Distinct roles of the anaphylatoxins C3a and C5a in dendritic cell-mediated allergic asthma

Journal of Immunology

Volumn 193, Issue 11, 2014, Pages 5387-5401

  Engelke, Carsten ^a   Wiese, Anna V ^a   Schmudde, Inken ^a   Ender, Fanny ^a   Ströver, Heike A ^a   Vollbrandt, Tillmann ^a   König, Peter ^a   Laumonnier, Yves ^a   Köhl, Jörg ^a,b  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA; C5AR1 PROTEIN, MOUSE; COMPLEMENT C3A RECEPTOR; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT RECEPTOR; CYTOKINE; HOUSE DUST ALLERGEN;

AIRWAY RESISTANCE; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HOMING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DERMATOPHAGOIDES; EFFECTOR CELL; EOSINOPHIL; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RNA ISOLATION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; TH2 CELL; ADOPTIVE TRANSFER; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PYROGLYPHIDAE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, DERMATOPHAGOIDES; ASTHMA; CELLS, CULTURED; COMPLEMENT C3A; COMPLEMENT C5A; CYTOKINES; DENDRITIC CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PYROGLYPHIDAE; RECEPTOR, ANAPHYLATOXIN C5A; RECEPTORS, COMPLEMENT; TH17 CELLS; TH2 CELLS;

EID: 84912535544     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400080     Document Type: Article

References (59)

1. Barnes, P. J. 2008. Immunology of asthma and chronic obstructive pulmonary disease. Nat. Rev. Immunol. 8: 183-192.
2. Durrant, D. M., and D. W. Metzger. 2010. Emerging roles of T helper subsets in the pathogenesis of asthma. Immunol. Invest. 39: 526-549.
3. Lambrecht, B. N., and H. Hammad. 2012. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu. Rev. Immunol. 30: 243-270.
4. Hammad, H., M. Chieppa, F. Perros, M. A. Willart, R. N. Germain, and B. N. Lambrecht. 2009. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 15: 410-416.
5. Vermaelen, K. Y., I. Carro-Muino, B. N. Lambrecht, and R. A. Pauwels. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J. Exp. Med. 193: 51-60.
6. Plantinga, M., M. Guilliams, M. Vanheerswynghels, K. Deswarte, F. Branco- Madeira, W. Toussaint, L. Vanhoutte, K. Neyt, N. Killeen, B. Malissen, et al. 2013. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38: 322-335.
7. Keane-Myers, A., W. C. Gause, P. S. Linsley, S. J. Chen, and M. Wills-Karp. 1997. B7-CD28/CTLA-4 costimulatory pathways are required for the development of T helper cell 2-mediated allergic airway responses to inhaled antigens. J. Immunol. 158: 2042-2049.
8. Lombardi, V., A. K. Singh, and O. Akbari. 2010. The role of costimulatory molecules in allergic disease and asthma. Int. Arch. Allergy Immunol. 151: 179-189.
9. Schmudde, I., Y. Laumonnier, and J. Köhl. 2013. Anaphylatoxins coordinate innate and adaptive immune responses in allergic asthma. Semin. Immunol. 25: 2-11.
10. Köhl, J. 2006. The role of complement in danger sensing and transmission. Immunol. Res. 34: 157-176.
11. Ricklin, D., G. Hajishengallis, K. Yang, and J. D. Lambris. 2010. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11: 785-797.
12. Maruo, K., T. Akaike, T. Ono, T. Okamoto, and H. Maeda. 1997. Generation of anaphylatoxins through proteolytic processing of C3 and C5 by house dust mite protease. J. Allergy Clin. Immunol. 100: 253-260.
13. Köhl, J., R. Baelder, I. P. Lewkowich, M. K. Pandey, H. Hawlisch, L. Wang, J. Best, N. S. Herman, A. A. Sproles, J. Zwirner, et al. 2006. A regulatory role for the C5a anaphylatoxin in type 2 immunity in asthma. J. Clin. Invest. 116: 783-796.
14. Klos, A., A. J. Tenner, K. O. Johswich, R. R. Ager, E. S. Reis, and J. Köhl. 2009. The role of the anaphylatoxins in health and disease. Mol. Immunol. 46: 2753-2766.
15. Humbles, A. A., B. Lu, C. A. Nilsson, C. Lilly, E. Israel, Y. Fujiwara, N. P. Gerard, and C. Gerard. 2000. A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature 406: 998-1001.
16. Bautsch, W., H. G. Hoymann, Q. Zhang, I. Meier-Wiedenbach, U. Raschke, R. S. Ames, B. Sohns, N. Flemme, A. Meyer zu Vilsendorf, M. Grove, et al. 2000. Cutting edge: guinea pigs with a natural C3a-receptor defect exhibit decreased bronchoconstriction in allergic airway disease: evidence for an involvement of the C3a anaphylatoxin in the pathogenesis of asthma. J. Immunol. 165: 5401-5405.
17. Drouin, S. M., D. B. Corry, T. J. Hollman, J. Kildsgaard, and R. A. Wetsel. 2002. Absence of the complement anaphylatoxin C3a receptor suppresses Th2 effector functions in a murine model of pulmonary allergy. J. Immunol. 169: 5926-5933.
18. Zhang, X., I. P. Lewkowich, G. Köhl, J. R. Clark, M. Wills-Karp, and J. Köhl. 2009. A protective role for C5a in the development of allergic asthma associated with altered levels of B7-H1 and B7-DC on plasmacytoid dendritic cells. J. Immunol. 182: 5123-5130.
19. Lajoie, S., I. P. Lewkowich, Y. Suzuki, J. R. Clark, A. A. Sproles, K. Dienger, A. L. Budelsky, and M. Wills-Karp. 2010. Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat. Immunol. 11: 928-935.
20. Lim, H., Y. U. Kim, S. M. Drouin, S. Mueller-Ortiz, K. Yun, E. Morschl, R. A. Wetsel, and Y. Chung. 2012. Negative regulation of pulmonary Th17 responses by C3a anaphylatoxin during allergic inflammation in mice. PLoS One 7: e52666.
21. Karp, C. L., A. Grupe, E. Schadt, S. L. Ewart, M. Keane-Moore, P. J. Cuomo, J. Köhl, L. Wahl, D. Kuperman, S. Germer, et al. 2000. Identification of complement factor 5 as a susceptibility locus for experimental allergic asthma. Nat. Immunol. 1: 221-226.
22. Drouin, S. M., M. Sinha, G. Sfyroera, J. D. Lambris, and R. A. Wetsel. 2006. A protective role for the fifth complement component (c5) in allergic airway disease. Am. J. Respir. Crit. Care Med. 173: 852-857.
23. Abe, M., K. Shibata, H. Akatsu, N. Shimizu, N. Sakata, T. Katsuragi, and H. Okada. 2001. Contribution of anaphylatoxin C5a to late airway responses after repeated exposure of antigen to allergic rats. J. Immunol. 167: 4651-4660.
24. Baelder, R., B. Fuchs, W. Bautsch, J. Zwirner, J. Köhl, H. G. Hoymann, T. Glaab, V. Erpenbeck, N. Krug, and A. Braun. 2005. Pharmacological targeting of anaphylatoxin receptors during the effector phase of allergic asthma suppresses airway hyperresponsiveness and airway inflammation. J. Immunol. 174: 783-789.
25. Chen, N. J., C. Mirtsos, D. Suh, Y. C. Lu, W. J. Lin, C. McKerlie, T. Lee, H. Baribault, H. Tian, and W. C. Yeh. 2007. C5L2 is critical for the biological activities of the anaphylatoxins C5a and C3a. Nature 446: 203-207.
26. Zhang, X., I. Schmudde, Y. Laumonnier, M. K. Pandey, J. R. Clark, P. König, N. P. Gerard, C. Gerard, M. Wills-Karp, and J. Köhl. 2010. A critical role for C5L2 in the pathogenesis of experimental allergic asthma. J. Immunol. 185: 6741-6752.
27. Strainic, M. G., J. Liu, D. Huang, F. An, P. N. Lalli, N. Muqim, V. S. Shapiro, G. R. Dubyak, P. S. Heeger, and M. E. Medof. 2008. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 28: 425-435.
28. Weaver, D. J., Jr., E. S. Reis, M. K. Pandey, G. Köhl, N. Harris, C. Gerard, and J. Köhl. 2010. C5a receptor-deficient dendritic cells promote induction of Treg and Th17 cells. Eur. J. Immunol. 40: 710-721.
29. Strainic, M. G., E. M. Shevach, F. An, F. Lin, and M. E. Medof. 2013. Absence of signaling into CD4+ cells via C3aR and C5aR enables autoinductive TGF-b1 signaling and induction of Foxp3+ regulatory T cells. Nat. Immunol. 14: 162-171.
30. Kwan, W. H., W. van der Touw, E. Paz-Artal, M. O. Li, and P. S. Heeger. 2013. Signaling through C5a receptor and C3a receptor diminishes function of murine natural regulatory T cells. J. Exp. Med. 210: 257-268.
31. Lambrecht, B. N., M. De Veerman, A. J. Coyle, J. C. Gutierrez-Ramos, K. Thielemans, and R. A. Pauwels. 2000. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J. Clin. Invest. 106: 551-559.
32. Lambrecht, B. N., R. A. Peleman, G. R. Bullock, and R. A. Pauwels. 2000. Sensitization to inhaled antigen by intratracheal instillation of dendritic cells. Clin. Exp. Allergy 30: 214-224.
33. Sung, S., C. E. Rose, and S. M. Fu. 2001. Intratracheal priming with ovalbuminand ovalbumin 323-339 peptide-pulsed dendritic cells induces airway hyperresponsiveness, lung eosinophilia, goblet cell hyperplasia, and inflammation. J. Immunol. 166: 1261-1271.
34. Barrett, N. A., O. M. Rahman, J. M. Fernandez, M. W. Parsons, W. Xing, K. F. Austen, and Y. Kanaoka. 2011. Dectin-2 mediates Th2 immunity through the generation of cysteinyl leukotrienes. J. Exp. Med. 208: 593-604.
35. Raymond, M., V. Q. Van, K. Wakahara, M. Rubio, and M. Sarfati. 2011. Lung dendritic cells induce T(H)17 cells that produce T(H)2 cytokines, express GATA-3, and promote airway inflammation. J. Allergy Clin. Immunol. 128: 192-201.e6.
36. Höpken, U. E., B. Lu, N. P. Gerard, and C. Gerard. 1996. The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 383: 86-89.
37. Schmudde, I., H. A. Ströver, T. Vollbrandt, P. König, C. M. Karsten, Y. Laumonnier, and J. Köhl. 2013. C5a receptor signalling in dendritic cells controls the development of maladaptive Th2 and Th17 immunity in experimental allergic asthma. Mucosal Immunol. 6: 807-825.
38. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261.
39. Ghoreschi, K., A. Laurence, X. P. Yang, C. M. Tato, M. J. McGeachy, J. E. Konkel, H. L. Ramos, L. Wei, T. S. Davidson, N. Bouladoux, et al. 2010. Generation of pathogenic T(H)17 cells in the absence of TGF-b signalling. Nature 467: 967-971.
40. Chen, L., and D. B. Flies. 2013. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 13: 227-242.
41. Moldaver, D. M., M. S. Bharhani, J. N. Wattie, R. Ellis, H. Neighbour, C. M. Lloyd, M. D. Inman, and M. Larché. 2014. Amelioration of ovalbumininduced allergic airway disease following Der p 1 peptide immunotherapy is not associated with induction of IL-35. Mucosal Immunol. 7: 379-390.
42. Johnson, L. A., and D. G. Jackson. 2010. Inflammation-induced secretion of CCL21 in lymphatic endothelium is a key regulator of integrin-mediated dendritic cell transmigration. Int. Immunol. 22: 839-849.
43. van Rijt, L. S., N. Vos, M. Willart, A. Kleinjan, A. J. Coyle, H. C. Hoogsteden, and B. N. Lambrecht. 2004. Essential role of dendritic cell CD80/CD86 costimulation in the induction, but not reactivation, of TH2 effector responses in a mouse model of asthma. J. Allergy Clin. Immunol. 114: 166-173.
44. Raymond, M., M. Rubio, G. Fortin, K. H. Shalaby, H. Hammad, B. N. Lambrecht, and M. Sarfati. 2009. Selective control of SIRP-alpha-positive airway dendritic cell trafficking through CD47 is critical for the development of T(H)2-mediated allergic inflammation. J. Allergy Clin. Immunol. 124: 1333-1342, e1.
45. Kuipers, H., T. Soullié, H. Hammad, M. Willart, M. Kool, D. Hijdra, H. C. Hoogsteden, and B. N. Lambrecht. 2009. Sensitization by intratracheally injected dendritic cells is independent of antigen presentation by host antigenpresenting cells. J. Leukoc. Biol. 85: 64-70.
46. Nathan, A. T., E. A. Peterson, J. Chakir, and M. Wills-Karp. 2009. Innate immune responses of airway epithelium to house dust mite are mediated through beta-glucan-dependent pathways. J. Allergy Clin. Immunol. 123: 612-618.
47. Trompette, A., S. Divanovic, A. Visintin, C. Blanchard, R. S. Hegde, R. Madan, P. S. Thorne, M. Wills-Karp, T. L. Gioannini, J. P. Weiss, and C. L. Karp. 2009. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 457: 585-588.
48. Lambrecht, B. N., and H. Hammad. 2012. The airway epithelium in asthma. Nat. Med. 18: 684-692.
49. Sun, L., R. F. Guo, H. Gao, J. V. Sarma, F. S. Zetoune, and P. A. Ward. 2009. Attenuation of IgG immune complex-induced acute lung injury by silencing C5aR in lung epithelial cells. FASEB J. 23: 3808-3818.
50. Huber-Lang, M., E. M. Younkin, J. V. Sarma, N. Riedemann, S. R. McGuire, K. T. Lu, R. Kunkel, J. G. Younger, F. S. Zetoune, and P. A. Ward. 2002. Generation of C5a by phagocytic cells. Am. J. Pathol. 161: 1849-1859.
51. Dillard, P., R. A. Wetsel, and S. M. Drouin. 2007. Complement C3a regulates Muc5ac expression by airway Clara cells independently of Th2 responses. Am. J. Respir. Crit. Care Med. 175: 1250-1258.
52. Karsten, C. M., M. K. Pandey, J. Figge, R. Kilchenstein, P. R. Taylor, M. Rosas, J. U. McDonald, S. J. Orr, M. Berger, D. Petzold, et al. 2012. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgRIIB and dectin-1. Nat. Med. 18: 1401-1406.
53. Shushakova, N., J. Skokowa, J. Schulman, U. Baumann, J. Zwirner, R. E. Schmidt, and J. E. Gessner. 2002. C5a anaphylatoxin is a major regulator of activating versus inhibitory FcgammaRs in immune complex-induced lung disease. J. Clin. Invest. 110: 1823-1830.
54. Soroosh, P., T. A. Doherty, W. Duan, A. K. Mehta, H. Choi, Y. F. Adams, Z. Mikulski, N. Khorram, P. Rosenthal, D. H. Broide, and M. Croft. 2013. Lungresident tissue macrophages generate Foxp3+ regulatory T cells and promote airway tolerance. J. Exp. Med. 210: 775-788.
55. 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.
56. Islam, S. A., and A. D. Luster. 2012. T cell homing to epithelial barriers in allergic disease. Nat. Med. 18: 705-715.
57. Ivanov, I. I., and D. R. Littman. 2010. Segmented filamentous bacteria take the stage. Mucosal Immunol. 3: 209-212.
58. Chehoud, C., S. Rafail, A. S. Tyldsley, J. T. Seykora, J. D. Lambris, and E. A. Grice. 2013. Complement modulates the cutaneous microbiome and inflammatory milieu. Proc. Natl. Acad. Sci. USA 110: 15061-15066.
59. Le Friec, G., J. Köhl, and C. Kemper. 2013. A complement a day keeps the Fox(p3) away. Nat. Immunol. 14: 110-112.