C5a receptor-deficient dendritic cells promote induction of Treg and Th17 cells

European Journal of Immunology

Volumn 40, Issue 3, 2010, Pages 710-721

  Weaver Jr , Donald J ^a   Reis, Edimara S ^a,b   Pandey, Manoj K ^a   Köhl, Gabriele ^a,b   Harris, Nathaniel ^a   Gerard, Craig ^c   Köhl, Jörg ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF LÜBECK   (Germany)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

C5a; Complement; DC; IL 17A; T cells

Indexed keywords

COMPLEMENT COMPONENT C5A; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE; OVALBUMIN; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; IMMUNIZATION; IMMUNOREGULATION; INFLAMMATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; TH17 CELL;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERLEUKIN-17; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; RECEPTOR, ANAPHYLATOXIN C5A; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 77749285675     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939333     Document Type: Article

References (39)

1. Köhl, J., The role of complement in danger sensing and transmission. Immunol. Res. 2006. 34: 157-176.
2. Gerard, C. and Gerard, N. P., C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu. Rev. Immunol. 1994. 12: 775-808.
3. Lee, H., Whitfeld, P. L. and Mackay, C. R., Receptors for complement C5a The importance of C5aR and the enigmatic role of C5L2. Immunol. Cell Biol. 2008. 86: 153-160.
4. Cain, S. A. and Monk, P. N., The orphan receptor C5L2 has high affinity binding sites for complement fragments C5a and C5a des-Arg(74). J. Biol. Chem. 2002. 277: 7165-7169.
5. Okinaga, S., Slattery, D., Humbles, A., Zsengeller, Z., Morteau, O., Kinrade, M. B., Brodbeck, R. M. et al., C5L2, a Nonsignaling C5A Binding Protein. Biochemistry 2003. 42: 9406-9415.
6. Gerard,N. P., Lu, B., Liu, P., Craig, S., Fujiwara, Y.,Okinaga, S. andGerard,C., An anti-inflammatory function for the complement anaphylatoxin C5a-binding protein, C5L2. J. Biol. Chem. 2005. 280: 39677-39680.
7. Chen, N. J., Mirtsos, C., Suh, D., Lu, Y. C., Lin, W. J., McKerlie, C., Lee, T. et al., C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 2007. 446: 203-207.
8. Hawlisch, H., Belkaid, Y., Baelder, R., Hildeman, D., Gerard, C. and Köhl, J., C5a negatively regulates Toll-like receptor 4-induced immune responses. Immunity 2005. 22: 415-426.
9. Zhang, X., Kimura, Y., Fang, C., Zhou, L., Sfyroera, G., Lambris, J. D., Wetsel, R. A. et al., Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 2007. 110: 228-236.
10. Karp, C. L., Grupe, A., Schadt, E., Ewart, S. L., Keane-Moore, M., Cuomo, P. J., Köhl, J. et al., Identification of complement factor 5 as a susceptibility locus for experimental allergic asthma. Nat. Immunol. 2000. 1: 221-226.
11. Köhl, J., Baelder, R., Lewkowich, I. P., Pandey, M. K., Hawlisch, H., Wang, L., Best, J. et al., A regulatory role for the C5a anaphylatoxin in type 2 immunity in asthma. J. Clin. Invest. 2006. 116: 783-796.
12. +T cells. Immunity 2008. 28: 425-435.
13. Ouyang, W., Kolls, J. K. and Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008. 28: 454-467.
14. McGeachy, M. J. and Cua, D. J., Th17 cell differentiation: the long and winding road. Immunity 2008. 28: 445-453.
15. Veldhoen,M., Hocking, R. J., Atkins, C. J., Locksley, R. M. and Stockinger, B., TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006. 24: 179-189.
16. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L. and Kuchroo, V. K., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006. 441: 235-238.
17. Yang, L., Anderson, D. E., Baecher-Allan, C., Hastings, W. D., Bettelli, E., Oukka, M.,Kuchroo,V.K.andHafler, D. A., IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008. 454: 350-352.
18. Volpe, E., Servant, N., Zollinger, R., Bogiatzi, S. I., Hupe, P., Barillot, E. and Soumelis, V., A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat. Immunol. 2008. 9: 650-657.
19. Korn, T., Bettelli, E., Gao,W., Awasthi, A., Jager, A., Strom, T. B., Oukka, M. and Kuchroo, V. K., IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007. 448: 484-487.
20. Nurieva, R., Yang, X. O., Martinez, G., Zhang, Y., Panopoulos, A. D., Ma, L., Schluns, K. et al., Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 2007. 448: 480-483.
21. +TCRlo thymocytes in vivo. Science 1990. 250: 1720-1723.
22. + naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 1999. 162: 5317-5326.
23. Letourneau, S., Krieg, C., Pantaleo, G. and Boyman, O., IL-2- and CD25-dependent immunoregulatory mechanisms in the homeostasis of T-cell subsets. J. Allergy Clin. Immunol. 2009. 123: 758-762.
24. Ogura, H., Murakami, M., Okuyama, Y., Tsuruoka, M., Kitabayashi, C., Kanamoto, M., Nishihara, M. et al., Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 2008. 29: 628-636.
25. Lalli, P. N., Strainic, M. G., Lin, F., Medof, M. E. and Heeger, P. S., Decay accelerating factor can control T cell differentiation into IFN-gamma-producing effector cells via regulating local C5a-induced IL-12 production. J. Immunol. 2007. 179: 5793-5802.
26. +cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 2003. 421: 388-392.
27. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M. C. and von, B. H., Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 2005. 6: 1219-1227.
28. +regulatory T cells. Proc. Natl. Acad. Sci. USA 2009. 106: 13445-13450.
29. +CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J. Immunol. 2007. 178: 6725-6729.
30. LeibundGut-Landmann, S., Gross, O., Robinson, M. J., Osorio, F., Slack, E. C., Tsoni, S. V., Schweighoffer, E. et al., Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 2007. 8: 630-638.
31. Fritz, J. H., Le, B. L., Sellge, G., Magalhaes, J. G., Fsihi, H., Kufer, T. A., Collins, C. et al., Nod1-mediated innate immune recognition of peptidoglycan contributes to the onset of adaptive immunity. Immunity 2007. 26: 445-459.
32. Schnare, M., Barton, G. M., Holt, A. C., Takeda, K., Akira, S. and Medzhitov, R., Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2001. 2: 947-950.
33. Fang,C., Zhang, X., Miwa, T. and Song, W. C., Complement promotes the development of inflammatory T-helper 17 cells through synergistic interaction with Toll-like receptor signaling and interleukin-6 production. Blood 2009. 114: 1005-1015.
34. de Haas, C. J., Veldkamp, K. E., Peschel, A., Weerkamp, F., Van Wamel, W. J., Heezius, E. C., Poppelier, M.J. et al., Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J. Exp. Med. 2004. 199: 687-695.
35. Jongerius, I., Köhl, J., Pandey, M. K., Ruyken, M., van Kessel, K. P., van Strijp, J. A. and Rooijakkers, S. H., Staphylococcal complement evasion by various convertase-blocking molecules. J. Exp. Med. 2007. 204: 2461-2471.
36. Wexler, D. E., Chenoweth, D. E. and Cleary, P. P., Mechanism of action of the group A streptococcal C5a inactivator. Proc. Natl. Acad. Sci. USA 1985. 82: 8144-8148.
37. Pangburn, M. K., Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement. Immunopharmacology 2000. 49: 149-157.
38. Köhl, J., Drug evaluation: The C5a receptor antagoist PMX-53. Curr. Opin. Mol. Ther. 2006. 8: 529-538.
39. Otto, M., Hawlisch, H., Monk, P. N., Muller, M., Klos, A., Karp, C. L. and Köhl, J., C5a mutants are potent antagonists of the C5a receptor (CD88) and of C5L2: position 69 is the locus that determines agonism or antagonism. J. Biol. Chem. 2004. 279: 142-151.