Signaling via the kinase p38α programs dendritic cells to drive T H17 differentiation and autoimmune inflammation

Nature Immunology

Volumn 13, Issue 2, 2012, Pages 152-161

  Huang, Gonghua ^a   Wang, Yanyan ^a   Vogel, Peter ^a   Kanneganti, Thirumala Devi ^a   Otsu, Kinya ^b,c   Chi, Hongbo ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD86 ANTIGEN; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 27; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 14;

ARTICLE; AUTOIMMUNE DISEASE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; HELPER CELL; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CYTOKINES; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE DELETION; HUMANS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 14; MYCOSES; RECEPTORS, INTERLEUKIN; RECEPTORS, PATTERN RECOGNITION; T-LYMPHOCYTES; TH17 CELLS;

EID: 84855929741     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2207     Document Type: Article

References (42)

1. Korn, T., Bettelli, E., Oukka, M. & Kuchroo, V. K. IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517 (2009).
2. Iwasaki, A. & Medzhitov, R. Regulation of adaptive immunity by the innate immune system. Science 327, 291-295 (2010).
3. LeibundGut-Landmann, S. et al. Syk-and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8, 630-638 (2007).
4. M ó csai, A., Ruland, J. & Tybulewicz, V. L. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat. Rev. Immunol. 10, 387-402 (2010).
5. Greter, M. et al. Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat. Med. 11, 328-334 (2005). (Pubitemid 40460562)
6. McMahon, E. J., Bailey, S. L., Castenada, C. V., Waldner, H. & Miller, S. D. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat. Med. 11, 335-339 (2005). (Pubitemid 40460563)
7. Bailey, S. L., Schreiner, B., McMahon, E. J. & Miller, S. D. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4 + T H-17 cells in relapsing EAE. Nat. Immunol. 8, 172-180 (2007). (Pubitemid 46152648)
8. Huang, G., Shi, L. Z. & Chi, H. Regulation of JNK and p38 MAPK in the immune system: signal integration, propagation and termination. Cytokine 48, 161-169 (2009).
9. Cohen, P. Targeting protein kinases for the development of anti-infl ammatory drugs. Curr. Opin. Cell Biol. 21, 317-324 (2009).
10. Bain, J. et al. The selectivity of protein kinase inhibitors; a further update. Biochem. J. 408, 297-315 (2007).
11. Berenson, L. S., Yang, J., Sleckman, B. P., Murphy, T. L. & Murphy, K. M. Selective requirement of p38 αMAPK in cytokine-dependent, but not antigen receptordependent, Th1 responses. J. Immunol. 176, 4616-4621 (2006).
12. Jirmanova, L., Giardino Torchia, M. L., Sarma, N. D., Mittelstadt, P. R. & Ashwell, J. D. Lack of the T-cell-specifi c alternative p38 activation pathway reduces autoimmunity and infl ammation. Blood 118, 3280-3289 (2011).
13. Noubade, R. et al. Activation of P38 MAPK in CD4 T cells controls IL-17 production and autoimmune encephalomyelitis. Blood 118, 290-300 (2011).
14. Gulen, M. F. et al. The receptor SIGIRR suppresses Th17 cell proliferation via inhibition of the interleukin-1 receptor pathway and mTOR kinase activation. Immunity 32, 54-66 (2010).
15. Lu, L. et al. Role of SMAD and non-SMAD signals in the development of Th17 and regulatory T cells. J. Immunol. 184, 4295-4306 (2010).
16. Li, L., Kim, J. & Boussiotis, V. A. IL-1 β-mediated signals preferentially drive conversion of regulatory T cells but not conventional T cells into IL-17-producing cells. J. Immunol. 185, 4148-4153 (2010).
17. Commodaro, A. G. et al. p38 αMAP kinase controls IL-17 synthesis in Vogt-Koyanagi-Harada syndrome and experimental autoimmune uveitis. Invest. Ophthalmol. Vis. Sci. 51, 3567-3574 (2010).
18. Kim, C. et al. The kinase p38 αserves cell type-specifi c infl ammatory functions in skin injury and coordinates pro-and anti-infl ammatory gene expression. Nat. Immunol. 9, 1019-1027 (2008).
19. Kang, Y. J. et al. Macrophage deletion of p38 αpartially impairs lipopolysaccharideinduced cellular activation. J. Immunol. 180, 5075-5082 (2008).
20. Stumhofer, J. S. et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic infl ammation of the central nervous system. Nat. Immunol. 7, 937-945 (2006). (Pubitemid 44263907)
21. Batten, M. et al. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7, 929-936 (2006). (Pubitemid 44263906)
22. Ivanov, I. I. et al. Induction of intestinal Th17 cells by segmented fi lamentous bacteria. Cell 139, 485-498 (2009).
23. Bettelli, E. et al. Myelin oligodendrocyte glycoprotein-specifi c T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197, 1073-1081 (2003). (Pubitemid 36570063)
24. Liu, X. et al. Crucial role of interleukin-7 in T helper type 17 survival and expansion in autoimmune disease. Nat. Med. 16, 191-197 (2010).
25. Zhou, L. et al. TGF-β-induced Foxp3 inhibits T H 17 cell differentiation by antagonizing ROR γt function. Nature 453, 236-240 (2008). (Pubitemid 351667978)
26. McGeachy, M. J. et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10, 314-324 (2009).
27. Ghoreschi, K. et al. Generation of pathogenic T H 17 cells in the absence of TGF-β signalling. Nature 467, 967-971 (2010).
28. Murugaiyan, G., Mittal, A. & Weiner, H. L. Identifi cation of an IL-27/osteopontin axis in dendritic cells and its modulation by IFN-γlimits IL-17-mediated autoimmune infl ammation. Proc. Natl. Acad. Sci. USA 107, 11495-11500 (2010).
29. Shinohara, M. L., Kim, J. H., Garcia, V. A. & Cantor, H. Engagement of the type I interferon receptor on dendritic cells inhibits T helper 17 cell development: role of intracellular osteopontin. Immunity 29, 68-78 (2008).
30. Park, H. et al. A distinct lineage of CD4 T cells regulates tissue infl ammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 (2005). (Pubitemid 41541791)
31. Odobasic, D., Leech, M. T., Xue, J. R. & Holdsworth, S. R. Distinct in vivo roles of CD80 and CD86 in the effector T-cell responses inducing antigen-induced arthritis. Immunology 124, 503-513 (2008). (Pubitemid 351962546)
32. Huang, G., Wang, Y., Shi, L. Z., Kanneganti, T. D. & Chi, H. Signaling by the phosphatase MKP-1 in dendritic cells imprints distinct effector and regulatory T cell fates. Immunity 35, 45-58 (2011).
33. van de Veerdonk, F. L. et al. The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5, 329-340 (2009).
34. Perona-Wright, G. et al. A pivotal role for CD40-mediated IL-6 production by dendritic cells during IL-17 induction in vivo. J. Immunol. 182, 2808-2815 (2009).
35. Iezzi, G. et al. CD40-CD40L cross-talk integrates strong antigenic signals and microbial stimuli to induce development of IL-17-producing CD4 + T cells. Proc. Natl. Acad. Sci. USA 106, 876-881 (2009).
36. Yin, F. et al. Noncanonical cAMP pathway and p38 MAPK mediate 2-adrenergic receptor-induced IL-6 production in neonatal mouse cardiac fi broblasts. J. Mol. Cell Cardiol. 40, 384-393 (2006). (Pubitemid 43277840)
37. Shi, L. Z. et al. HIF1 β-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 208, 1367-1376 (2011).
38. Manicassamy, S. et al. Activation of β-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329, 849-853 (2010).
39. Suter, T. et al. The brain as an immune privileged site: dendritic cells of the central nervous system inhibit T cell activation. Eur. J. Immunol. 33, 2998-3006 (2003). (Pubitemid 37428332)
40. Heppner, F. L. et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11, 146-152 (2005). (Pubitemid 40321349)
41. Axtell, R. C., Raman, C. & Steinman, L. Interferon-βexacerbates Th17-mediated infl ammatory disease. Trends Immunol. 32, 272-277 (2011).
42. Sy, J. C. et al. Sustained release of a p38 inhibitor from non-infl ammatory microspheres inhibits cardiac dysfunction. Nat. Mater. 7, 863-868 (2008).