Complement C3a-induced IL-17 plays a critical role in an IgE-mediated late-phase asthmatic response and airway hyperresponsiveness via neutrophilic inflammation in mice

Journal of Immunology

Volumn 188, Issue 11, 2012, Pages 5694-5705

  Mizutani, Nobuaki ^a   Goshima, Hirofumi ^a   Nabe, Takeshi ^b   Yoshino, Shin ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^b KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3A MONOCLONAL ANTIBODY; COMPLEMENT INHIBITOR; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; MONOCLONAL ANTIBODY; OVALBUMIN; SB 290157; UNCLASSIFIED DRUG;

AIRWAY RESISTANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; INFLAMMATION; INTERLEUKIN 17+ CD4+ T LYMPHOCYTE; MALE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; SINGLE DRUG DOSE; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ASTHMA; BRONCHIAL HYPERREACTIVITY; CD4-POSITIVE T-LYMPHOCYTES; COMPLEMENT C3A; IMMUNOGLOBULIN E; INFLAMMATION MEDIATORS; INTERLEUKIN-17; MALE; MICE; MICE, INBRED BALB C; NEUTROPHILS; RECEPTORS, COMPLEMENT; TIME FACTORS;

EID: 84862081068     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103176     Document Type: Article

References (67)

1. Cohn, L., J. A. Elias, and G. L. Chupp. 2004. Asthma: mechanisms of disease persistence and progression. Annu. Rev. Immunol. 22: 789-815. (Pubitemid 38680442)
2. Robinson, D. S., Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A. M. Bentley, C. Corrigan, S. R. Durham, and A. B. Kay. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326: 298-304.
3. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17: 255-281. (Pubitemid 29241125)
4. Pauwels, R. 1989. The relationship between airway inflammation and bronchial hyperresponsiveness. Clin. Exp. Allergy 19: 395-398. (Pubitemid 19201357)
5. Hogan, S. P., K. I. Matthaei, J. M. Young, A. Koskinen, I. G. Young, and P. S. Foster. 1998. A novel T cell-regulated mechanism modulating allergeninduced airways hyperreactivity in BALB/c mice independently of IL-4 and IL-5. J. Immunol. 161: 1501-1509. (Pubitemid 28380583)
6. 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. (Pubitemid 29004074)
7. De Sanctis, G. T., A. Itoh, F. H. Green, S. Qin, T. Kimura, J. K. Grobholz, T. R. Martin, T. Maki, and J. M. Drazen. 1997. T-lymphocytes regulate genetically determined airway hyperresponsiveness in mice. Nat. Med. 3: 460-462. (Pubitemid 27145691)
8. Meyts, I., J. A. Vanoirbeek, G. Hens, B. M. Vanaudenaerde, B. Verbinnen, D. M. Bullens, L. Overbergh, C. Mathieu, J. L. Ceuppens, and P. W. Hellings. 2008. T-cell mediated late increase in bronchial tone after allergen provocation in a murine asthma model. Clin. Immunol. 128: 248-258.
9. Yoshimoto, T., K. Yasuda, H. Tanaka, M. Nakahira, Y. Imai, Y. Fujimori, and K. Nakanishi. 2009. Basophils contribute to T(H)2-IgE responses in vivo via IL- 4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat. Immunol. 10: 706-712.
10. Coyle, A. J., K. Wagner, C. Bertrand, S. Tsuyuki, J. Bews, and C. Heusser. 1996. Central role of immunoglobulin (Ig) E in the induction of lung eosinophil infiltration and T helper 2 cell cytokine production: inhibition by a non-anaphylactogenic anti-IgE antibody. J. Exp. Med. 183: 1303-1310.
11. Oshiba, A., E. Hamelmann, K. Takeda, K. L. Bradley, J. E. Loader, G. L. Larsen, and E. W. Gelfand. 1996. Passive transfer of immediate hypersensitivity and airway hyperresponsiveness by allergen-specific immunoglobulin (Ig) E and IgG1 in mice. J. Clin. Invest. 97: 1398-1408. (Pubitemid 26097028)
12. Busse,W., J. Corren, B. Q. Lanier, M. McAlary, A. Fowler-Taylor, G. D. Cioppa, A. van As, and N. Gupta. 2001. Omalizumab, anti-IgE recombinant humanized monoclonal antibody, for the treatment of severe allergic asthma. J. Allergy Clin. Immunol. 108: 184-190. (Pubitemid 32735398)
13. Holgate, S., T. Casale, S. Wenzel, J. Bousquet, Y. Deniz, and C. Reisner. 2005. The anti-inflammatory effects of omalizumab confirm the central role of IgE in allergic inflammation. J. Allergy Clin. Immunol. 115: 459-465. (Pubitemid 40341694)
14. Holgate, S. T., A. G. Chuchalin, J. Hébert, J. Lötvall, G. B. Persson, K. F. Chung, J. Bousquet, H. A. Kerstjens, H. Fox, J. Thirlwell, and G. D. Cioppa; Omalizumab 011 International Study Group. 2004. Efficacy and safety of a recombinant anti-immunoglobulin E antibody (omalizumab) in severe allergic asthma. Clin. Exp. Allergy 34: 632-638. (Pubitemid 38534897)
15. Barczyk, A., W. Pierzchala, and E. Sozañska. 2003. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir. Med. 97: 726-733. (Pubitemid 36675678)
16. Hashimoto, T., K. Akiyama, N. Kobayashi, and A. Mori. 2005. Comparison of IL-17 production by helper T cells among atopic and nonatopic asthmatics and control subjects. Int. Arch. Allergy Immunol. 137(Suppl 1): 51-54. (Pubitemid 40868774)
17. Molet, S., Q. Hamid, F. Davoine, E. Nutku, R. Taha, N. Pagé, R. Olivenstein, J. Elias, and J. Chakir. 2001. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108: 430-438. (Pubitemid 32881066)
18. Lindén, A., and M. Adachi. 2002. Neutrophilic airway inflammation and IL-17. Allergy 57: 769-775. (Pubitemid 34969998)
19. Kolls, J. K., S. T. Kanaly, and A. J. Ramsay. 2003. Interleukin-17: an emerging role in lung inflammation. Am. J. Respir. Cell Mol. Biol. 28: 9-11. (Pubitemid 36017045)
20. Hellings, P. W., A. Kasran, Z. Liu, P. Vandekerckhove, A. Wuyts, L. Overbergh, C. Mathieu, and J. L. Ceuppens. 2003. Interleukin-17 orchestrates the granulocyte influx into airways after allergen inhalation in a mouse model of allergic asthma. Am. J. Respir. Cell Mol. Biol. 28: 42-50. (Pubitemid 36017049)
21. Oda, N., P. B. Canelos, D. M. Essayan, B. A. Plunkett, A. C. Myers, and S. K. Huang. 2005. Interleukin-17F induces pulmonary neutrophilia and amplifies antigen-induced allergic response. Am. J. Respir. Crit. Care Med. 171: 12-18. (Pubitemid 40051689)
22. He, R., M. K. Oyoshi, H. Jin, and R. S. Geha. 2007. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc. Natl. Acad. Sci. USA 104: 15817-15822. (Pubitemid 350035382)
23. 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.
24. Mizutani, N., H. Goshima, T. Nabe, and S. Yoshino. 2012. Establishment and characterization of a murine model for allergic asthma using allergen-specific IgE monoclonal antibody to study pathological roles of IgE. Immunol. Lett. 141: 235-245.
25. Yamaki, K., and S. Yoshino. 2009. Comparison of inhibitory activities of zinc oxide ultrafine and fine particulates on IgE-induced mast cell activation. Biometals 22: 1031-1040.
26. Nabe, T., C. L. Zindl, Y. W. Jung, R. Stephens, A. Sakamoto, S. Kohno, T. P. Atkinson, and D. D. Chaplin. 2005. Induction of a late asthmatic response associated with airway inflammation in mice. Eur. J. Pharmacol. 521: 144-155. (Pubitemid 41427802)
27. Mizutani, N., T. Nabe, and S. Yoshino. 2009. Complement C3a regulates late asthmatic response and airway hyperresponsiveness in mice. J. Immunol. 183: 4039-4046.
28. Nabe, T., T. Morishita, K. Matsuya, A. Ikedo, M. Fujii, N. Mizutani, and S. Yoshino. 2011. Complete dependence on CD4+ cells in late asthmatic response, but limited contribution of the cells to airway remodeling in sensitized mice. J. Pharmacol. Sci. 116: 373-383.
29. Nabe, T., F. Hosokawa, K.Matsuya, T. Morishita, A. Ikedo, M. Fujii, N. Mizutani, S. Yoshino, and D. D. Chaplin. 2011. Important role of neutrophils in the late asthmatic response in mice. Life Sci. 88: 1127-1135.
30. Fujiwara, M., K. Hirose, S. Kagami, H. Takatori, H. Wakashin, T. Tamachi, N. Watanabe, Y. Saito, I. Iwamoto, and H. Nakajima. 2007. T-bet inhibits both TH2 cell-mediated eosinophil recruitment and TH17 cell-mediated neutrophil recruitment into the airways. J. Allergy Clin. Immunol. 119: 662-670.
31. Czuprynski, C. J., J. F. Brown, N. Maroushek, R. D. Wagner, and H. Steinberg. 1994. Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J. Immunol. 152: 1836-1846. (Pubitemid 24075716)
32. Pennock, B. E., C. P. Cox, R. M. Rogers, W. A. Cain, and J. H. Wells. 1979. A noninvasive technique for measurement of changes in specific airway resistance. J. Appl. Physiol. 46: 399-406. (Pubitemid 9158788)
33. Yamaki, K., H. Uchida, Y. Harada, R. Yanagisawa, H. Takano, H. Hayashi, Y. Mori, and S. Yoshino. 2003. Effect of the nonsteroidal anti-inflammatory drug indomethacin on Th1 and Th2 immune responses in mice. J. Pharm. Sci. 92: 1723-1729. (Pubitemid 36929691)
34. 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. (Pubitemid 40189432)
35. Weaver, C. T., L. E. Harrington, P. R. Mangan, M. Gavrieli, and K. M. Murphy. 2006. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24: 677-688. (Pubitemid 43867371)
36. McGeachy, M. J., and D. J. Cua. 2008. Th17 cell differentiation: the long and winding road. Immunity 28: 445-453. (Pubitemid 351467042)
37. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL- 12. Immunity 13: 715-725.
38. Lankford, C. S., and D. M. Frucht. 2003. A unique role for IL-23 in promoting cellular immunity. J. Leukoc. Biol. 73: 49-56. (Pubitemid 36125674)
39. Brentano, F., C. Ospelt, J. Stanczyk, R. E. Gay, S. Gay, and D. Kyburz. 2009. Abundant expression of the interleukin (IL)23 subunit p19, but low levels of bioactive IL23 in the rheumatoid synovium: differential expression and Toll-like receptor-(TLR) dependent regulation of the IL23 subunits, p19 and p40, in rheumatoid arthritis. Ann. Rheum. Dis. 68: 143-150.
40. Happel, K. I., M. Zheng, E. Young, L. J. Quinton, E. Lockhart, A. J. Ramsay, J. E. Shellito, J. R. Schurr, G. J. Bagby, S. Nelson, and J. K. Kolls. 2003. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J. Immunol. 170: 4432-4436. (Pubitemid 36519946)
41. 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.
42. Schwartz, L. B., M. S. Kawahara, T. E. Hugli, D. Vik, D. T. Fearon, and K. F. Austen. 1983. Generation of C3a anaphylatoxin from human C3 by human mast cell tryptase. J. Immunol. 130: 1891-1895. (Pubitemid 13091654)
43. Mulligan, M. S., E. Schmid, B. Beck-Schimmer, G. O. Till, H. P. Friedl, R. B. Brauer, T. E. Hugli, M. Miyasaka, R. L. Warner, K. J. Johnson, and P. A. Ward. 1996. Requirement and role of C5a in acute lung inflammatory injury in rats. J. Clin. Invest. 98: 503-512. (Pubitemid 26255752)
44. 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. (Pubitemid 35291699)
45. Zhang, X., Y. Kimura, C. Fang, L. Zhou, G. Sfyroera, J. D. Lambris, R. A. Wetsel, T. Miwa, and W. C. Song. 2007. Regulation of Toll-like receptormediated inflammatory response by complement in vivo. Blood 110: 228-236. (Pubitemid 47026839)
46. Kumar, R. K., and P. S. Foster. 2002. Modeling allergic asthma in mice: pitfalls and opportunities. Am. J. Respir. Cell Mol. Biol. 27: 267-272. (Pubitemid 34979284)
47. Leckie, M. J., A. ten Brinke, J. Khan, Z. Diamant, B. J. O'Connor, C. M. Walls, A. K. Mathur, H. C. Cowley, K. F. Chung, R. Djukanovic, et al. 2000. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyperresponsiveness, and the late asthmatic response. Lancet 356: 2144-2148.
48. Louis, R., and R. Djukanovic. 2006. Is the neutrophil a worthy target in severe asthma and chronic obstructive pulmonary disease? Clin. Exp. Allergy 36: 563-567.
49. Wenzel, S. E., S. J. Szefler, D. Y. Leung, S. I. Sloan, M. D. Rex, and R. J. Martin. 1997. Bronchoscopic evaluation of severe asthma. Persistent inflammation associated with high dose glucocorticoids. Am. J. Respir. Crit. Care Med. 156: 737-743. (Pubitemid 27396409)
50. Jatakanon, A., C. Uasuf, W. Maziak, S. Lim, K. F. Chung, and P. J. Barnes. 1999. Neutrophilic inflammation in severe persistent asthma. Am. J. Respir. Crit. Care Med. 160: 1532-1539.
51. Green, R. H., C. E. Brightling, G. Woltmann, D. Parker, A. J. Wardlaw, and I. D. Pavord. 2002. Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax 57: 875-879. (Pubitemid 35178612)
52. Kurlander, R. J., D. M. Ellison, and J. Hall. 1984. The blockade of Fc receptormediated clearance of immune complexes in vivo by a monoclonal antibody (2.4G2) directed against Fc receptors on murine leukocytes. J. Immunol. 133: 855-862. (Pubitemid 14093480)
53. Chen, L., T. Watanabe, H. Watanabe, and F. Sendo. 2001. Neutrophil depletion exacerbates experimental Chagas' disease in BALB/c, but protects C57BL/6 mice through modulating the Th1/Th2 dichotomy in different directions. Eur. J. Immunol. 31: 265-275.
54. Mednick, A. J., M. Feldmesser, J. Rivera, and A. Casadevall. 2003. Neutropenia alters lung cytokine production in mice and reduces their susceptibility to pulmonary cryptococcosis. Eur. J. Immunol. 33: 1744-1753. (Pubitemid 36790436)
55. McKinley, L., J. F. Alcorn, A. Peterson, R. B. Dupont, S. Kapadia, A. Logar, A. Henry, C. G. Irvin, J. D. Piganelli, A. Ray, and J. K. Kolls. 2008. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181: 4089-4097.
56. Wilson, R. H., G. S. Whitehead, H. Nakano, M. E. Free, J. K. Kolls, and D. N. Cook. 2009. Allergic sensitization through the airway primes Th17- dependent neutrophilia and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 180: 720-730.
57. Wakashin, H., K. Hirose, Y. Maezawa, S. Kagami, A. Suto, N. Watanabe, Y. Saito, M. Hatano, T. Tokuhisa, Y. Iwakura, et al. 2008. IL-23 and Th17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 178: 1023-1032.
58. Komai, M., H. Tanaka, T. Masuda, K. Nagao, M. Ishizaki, M. Sawada, and H. Nagai. 2003. Role of Th2 responses in the development of allergen-induced airway remodelling in a murine model of allergic asthma. Br. J. Pharmacol. 138: 912-920. (Pubitemid 36390648)
59. Aikawa, T., S. Shimura, H. Sasaki, M. Ebina, and T. Takishima. 1992. Marked goblet cell hyperplasia with mucus accumulation in the airways of patients who died of severe acute asthma attack. Chest 101: 916-921.
60. Dunnill, M. S., G. R. Massarella, and J. A. Anderson. 1969. A comparison of the quantitative anatomy of the bronchi in normal subjects, in status asthmaticus, in chronic bronchitis, and in emphysema. Thorax 24: 176-179.
61. Shimura, S., Y. Andoh, M. Haraguchi, and K. Shirato. 1996. Continuity of airway goblet cells and intraluminal mucus in the airways of patients with bronchial asthma. Eur. Respir. J. 9: 1395-1401. (Pubitemid 26233780)
62. Rankin, J. A., D. E. Picarella, G. P. Geba, U. A. Temann, B. Prasad, B. DiCosmo, A. Tarallo, B. Stripp, J. Whitsett, and R. A. Flavell. 1996. Phenotypic and physiologic characterization of transgenic mice expressing interleukin 4 in the lung: lymphocytic and eosinophilic inflammation without airway hyperreactivity. Proc. Natl. Acad. Sci. USA 93: 7821-7825. (Pubitemid 26277122)
63. Zhu, Z., R. J. Homer, Z. Wang, Q. Chen, G. P. Geba, J. Wang, Y. Zhang, and J. A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103: 779-788. (Pubitemid 29152623)
64. DiScipio, R. G., P. J. Daffern, M. A. Jagels, D. H. Broide, and P. Sriramarao. 1999. A comparison of C3a and C5a-mediated stable adhesion of rolling eosinophils in postcapillary venules and transendothelial migration in vitro and in vivo. J. Immunol. 162: 1127-1136. (Pubitemid 29035444)
65. Zwirner, J., T. Werfel, H. C. Wilken, E. Theile, and O. Götze. 1998. Anaphylatoxin C3a but not C3a(desArg) is a chemotaxin for the mouse macrophage cell line J774. Eur. J. Immunol. 28: 1570-1577. (Pubitemid 28221160)
66. Nagata, S., and M. M. Glovsky. 1987. Activation of human serum complement with allergens. I. Generation of C3a, C4a, and C5a and induction of human neutrophil aggregation. J. Allergy Clin. Immunol. 80: 24-32. (Pubitemid 17093318)
67. 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. (Pubitemid 46905750)