science 192, 62. [DOI] [PubMed] [Google Scholar]
  41. de Martin, R. , Haendler, B. , Hofer‐Warbinek, R. , Gaugitsch, H. , Wrann, M. , Schlüsener, H. , Seifert, J. M. , Bodmer, S. , Fontana, A. & Hofer, E. (1987) Complementary DNA for human glioblastoma‐derived T cell suppressor factor, a novel member of the transforming‐β gene family. EMBO J. (in press). [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Mason, A. J. , Hayflick, J. S. , Ling, N. , Esch, R. Ueno, N. , Ying, S.‐Y. , Guillenin, R. , Niall, H. & Seeburg, P. H. (1985) Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor β. Nature 318, 659. [DOI] [PubMed] [Google Scholar]
  43. Massa, P. T. Dörries, R. & ter Meulen, V. (1986) Viral particles induce la antigen expression on astrocytes. Nature 320, 543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Massa, P. T. ter Meulen, V. & Fontana, A. (1987) Hyperinducibility of la antigen on astrocytes correlates with strain‐specific susceptibility to experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 84, 4219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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. [PubMed] [Google Scholar]
  46. McCarron, R. M. , Kempski, O. , Spatz, M. & McFarlin, D. E. (1985) Presentation of myelin basic protein by murine cerebral vascular endothelial cells. J. Immunol. 134, 3100. [PubMed] [Google Scholar]
  47. Merrill, J. E. , Kutsunai, S. , Mohlstrom, C. , Hofman, F. , Groopman, J. & Golde, D. W. (1984) Proliferation of astroglia and oligodendroglia in response to human T cell‐derived factors. Science 224, 1428. [DOI] [PubMed] [Google Scholar]
  48. Miescher, S. , Whiteside, T. L. , Carrel, S. & von Fliedner, U. (1986) Functional properties of tumor‐infiltrating and blood lymphocytes in patients with solid tumors: effects of tumor cells and their supernatants on proliferative responses of lymphocytes. J. Immunol. 136, 1899. [PubMed] [Google Scholar]
  49. Momburg, F. Koch, N. , Moller, R. Moldenhauer, G. , Butcher, G. W. & Hammerling, G. J. (1986) Differential expression of la and la‐associated invariant chain in mouse tissues after in vivo treatment with interferon‐γ. J. Immunol. 136, 940. [PubMed] [Google Scholar]
  50. Montgomery, I. N. & Rauch, H. C. (1982) Experimental allergic encephalomyelitis (EAE) in mice: primary control of EAE susceptibility is outside the H‐2 complex. J. Immunol 128, 421. [PubMed] [Google Scholar]
  51. Morgan, I. M. (1946) Allergic encephalomyelitis in monkeys in response to injection of normal monkey cord J. Bact. 51, 53. [PubMed] [Google Scholar]
  52. Naparstek, Y. , Cohen, I. R. , Fuks, Z. & Vlodavsky, I. (1984) Activated T lymphocytes produce a matrix‐degrading heparan sulfate endoglykosidase. Nature 310, 241. [DOI] [PubMed] [Google Scholar]
  53. Panitch, H. S. , Hirsch, R. L. , Haley, A. S. & Johnson, K. P , (1987) Exacerbation of multiple sclerosis in patients treated with gamma interferon. Lancet 1, 893. [DOI] [PubMed] [Google Scholar]
  54. Paterson, P. Y. (1960) Transfer of allergic encephalomyelitis in rats by means of lymph node cells. J. Exp. Med. 111, 119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Paterson, P. Y. (1973) Multiple sclerosis: An immunologic reassessment. J. Chronic. Dis 26 119. [DOI] [PubMed] [Google Scholar]
  56. Perry, V. H. , Hume, D. A. & Gordon, S. (1985) Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15, 313. [DOI] [PubMed] [Google Scholar]
  57. Pulver, M. , Carrel, S. , Mach, J. R & de Tribolet, N. (1987) Cultured human fetal astrocytes can be induced by interferon‐γ to express HLA‐DR. J. Neuroimmunol. 14, 123. [DOI] [PubMed] [Google Scholar]
  58. Raff, M. C. , Miller, R. H. & Noble, M. (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyle depending on culture medium. Nature 303, 390. [DOI] [PubMed] [Google Scholar]
  59. Raine, C. S. (1983) Multiple sclerosis and chronic relapsing EAE: Comparative ultrastructural neuropathology In: Multiple Sclerosis – Pathology, Diagnosis and Management, Hallpike J., Adams C. W. M. & Tourtelotte W. W., eds. Chapman and Hall, London , p. 413. [Google Scholar]
  60. Rivers, T. M. , Sprunt, D. H. & Berry, G. P. (1933) Observations on attempts to produce acute disseminated encephalomyelitis in monkeys. J. Exp. Med. 58, 39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Rodriguez, M. , Pierce, M. L. & Howie, E. A. (1987) Immune response gene products (Ia antigens) on glial and endothelial cells in virus‐induced demyelination. J. Immunol 138, 3438. [PubMed] [Google Scholar]
  62. Sakai, K. , Tabira, T. Endoh, M. & Steinman, L. (1986) La expression in chronic relapsing experimental allergic encephalomyelitis induced by long‐term cultured T cell lines in mice. Lab. Invest. 54, 345. [PubMed] [Google Scholar]
  63. Saneto, R. P. , Altman, A. , Knobler, R. L. , Johnson, H. M. & de Vellis, J , (1986) Interleukin‐2 mediates the inhibition of oligodendrocyte progenitor cell proliferation in vitro. Proc. Natl. Acad. Sci. USA 83, 9221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schwyzer, M. & Fontana, A. (1985) Partial purification and biochemical characterization of a T cell suppressor factor produced by human glioblastoma cells. J. Immunol. 134, 1003. [PubMed] [Google Scholar]
  65. Seyedin, S. M. , Segarini, P. R. , Rosen, D. M. , Thompson, A. J. , Bentz, H. & Graycar, J. (1987) Cartilage‐inducing factor‐B is a unique protein structurally and functionally related to transforming growth factor‐B. J. Biol. Chem. 262, 1946. [PubMed] [Google Scholar]
  66. Skias, D. D. , Kim, D.‐K. , Reder, A. T. Antel, J. P. , Laucki, D. W. & Fitch, F. W. (1987) Susceptibility of astrocytes to class I MHC antigen‐specific cytotoxicity. J. Immunol. 138, 3254. [PubMed] [Google Scholar]
  67. Sun, D. & Wekerle, H. (1986) La‐restricted encephalitogenic T lymphocytes mediating EAE lyse autoantigen‐presenting astrocytes. Nature 320, 70. [DOI] [PubMed] [Google Scholar]
  68. Suzumura, A. , Lavi, E. , Weiss, S. R. & Silberberg, D. H. (1986b) Coronavirus infection induces H‐2 antigen expression on oligodendrocytes and astrocytes. Science 232, 991. [DOI] [PubMed] [Google Scholar]
  69. Suzumura, A. , Mezitis, S. G. E. , Gonatas, N. K. & Silberberg, D. H. (1987) MHC antigen expression on bulk isolated macrophage‐microglia from newborn mouse brain: induction of la antigen expression by interferon‐γ. J. Neuroimmunol. 15, 263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Suzumura, A. , Silberberg, D. H. & Lisak, R. P. (1986a) The expression of MHC antigens on oligodendrocytes: induction of polymorphic H‐2 expression by lymphokines. J. Neuroimmunol. 11, 179. [DOI] [PubMed] [Google Scholar]
  71. Takehara, K. , Le Roy, E. C. & Grotendorst, G. R. (1987) TGF‐β inhibition of endothelial cell proliferation: alteration of EGF binding and EGF‐induced growth‐regulatory (competence) gene expression. Cell 49, 415. [DOI] [PubMed] [Google Scholar]
  72. Takiguchi, M. & Frelinger, J. A. (1986) Induction of antigen presentation ability in purified cultures of astroglia by interferon‐γ. J. Mol. Cell. Immunol. 2, 269. [PubMed] [Google Scholar]
  73. Ting, J. P. Y. , Shigekawa, B. L. , Linthicum, S. , Weiner, L. P. & Frelinger, J. A. (1981) Expression and synthesis of murine immune response‐associated (Ia) antigens by brain cells. Proc. Natl., Acad. Sci. USA 78, 3170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tourtelotte, W. W. & Ma, I. B. (1978) Multiple sclerosis: The blood‐brain barrier and the measurement of de novo central nervous system IgG synthesis. Neurology 28, 76. [DOI] [PubMed] [Google Scholar]
  75. Traugott, U. , Scheinberg, L. C. & Raine, C. S. (1985) On the presence of la‐positive endothelial cells and astrocytes in multiple sclerosis lesions and its relevance to antigen presentation. J. Neuroimmunol. 28 76. [DOI] [PubMed] [Google Scholar]
  76. Traugott, U. , Shevach, E. , Chiba, J. , Stone, S. H. & Raine, C. S. (1981) Autoimmune encephalomyelitis: simultaneous localization of T and B ceils in the target organ. Science 214, 1251. [DOI] [PubMed] [Google Scholar]
  77. Traugott, U. , Shevach, E. , Chiba, J. , Stone, S. H. & Raine, C. S. (1982) Acute experimental autoimmune encephalomyelitis: T‐ and B‐cell distribution within the target organ. Cell. Immunol. 70, 345. [DOI] [PubMed] [Google Scholar]
  78. Vass, K. , Lassmann, H. , Wekerle, H. & Wisniewski, H. M. (1986) The distribution of la antigen in the lesions of rat acute experimental allergic encephalomyelitis. Acta Neuropathol. (Berl.) 70, 149. [DOI] [PubMed] [Google Scholar]
  79. Williams, K. A. , Hart, D. N. J. , Fabri, J. W. & Morris, P. J. (1980) Distribution and quantitation of HLA‐ABC and DR (la) antigens on human kidney and other tissues. Transplantation 29, 274. [DOI] [PubMed] [Google Scholar]
  80. Wong, G. M. W. , Bartlett, P. F. , Clark‐Lewis, I. , Battye, F & Schrader, J. W. (1984) Inducible expression of H‐2 and la antigens on brain cells. Nature 310, 688. [DOI] [PubMed] [Google Scholar]
  81. Wrann, M. , Bodmer, S. , de Martin, R. , Siepl, C. Hofer‐Warbinek, R. , Frei, K. , Hofer, E. & Fontana, A. (1987) T cell suppressor factor from human glioblastoma cells is a 12.5 kd protein closely related to transforming growth factor‐β. EMBO Journal 6, 1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Zamvil, S. , Nelson, P. , Trotter, J. , Mitchell, D. , Knobler, R. , Fritz, R. & Steinman, L. (1985) T‐cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination. Nature 317, 355. [DOI] [PubMed] [Google Scholar]

Articles from Immunological Reviews are provided here courtesy of Wiley

RESOURCES