The brain as an immune privileged site: Dendritic cells of the central nervous system inhibit T cell activation

European Journal of Immunology

Volumn 33, Issue 11, 2003, Pages 2998-3006

  Suter, Tobias ^a   Biollaz, Gregoire ^a   Gatto, Dominique ^a   Bernasconi, Luca ^a   Herren, Tobias ^a   Reith, Walter ^b   Fontana, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Autoimmunity; Central nervous system infection; Experimental autoimmune encephalomyelitis; Immune tolerance; Multiple sclerosis

Indexed keywords

B7 ANTIGEN; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL ACTIVITY; CELL INTERACTION; CELL MATURATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENDRITIC CELL; ENCEPHALOMYELITIS; FEMALE; IMMUNE RESPONSE; IMMUNITY; IMMUNOREGULATION; LYMPHOCYTE PROLIFERATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD80; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; BRAIN; DENDRITIC CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; T-LYMPHOCYTES;

EID: 0242643750     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200323611     Document Type: Article

References (38)

1. Mellman, I. and Steinman, R. M., Dendritic cells: specialized and regulated antigen processing machines. Cell 2001. 106: 255-258.
2. Steinman, R. M. and Nussenzweig, M. C., Inaugural Article: Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance. Proc.Natl.Acad.Sci.USA 2002. 99: 351-358.
3. Shortman, K. and Heath, W. R., Immunity or tolerance? That is the question for dendritic cells. Nat. Immunol. 2001. 2: 988-989.
4. Matsumoto, Y., Hara, N., Tanaka, R. and Fujiwara, M., Immunohistochemical analysis of the rat central nervous system during experimental allergic encephalomyelitis, with special reference to Ia-positive cells with dendritic morphology. J. Immunol. 1986. 136: 3668-3676.
5. Waldburger, J. M., Suter, T., Fontana, A., Acha-Orbea, H. and Reith, W., Selective abrogation of major histocompatibility complex class II expression on extrahematopoietic cells in mice lacking promoter IV of the class II transactivator gene. J. Exp. Med. 2001. 194: 393-406.
6. Medawar, P. B., Immunity to homologous grafted skin. III. The fate of skin homo-grafts transplanted to the brain, to subcutaneous tissue, and to the an-terior chamber of the eye. British J. Exp. Pathol. 1948. 29: 58-59.
7. Lassmann, H., Vass, K., Brunner, C. and Seitelberger, M. Characterization of inflammatory infiltrates in experimental allergic encephalomyelitis. In Zimmermann, H. M. (Ed.), Progress in Neuropathology, Raven Press, New York.
8. Matyszak, M. K. and Perry, V. H., The potential role of dendritic cells in immune-mediated inflammatory diseases in the central nervous system. Neuroscience 1996. 74: 599-608.
9. Fischer, H. G., Bonifas, U. and Reichmann, G., Phenotype and functions of brain dendritic cells emerging during chronic infection of mice with Toxoplasma gondii. J. Immunol. 2000. 164: 4826-4834.
10. Hohlfeld, R. and Wekerle, H., Immunological update on multiple sclerosis. Curr.Opin.Neurol. 2001. 14: 299-304.
11. Gold, R., Hartung, H. P. and Toyka, K. V., Animal models for autoimmune demyelinating disorders of the nervous system. Mol. Med. Today 2000. 6: 88-91.
12. Suter, T., Malipiero, U., Otten, L., Ludewig, B., Muelethaler-Mottet, A., Mach, B., Reith, W. and Fontana, A., Dendritic cells and differential usage of the MHC class II transactivator promoters in the central nervous system in experimental autoimmune encephalitis. Eur. J. Immunol. 2000. 30: 794-802.
13. Serafini, B., Columba-Cabezas, S., Di Rosa, F. and Aloisi, F., Intracerebral recruitment and maturation of dendritic cells in the onset and progression of experimental autoimmune encephalomyelitis. Am. J. Pathol. 2000. 157: 1991-2002.
14. Muhlethaler, M. A., Otten, L. A., Steimle, V. and Mach, B., Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO J. 1997. 16: 2851-2860.
15. Landmann, S., Muhlethaler-Mottet, A., Bernasconi, L., Suter,T., Waldburger, J. M., Masternak, K., Arrighi, J. F., Hauser, C., Fontana, A. and Reith,W., Maturation of dendritic cells is accompanied by rapid transcriptional silencing of class ii transactivator (ciita) expression. J. Exp. Med. 2001. 194: 379-392.
16. Shortman, K. and Caux, C., Dendritic cell development: multiple pathways to nature's adjuvants. Stem Cells 1997. 15: 409-419.
17. Henri, S., Vremec, D., Kamath, A., Waithman, J., Williams, S., Benoist, C., Burnham, K., Saeland, S., Handman, E. and Shortman, K., The dendritic cell populations of mouse lymph nodes. J. Immunol. 2001. 167: 741-748.
18. Caminschi, I., Lucas, K. M., O'Keeffe, M. A., Hochrein, H., Laabi, Y., Kontgen, F., Lew, A. M., Shortman, K. and Wright, M.D., Molecular cloning of F4/80-like-receptor, a seven-span membrane protein expressed differentially by dendritic cell and monocyte-macrophage subpopulations. J. Immunol. 2001. 167: 3570-3576.
19. Forster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Muller, I., Wolf, E. and Lipp, M., CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999. 99: 23-33.
20. Akbari, O., DeKruyff, R. H. and Umetsu, D. T., Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2001. 2: 725-731.
21. Jonuleit, H., Schmitt, E., Steinbrink, K. and Enk, A. H., Dendritic cells as a tool to induce anergic and regulatory T cells. Trends Immunol. 2001. 22: 394-400.
22. Fanger, N. A., Maliszewski, C. R., Schooley, K. and Griffith, T. S., Human dendritic cells mediate cellular apoptosis via tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J. Exp. Med. 1999. 190: 1155-1164.
23. Letterio, J. J. and Roberts, A. B., Regulation of immune responses by TGF-beta. Annu.Rev.Immunol. 1998. 16: 137-161.
24. Aiello, S., Noris, M., Piccinini, G., Tomasoni, S., Casiraghi, F., Bonazzola, S., Mister, M., Sayegh, M. H. and Remuzzi, G., Thymic dendritic cells express inducible nitric oxide synthase and generate nitric oxide in response to self- and alloantigens. J. Immunol. 2000. 164: 4649-4658.
25. Fischer, H. G. and Reichmann, G., Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J. Immunol. 2001. 166: 2717-2726.
26. Link, H., Huang, Y. M., Masterman, T. and Xiao, B. G., Vaccination with autologous dendritic cells: from experimental autoimmune encephalomyelitis to multiple sclerosis. J.Neuroimmunol. 2001. 114: 1-7.
27. Bourguin, I., Moser, M., Buzoni-Gatel, D., Tielemans, F., Bout, D., Urbain, J. and Leo, O., Murine dendritic cells pulsed in vitro with Toxoplasma gondii antigens induce protective immunity in vivo. Infect. Immun. 1998. 66: 4867-4874.
28. Knight, S. C., Mertin, J., Stackpoole, A. and Clark, J., Induction of immune responses in vivo with small numbers of veiled (dendritic) cells. Proc. Natl. Acad. Sci.USA 1983. 80: 6032-6035.
29. Karandikar, N. J., Eagar, T. N., Vanderlugt, C. L., Bluestone, J. A. and Miller, S. D., CTLA-4 downregulates epitope spreading and mediates remission in relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2000. 109: 173-180.
30. Hilliard, B., Wilmen, A., Seidel, C., Liu, T. S., Goke, R. and Chen, Y., Roles of TNF-related apoptosis-inducing ligand in experimental autoimmune encephalomyelitis. J. Immunol. 2001. 166: 1314-1319.
31. Sahrbacher, U. C., Lechner, F., Eugster, H. P., Frei, K., Lassmann, H. and Fontana, A., Mice with an inactivation of the inducible nitric oxide synthase gene are susceptible to experimental autoimmune encephalomyelitis. Eur. J. Immunol. 1998. 28: 1332-1338.
32. Maron, R., Hancock, W. W., Slavin, A., Hattori, M., Kuchroo, V. and Weiner, H. L., Genetic susceptibility or resistance to autoimmune encephalomyelitis in MHC congenic mice is associated with differential production of pro- and anti-inflammatory cytokines. Int. Immunol. 1999. 11: 1573-1580.
33. Malipiero, U., Frei, K., Spanaus, K. S., Agresti, C., Lassmann, H., Hahne, M., Tschopp, J., Eugster, H. P. and Fontana, A., Myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis is chronic/relapsing in perforin knockout mice, but monophasic in Fas- and Fas ligand-deficient lpr and gld mice. Eur. J. Immunol. 1997. 27: 3151-3160.
34. Brabb, T., von Dassow, P., Ordonez, N., Schnabel, B., Duke, B. and Goverman, J., In situ tolerance within the central nervous system as a mechanism for preventing autoimmunity. J. Exp. Med. 2000. 192: 871-880.
35. Brabb, T., Goldrath, A. W., von, D. P., Paez, A., Liggitt, H. D. and Goverman,J., Triggers of autoimmune disease in a murine TCR-transgenic model for multiple sclerosis. J. Immunol. 1997. 159: 497-507.
36. Flugel, A., Berkowicz, T., Ritter, T., Labeur, M., Jenne, D. E., Li, Z., Ellwart, J. W., Willem, M., Lassmann, H. and Wekerle, H., Migratory activity and functional changes of green fluorescent effector cells before and during experimental autoimmune encephalomyelitis. Immunity. 2001. 14: 547-560.
37. Plautz, G. E., Touhalisky, J. E. and Shu, S., Treatment of murine gliomas by adoptive transfer of ex vivo activated tumor-draining lymph node cells. Cell. Immunol. 1997. 178: 101-107.
38. Oxenius, A., Bachmann, M. F., Zinkernagel, R. M. and Hengartner, H., Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 1998. 28: 390-400.