MHC class II-restricted antigen presentation by plasmacytoid dendritic cells inhibits T cell-mediated autoimmunity

Journal of Experimental Medicine

Volumn 207, Issue 9, 2010, Pages 1891-1905

  Irla, Magali ^a   Küpfer, Natalia ^a   Suter, Tobias ^b   Lissilaa, Rami ^c   Benkhoucha, Mahdia ^a   Skupsky, Jonathan ^d   Lalive, Patrice H ^a,e   Fontana, Adriano ^b   Reith, Walter ^a   Hugues, Stéphanie ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c NOVIMMUNE SA   (Switzerland)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; LYMPHOCYTE FUNCTION; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; AUTOIMMUNITY; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HISTOCOMPATIBILITY ANTIGENS CLASS II; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES;

EID: 77956098825     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20092627     Document Type: Article

References (49)

1. Aloisi, F. 2001. Immune function of microglia. Glia. 36:165-179. doi:10.1002/glia.1106
2. Bailey, S.L., B. Schreiner, E.J. McMahon, and S.D. Miller. 2007. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 8:172-180. doi:10.1038/ni1430
3. Bailey-Bucktrout, S.L., S.C. Caulkins, G. Goings, J.A. Fischer, A. Dzionek, and S.D. Miller. 2008. Cutting edge: central nervous system plasmacytoid dendritic cells regulate the severity of relapsing experimental autoimmune encephalomyelitis. J. Immunol. 180:6457-6461.
4. Bajénoff, M., S. Granjeaud, and S. Guerder. 2003. The strategy of T cell antigen-presenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J. Exp. Med. 198:715-724. doi:10.1084/jem.20030167 (Pubitemid 37087771)
5. Barnden, M.J., J. Allison, W.R. Heath, and F.R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76:34-40. doi:10.1046/j.1440-1711.1998.00709.x
6. Bettelli, E., M. Pagany, H.L. Weiner, C. Linington, R.A. Sobel, and V.K. Kuchroo. 2003. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197:1073-1081. doi:10.1084/jem.20021603 (Pubitemid 36570063)
7. Colonna, M., G. Trinchieri, and Y.J. Liu. 2004. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5:1219-1226. doi:10.1038/ni1141
8. Darrasse-Jèze, G., S. Deroubaix, H. Mouquet, G.D. Victora, T. Eisenreich, K.H. Yao, R.F. Masilamani, M.L. Dustin, A. Rudensky, K. Liu, and M.C. Nussenzweig. 2009. Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J. Exp. Med. 206:1853-1862. doi:10.1084/jem.20090746
9. de Heer, H.J., H. Hammad, T. Soullié, D. Hijdra, N. Vos, M.A. Willart, H.C. Hoogsteden, and B.N. Lambrecht. 2004. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200:89-98. doi:10.1084/jem.20040035
10. Di Pucchio, T., B. Chatterjee, A. Smed-Sörensen, S. Clayton, A. Palazzo, M. Montes, Y. Xue, I. Mellman, J. Banchereau, and J.E. Connolly. 2008. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat. Immunol. 9:551-557. doi:10.1038/ni.1602
11. Fillatreau, S., C.H. Sweenie, M.J. McGeachy, D. Gray, and S.M. Anderton. 2002. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 3:944-950. doi:10.1038/ni833 (Pubitemid 35154008)
12. Gerdes, J., H. Lemke, H. Baisch, H.H. Wacker, U. Schwab, and H. Stein. 1984. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133:1710-1715. (Pubitemid 14035254)
13. Goubier, A., B. Dubois, H. Gheit, G. Joubert, F. Villard-Truc, C. Asselin-Paturel, G. Trinchieri, and D. Kaiserlian. 2008. Plasmacytoid dendritic cells mediate oral tolerance. Immunity. 29:464-475. doi:10.1016/j.immuni.2008. 06.017
14. Greter, M., F.L. Heppner, M.P. Lemos, B.M. Odermatt, N. Goebels, T. Laufer, R.J. Noelle, and B. Becher. 2005. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11:328-334. doi:10.1038/nm1197 (Pubitemid 40460562)
15. Hadeiba, H., T. Sato, A. Habtezion, C. Oderup, J. Pan, and E.C. Butcher. 2008. CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat. Immunol. 9:1253-1260.
16. Hjelmström, P., A.E. Juedes, J. Fjell, and N.H. Ruddle. 1998. B-cell-deficient mice develop experimental allergic encephalomyelitis with demyelination after myelin oligodendrocyte glycoprotein sensitization. J. Immunol. 161:4480-4483. (Pubitemid 28492015)
17. Hoeffel, G., A.C. Ripoche, D. Matheoud, M. Nascimbeni, N. Escriou, P. Lebon, F. Heshmati, J.G. Guillet, M. Gannagé, S. Caillat-Zucman, et al. 2007. Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity. 27:481-492. doi:10.1016/j.immuni.2007.07.021
18. Hugues, S., A. Boissonnas, S. Amigorena, and L. Fetler. 2006. The dynamics of dendritic cell-T cell interactions in priming and tolerance. Curr. Opin. Immunol. 18:491-495. doi:10.1016/j.coi.2006.03.021
19. Irla, M., S. Hugues, J. Gill, T. Nitta, Y. Hikosaka, I.R. Williams, F.X. Hubert, H.S. Scott, Y. Takahama, G.A. Holländer, and W. Reith. 2008. Autoantigen-specific interactions with CD4+ thymocytes control mature medullary thymic epithelial cell cellularity. Immunity. 29:451-463. doi:10.1016/j.immuni. 2008.08.007
20. Isaksson, M., B. Ardesjö, L. Rönnblom, O. Kämpe, H. Lassmann, M.L. Eloranta, and A. Lobell. 2009. Plasmacytoid DC promote priming of autoimmune Th17 cells and EAE. Eur. J. Immunol. 39:2925-2935. doi:10.1002/eji.200839179
21. Jongbloed, S.L., R.A. Benson, M.B. Nickdel, P. Garside, I.B. McInnes, and J.M. Brewer. 2009. Plasmacytoid dendritic cells regulate breach of self-tolerance in autoimmune arthritis. J. Immunol. 182:963-968.
22. Katz-Levy, Y., K.L. Neville, A.M. Girvin, C.L. Vanderlugt, J.G. Pope, L.J. Tan, and S.D. Miller. 1999. Endogenous presentation of self myelin epitopes by CNS-resident APCs in Theiler's virus-infected mice. J. Clin. Invest. 104:599-610. doi:10.1172/JCI7292
23. Kitamura, D., J. Roes, R. Kühn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 350:423-426. doi:10.1038/350423a0
24. Klein, L., K. Khazaie, and H. von Boehmer. 2003. In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc. Natl. Acad. Sci. USA. 100:8886-8891. doi:10.1073/pnas.1533365100
25. Köntgen, F., G. Süss, C. Stewart, M. Steinmetz, and H. Bluethmann. 1993. Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int. Immunol. 5:957-964. doi:10.1093/intimm/5.8.957
26. Korn, T., J. Reddy, W. Gao, E. Bettelli, A. Awasthi, T.R. Petersen, B.T. Bäckström, R.A. Sobel, K.W. Wucherpfennig, T.B. Strom, et al. 2007. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 13:423-431. doi:10.1038/nm1564
27. Lampropoulou, V., K. Hoehlig, T. Roch, P. Neves, E. Calderón Gómez, C.H. Sweenie, Y. Hao, A.A. Freitas, U. Steinhoff, S.M. Anderton, and S. Fillatreau. 2008. TLR-activated B cells suppress T cell-mediated autoimmunity. J. Immunol. 180:4763-4773.
28. Lande, R., V. Gafa, B. Serafini, E. Giacomini, A. Visconti, M.E. Remoli, M. Severa, M. Parmentier, G. Ristori, M. Salvetti, et al. 2008. Plasmacytoid dendritic cells in multiple sclerosis: intracerebral recruitment and impaired maturation in response to interferon-beta. J. Neuropathol. Exp. Neurol. 67:388-401.
29. Langrish, C.L., Y. Chen, W.M. Blumenschein, J. Mattson, B. Basham, J.D. Sedgwick, T. McClanahan, R.A. Kastelein, and D.J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201:233-240. doi:10.1084/jem.20041257
30. Lebedeva, T., M.L. Dustin, and Y. Sykulev. 2005. ICAM-1 co-stimulates target cells to facilitate antigen presentation. Curr. Opin. Immunol. 17:251-258. doi:10.1016/j.coi.2005.04.008
31. LeibundGut-Landmann, S., J.M. Waldburger, C. Reis e Sousa, H. Acha-Orbea, W. Reith, and W. Reith. 2004. MHC class II expression is differentially regulated in plasmacytoid and conventional dendritic cells. Nat. Immunol. 5:899-908. doi:10.1038/ni1109
32. Matsushita, T., K. Yanaba, J.D. Bouaziz, M. Fujimoto, and T.F. Tedder. 2008. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118:3420-3430.
33. Murphy, C.A., C.L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R.A. Kastelein, J.D. Sedgwick, and D.J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198:1951-1957. doi:10.1084/jem.20030896
34. O'Connor, R.A., and S.M. Anderton. 2008. Foxp3+ regulatory T cells in the control of experimental CNS autoimmune disease. J. Neuroimmunol. 193:1-11. doi:10.1016/j.jneuroim.2007.11.016
35. Ochando, J.C., C. Homma, Y. Yang, A. Hidalgo, A. Garin, F. Tacke, V. Angeli, Y. Li, P. Boros, Y. Ding, et al. 2006. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7:652-662. doi:10.1038/ni1333
36. Pashenkov, M., Y.M. Huang, V. Kostulas, M. Haglund, M. Söderström, and H. Link. 2001. Two subsets of dendritic cells are present in human cerebrospinal fluid. Brain. 124:480-492. doi:10.1093/brain/124. 3.480
37. Reith, W., S. LeibundGut-Landmann, and J.M. Waldburger. 2005. Regulation of MHC class II gene expression by the class II transactivator. Nat. Rev. Immunol. 5:793-806. doi:10.1038/nri1708
38. Sapoznikov, A., J.A. Fischer, T. Zaft, R. Krauthgamer, A. Dzionek, and S. Jung. 2007. Organ-dependent in vivo priming of naive CD4+, but not CD8+, T cells by plasmacytoid dendritic cells. J. Exp. Med. 204:1923-1933. doi:10.1084/jem.20062373
39. Skupsky, J., A.H. Zhang, Y. Su, and D.W. Scott. 2010. B-cell-delivered gene therapy induces functional T regulatory cells and leads to a loss of antigen-specific effector cells. Mol. Ther. In press.
40. Stasiolek, M., A. Bayas, N. Kruse, A. Wieczarkowiecz, K.V. Toyka, R. Gold, and K. Selmaj. 2006. Impaired maturation and altered regulatory function of plasmacytoid dendritic cells in multiple sclerosis. Brain. 129:1293-1305. doi:10.1093/brain/awl043
41. Steinman, L., R. Martin, C. Bernard, P. Conlon, and J.R. Oksenberg. 2002. Multiple sclerosis: deeper understanding of its pathogenesis reveals new targets for therapy. Annu. Rev. Neurosci. 25:491-505. doi:10.1146/annurev.neuro. 25.112701.142913
42. Steinman, R.M., D. Hawiger, and M.C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711. doi:10.1146/annurev.immunol.21. 120601.141040
43. Suter, T., U. Malipiero, L. Otten, B. Ludewig, A. Muelethaler-Mottet, B. Mach, W. Reith, and A. Fontana. 2000. Dendritic cells and differential usage of the MHC class II transactivator promoters in the central nervous system in experimental autoimmune encephalitis. Eur. J. Immunol. 30:794-802. doi:10.1002/1521-4141(200003)30:3〈794::AID-IMMU794〉3.0.CO;2-Q
44. Urich, E., I. Gutcher, M. Prinz, and B. Becher. 2006. Autoantibody-mediated demyelination depends on complement activation but not activatory Fc-receptors. Proc. Natl. Acad. Sci. USA. 103:18697-18702. doi:10.1073/pnas.0607283103
45. Villadangos, J.A., and L. Young. 2008. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity. 29:352-361. doi:10.1016/j.immuni.2008. 09.002
46. Waldburger, J.M., S. Rossi, G.A. Hollander, H.R. Rodewald, W. Reith, and H. Acha-Orbea. 2003. Promoter IV of the class II transactivator gene is essential for positive selection of CD4+ T cells. Blood. 101:3550-3559. doi:10.1182/blood-2002-06-1855
47. Wekerle, H. 2008. Lessons from multiple sclerosis: models, concepts, observations. Ann. Rheum. Dis. 67:iii56-iii60. doi:10.1136/ard.2008.098020
48. Wekerle, H., D. Sun, R.L. Oropeza-Wekerle, and R. Meyermann. 1987. Immune reactivity in the nervous system: modulation of T-lymphocyte activation by glial cells. J. Exp. Biol. 132:43-57.
49. Young, L.J., N.S. Wilson, P. Schnorrer, A. Proietto, T. ten Broeke, Y. Matsuki, A.M. Mount, G.T. Belz, M. O'Keeffe, M. Ohmura-Hoshino, et al. 2008. Differential MHC class II synthesis and ubiquitination confers distinct antigen-presenting properties on conventional and plasmacytoid dendritic cells. Nat. Immunol. 9:1244-1252. doi:10.1038/ni.1665