Antigens expressed by myelinating glia cells induce peripheral cross-tolerance of endogenous CD8+ T cells

European Journal of Immunology

Volumn 39, Issue 6, 2009, Pages 1505-1515

  Schildknecht, Anita ^a,b,c   Probst, Hans Christian ^a,d   McCoy, Kath D ^a,g   Miescher, Iris ^a   Brenner, Corinne ^a   Leone, Dino P ^e,h   Suter, Ueli ^e   Ohashi, Pamela S ^b,c   van den Broek, Maries ^a,f  

^a INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

^e ETH ZURICH   (Switzerland)

^f UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^g MCMASTER UNIVERSITY   (Canada)

^h STANFORD UNIVERSITY   (United States)

Author keywords

Cross presentation; Cytotoxic T cells; Myelinating glia cells

Indexed keywords

EPITOPE; ANTIGEN; GAMMA INTERFERON; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; BONE MARROW CELL; CD8+ T LYMPHOCYTE; CELL FATE; CONTROLLED STUDY; CROSS REACTION; GLIA CELL; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOID ORGAN; MOUSE; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; SCHWANN CELL; THYMUS; ADOPTIVE TRANSFER; ANIMAL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CROSS PRESENTATION; CYTOLOGY; DENDRITIC CELL; GENETICS; GLIA; HISTOCOMPATIBILITY; IMMUNOLOGY; LYMPH NODE; METABOLISM; MOUSE MUTANT; SPLEEN; TRANSGENIC MOUSE; TRANSPLANTATION; VIRUS INFECTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; ANTIGENS, VIRAL; ARENAVIRIDAE INFECTIONS; BONE MARROW TRANSPLANTATION; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; IMMUNE TOLERANCE; INTERFERON-GAMMA; LYMPH NODES; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEUROGLIA; OLIGODENDROGLIA; SCHWANN CELLS; SPLEEN; THYMUS GLAND; TRANSPLANTATION CHIMERA;

EID: 67649497106     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200839019     Document Type: Article

References (37)

1. Derbinski, J., Schulte, A., Kyewski, B. and Klein, L., Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat. Immunol. 2001. 2: 1032-1039.
2. Anderson, M. S., Venanzi, E. S., Klein, L., Chen, Z., Berzins, S. P., Turley, S. J., von Boehmer, H. et al., Projection of an immunological self shadow within the thymus by the aire protein. Science 2002. 298: 1395-1401.
3. Derbinski, J. and Kyewski, B., Linking signalling pathways, thymic stroma integrity and autoimmunity. Trends Immunol. 2005. 26: 503-506.
4. + T cell tolerance. J. Exp. Med. 2002. 196: 1627-1638.
5. Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V. et al., Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo J. Exp. Med. 2001. 194: 769-779.
6. + T cell tolerance. Immunity 2003. 18: 713-720.
7. Scheinecker, C., McHugh, R., Shevach, E. M. and Germain, R.N., Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J. Exp. Med. 2002. 196: 1079-1090.
8. Bitsch, A., Schuchardt, J., Bunkowski, S., Kuhlmann, T. and Bruck, W., Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain 2000. 123: 1174-1183.
9. Kuhlmann, T., Lingfeld, G., Bitsch, A., Schuchardt, J. and Bruck, W., Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 2002. 125: 2202-2212.
10. + T-cells in lesion formation and axonal dysfunction in multiple sclerosis. Neurol. Res. 2006. 28: 256-261.
11. Goverman, J., Perchellet, A. and Huseby, E. S., The role of CD8(+) T cells in multiple sclerosis and its animal models. Curr. Drug Targets Inflamm. Allergy 2005. 4: 239-245.
12. Muraro, P. A., Vergelli, M., Kalbus, M., Banks, D. E., Nagle, J. W., Tranquill, L. R., Nepom, G. T. et al., Immunodominance of a low-affinity major histocompatibility complex-binding myelin basic protein epitope (residues 111-129) in HLA-DR4 (B1-0401) subjects is associated with a restricted T cell receptor repertoire. J. Clin. Invest. 1997. 100: 339-349.
13. Scholz, C., Patton, K. T., Anderson, D. E., Freeman, G. J. and Hafler, D. A., Expansion of autoreactive T cells in multiple sclerosis is independent of exogenous B7 costimulation. J. Immunol. 1998. 160: 1532-1538.
14. Huseby, E. S., Liggitt, D., Brabb, T., Schnabel, B., Ohlen, C. and Goverman, J., A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J. Exp. Med. 2001. 194: 669-676.
15. Saxena, A., Bauer, J., Scheikl, T., Zappulla, J., Audebert, M., Desbois, S., Waisman, A. et al., Cutting edge: Multiple sclerosis-like lesions induced by effector CD8 T cells recognizing a sequestered antigen on oligodendrocytes. J. Immunol. 2008. 181: 1617-1621.
16. Leone, D. P., Genoud, S., Atanasoski, S., Grausenburger, R., Berger, P., Metzger, D., Macklin, W. B. et al., Tamoxifen-inducible glia-specific Cre mice for somatic mutagenesis in oligodendrocytes and Schwann cells. Mol. Cell. Neurosci. 2003. 22: 430-440.
17. Marty, M. C., Alliot, F., Rutin, J., Fritz, R., Trisler, D. and Pessac, B., The myelin basic protein gene is expressed in differentiated blood cell lineages and in hemopoietic progenitors. Proc. Natl. Acad. Sci. USA 2002. 99: 8856-8861.
18. Soriano, P., Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999. 21: 70-71.
19. Banchereau, J. and Steinman, R. M., Dendritic cells and the control of immunity. Nature 1998. 392: 245-252.
20. Cabbage, S. E., Huseby, E. S., Sather, B. D., Brabb, T., Liggitt, D. and Goverman, J., Regulatory T cells maintain long-term tolerance to myelin basic protein by inducing a novel, dynamic state of T cell tolerance. J. Immunol. 2007. 178: 887-896.
21. Klein, L., Klugmann, M., Nave, K. A., Tuohy, V. K. and Kyewski, B., Shaping of the autoreactive T-cell repertoire by a splice variant of self protein expressed in thymic epithelial cells. Nat. Med. 2000. 6: 56-61.
22. Felten, D. L., Felten, S. Y., Carlson, S. L., Olschowka, J. A. and Livnat, S., Noradrenergic and peptidergic innervation of lymphoid tissue. J. Immunol. 1985. 135: 755s-765s.
23. Prinz, M., Heikenwalder, M., Junt, T., Schwarz, P., Glatzel, M., Heppner, F. L., Fu, Y. X. et al., Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 2003. 425: 957-962.
24. Brossart, P. and Bevan, M. J., Presentation of exogenous protein antigens on major histocompatibility complex class I molecules by dendritic cells: Pathway of presentation and regulation by cytokines. Blood 1997. 90: 1594-1599.
25. Jung, S., Unutmaz, D., Wong, P., Sano, G., De los Santos, K., Sparwasser, T., Wu, S. et al., In vivo depletion of CD11c(1) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 2002. 17: 211-220.
26. Ichikawa, H. T., Williams, L. P. and Segal, B. M., Activation of APC through CD40 or Toll-like receptor 9 overcomes tolerance and precipitates autoimmune disease. J. Immunol. 2002. 169: 2781-2787.
27. Waldner, H., Collins, M. and Kuchroo, V. K., Activation of antigen-presenting cells by microbial products breaks self tolerance and induces autoimmune disease. J. Clin. Invest. 2004. 113: 990-997.
28. Rolink, A., Melchers, F. and Andersson, J., The SCID but not the RAG-2 gene product is required for S mu-S epsilon heavy chain class switching. Immunity 1996. 5: 319-330.
29. Ohashi, P. S., Oehen, S., Buerki, K., Pircher, H., Ohashi, C. T., Odermatt, B., Malissen, B. et al., Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 1991. 65: 305-317.
30. Oldstone, M. B., Nerenberg, M., Southern, P., Price, J. and Lewicki, H., Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: Role of anti-self (virus) immune response. Cell 1991. 65: 319-331.
31. Kurts, C., Kosaka, H., Carbone, F. R., Miller, J. F. and Heath, W. R., Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(1) T cells. J. Exp. Med. 1997. 186: 239-245.
32. Lo, D., Freedman, J., Hesse, S., Palmiter, R. D., Brinster, R. L. and Sherman, L. A., Peripheral tolerance to an islet cell-specific hemagglutinin transgene affects both CD4+ and CD8+ T cells. Eur. J. Immunol. 1992. 22: 1013-1022.
33. Morgan, D. J., Kreuwel, H. T. and Sherman, L. A., Antigen concentration and precursor frequency determine the rate of CD8+ T cell tolerance to peripherally expressed antigens. J. Immunol. 1999. 163: 723-727.
34. Pascolo, S., Bervas, N., Ure, J. M., Smith, A. G., Lemonnier, F. A. and Perarnau, B., HLA-A2.1-restricted education and cytolytic activity of CD8 (+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J. Exp. Med. 1997. 185: 2043-2051.
35. Pircher, H., Ohashi, P., Miescher, G., Lang, R., Zikopoulos, A., Burki, K., Mak, T. W. et al., T cell receptor (TcR) beta chain transgenic mice: Studies on allelic exclusion and on the TcR+ gamma/delta population. Eur. J. Immunol. 1990. 20: 417-424.
36. Altman, J. D., Moss, P. A., Goulder, P. J., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J. and Davis, M. M., Phenotypic analysis of antigen-specific T lymphocytes. Science 1996. 274: 94-96.
37. Gallimore, A., Glithero, A., Godkin, A., Tissot, A. C., Pluckthun, A., Elliott, T., Hengartner, H. and Zinkernagel, R., Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 1998. 187: 1383-1393.