STAT6 regulates the development of eosinophilic versus neutrophilic asthma in response to Alternaria alternata

Journal of Immunology

Volumn 197, Issue 12, 2016, Pages 4541-4551

  Valladao, Andrea C ^a,b   Frevert, Charles W ^a   Koch, Lisa K ^b   Campbell, Daniel J ^a,b   Ziegler, Steven F ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; INTERLEUKIN 13; INTERLEUKIN 4; STAT6 PROTEIN; TUMOR NECROSIS FACTOR; ALLERGEN; CELL EXTRACT; FUNGUS ANTIGEN; STAT6 PROTEIN, MOUSE;

ALTERNARIA ALTERNATA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHILIA; FEMALE; INNATE IMMUNITY; MALE; MOUSE; NEUTROPHIL COUNT; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ALTERNARIA; ANIMAL; BAGG ALBINO MOUSE; COMPARATIVE STUDY; DISEASE MODEL; EOSINOPHIL; GENETICS; HISTOCOMPATIBILITY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL;

ALLERGENS; ALTERNARIA; ANIMALS; ANTIGENS, FUNGAL; ASTHMA; CELL EXTRACTS; DISEASE MODELS, ANIMAL; EOSINOPHILS; FEMALE; INTERLEUKIN-13; INTERLEUKIN-4; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NEUTROPHILS; STAT6 TRANSCRIPTION FACTOR; TRANSPLANTATION CHIMERA;

EID: 85002196307     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600007     Document Type: Article

References (57)

1. Salo, P. M., S. J. Arbes, Jr., M. Sever, R. Jaramillo, R. D. Cohn, S. J. London, and D. C. Zeldin. 2006. Exposure to Alternaria alternata in US homes is associated with asthma symptoms. J. Allergy Clin. Immunol. 118: 892-898.
2. Bush, R. K., and J. J. Prochnau. 2004. Alternaria-induced asthma. J. Allergy Clin. Immunol. 113: 227-234.
3. Downs, S. H., T. Z. Mitakakis, G. B. Marks, N. G. Car, E. G. Belousova, J. D. Leüppi, W. Xuan, S. R. Downie, A. Tobias, and J. K. Peat. 2001. Clinical importance of Alternaria exposure in children. Am. J. Respir. Crit. Care Med. 164: 455-459.
4. Bartemes, K. R., K. Iijima, T. Kobayashi, G. M. Kephart, A. N. McKenzie, and H. Kita. 2012. IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J. Immunol. 188: 1503-1513.
5. Doherty, T. A., N. Khorram, K. Sugimoto, D. Sheppard, P. Rosenthal, J. Y. Cho, A. Pham, M. Miller, M. Croft, and D. H. Broide. 2012. Alternaria induces STAT6-dependent acute airway eosinophilia and epithelial FIZZ1 expression that promotes airway fibrosis and epithelial thickness. J. Immunol. 188: 2622-2629.
6. Kobayashi, T., K. Iijima, S. Radhakrishnan, V. Mehta, R. Vassallo, C. B. Lawrence, J. C. Cyong, L. R. Pease, K. Oguchi, and H. Kita. 2009. Asthma-related environmental fungus, Alternaria, activates dendritic cells and produces potent Th2 adjuvant activity. J. Immunol. 182: 2502-2510.
7. Saha, S. K., M. A. Berry, D. Parker, S. Siddiqui, A. Morgan, R. May, P. Monk, P. Bradding, A. J. Wardlaw, I. D. Pavord, and C. E. Brightling. 2008. Increased sputum and bronchial biopsy IL-13 expression in severe asthma. J. Allergy Clin. Immunol. 121: 685-691.
8. Humbert, M., S. R. Durham, S. Ying, P. Kimmitt, J. Barkans, B. Assoufi, R. Pfister, G. Menz, D. S. Robinson, A. B. Kay, and C. J. Corrigan. 1996. IL-4 and IL-5 mRNA and protein in bronchial biopsies from patients with atopic and nonatopic asthma: evidence against "intrinsic" asthma being a distinct immunopathologic entity. Am. J. Respir. Crit. Care Med. 154: 1497-1504.
9. Kuperman, D., B. Schofield, M. Wills-Karp, and M. J. Grusby. 1998. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J. Exp. Med. 187: 939-948.
10. Hoshino, A., T. Tsuji, J. Matsuzaki, T. Jinushi, S. Ashino, T. Teramura, K. Chamoto, Y. Tanaka, Y. Asakura, T. Sakurai, et al. 2004. STAT6-mediated signaling in Th2-dependent allergic asthma: critical role for the development of eosinophilia, airway hyper-responsiveness and mucus hypersecretion, distinct from its role in Th2 differentiation. Int. Immunol. 16: 1497-1505.
11. Chatila, T. A. 2004. Interleukin-4 receptor signaling pathways in asthma pathogenesis. Trends Mol. Med. 10: 493-499.
12. Wills-Karp, M. 2004. Interleukin-13 in asthma pathogenesis. Immunol. Rev. 202: 175-190.
13. Catley, M. C., J. Coote, M. Bari, and K. L. Tomlinson. 2011. Monoclonal antibodies for the treatment of asthma. Pharmacol. Ther. 132: 333-351.
14. Newcomb, D. C., and R. S. Peebles, Jr. 2013. Th17-mediated inflammation in asthma. Curr. Opin. Immunol. 25: 755-760.
15. Zhao, Y., J. Yang, Y. D. Gao, and W. Guo. 2010. Th17 immunity in patients with allergic asthma. Int. Arch. Allergy Immunol. 151: 297-307.
16. Fogli, L. K., M. S. Sundrud, S. Goel, S. Bajwa, K. Jensen, E. Derudder, A. Sun, M. Coffre, C. Uyttenhove, J. van Snick, et al. 2013. T cell-derived IL-17 mediated epithelial changes in the airway and drives pulmonary neutrophilia. J. Immunol. 191: 3100-3111.
17. Liang, S. C., A. J. Long, F. Bennett, M. J. Whitters, R. Karim, M. Collins, S. J. Goldman, K. Dunussi-Joannopoulos, C. M. M. Williams, J. F. Wright, and L. A. Fouser. 2007. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J. Immunol. 179: 7791-7799.
18. 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.
19. Barczyk, A., W. Pierzchala, and E. Sozañska. 2003. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir. Med. 97: 726-733.
20. Vazquez-Tello, A., A. Semlali, J. Chakir, J. G.Martin, D. Y. Leung, D. H. Eidelman, and Q. Hamid. 2010. Induction of glucocorticoid receptor-b expression in epithelial cells of asthmatic airways by T-helper type 17 cytokines. Clin. Exp. Allergy 40: 1312-1322.
21. Fei, M., S. Bhatia, T. B. Oriss, M. Yarlagadda, A. Khare, S. Akira, S. Saijo, Y. Iwakura, B. A. Fallert Junecko, T. A. Reinhart, et al. 2011. TNF-alpha from inflammatory dendritic cells (DCs) regulates lung IL-17A/IL-5 levels and neutrophilia versus eosinophilia during persistent fungal infection. Proc. Natl. Acad. Sci. USA 108: 5360-5365.
22. Howarth, P. H., K. S. Babu, H. S. Arshad, L. Lau, M. Buckley, W. McConnell, P. Beckett, M. Al Ali, A. Chauhan, S. J. Wilson, et al. 2005. Tumour necrosis factor (TNFalpha) as a novel therapeutic target in symptomatic corticosteroid dependent asthma. Thorax 60: 1012-1018.
23. Choy, D. F., K. M. Hart, L. A. Borthwick, A. Shikotra, D. R. Nagarkar, S. Siddiqui, G. Jia, C. M. Ohri, E. Doran, K. M. Vannella, et al. 2015. TH2 and TH17 inflammatory pathways are reciprocally regulated in asthma. Sci. Transl. Med. 7: 301ra129.
24. Haldar, P., and I. D. Pavord. 2007. Noneosinophilic asthma: a distinct clinical and pathologic phenotype. J. Allergy Clin. Immunol. 119: 1043-1052, quiz 1053-1054.
25. Truyen, E., L. Coteur, E. Dilissen, L. Overbergh, L. J. Dupont, J. L. Ceuppens, and D. M. A. Bullens. 2006. Evaluation of airway inflammation by quantitative Th1/Th2 cytokine mRNA measurement in sputum of asthma patients. Thorax 61: 202-208.
26. Wenzel, S. E., S. J. Szefler, D. Y. M. 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.
27. 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.
28. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
29. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141.
30. Schnyder-Candrian, S., D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203: 2715-2725.
31. He, R., H. Y. Kim, J. Yoon, M. K. Oyoshi, A. MacGinnitie, S. Goya, E. J. Freyschmidt, P. Bryce, A. N. J. McKenzie, D. T. Umetsu, et al. 2009. Exaggerated IL-17 response to epicutaneous sensitization mediates airway inflammation in the absence of IL-4 and IL-13. J. Allergy Clin. Immunol. 124: 761-70.e1.
32. Newcomb, D. C., M. G. Boswell, W. Zhou, M. M. Huckabee, K. Goleniewska, C. M. Sevin, G. K. Hershey, J. K. Kolls, and R. S. Peebles, Jr. 2011. Human TH17 cells express a functional IL-13 receptor and IL-13 attenuates IL-17A production. J. Allergy Clin. Immunol. 127: 1006-13.e1-e4.
33. Fahy, J. V. 2009. Eosinophilic and neutrophilic inflammation in asthma: insights from clinical studies. Proc. Am. Thorac. Soc. 6: 256-259.
34. Lloyd, C. M., and E. M. Hessel. 2010. Functions of T cells in asthma: more than just T(H)2 cells. Nat. Rev. Immunol. 10: 838-848.
35. Barnes, P. J. 2007. New molecular targets for the treatment of neutrophilic diseases. J. Allergy Clin. Immunol. 119: 1055-1062, quiz 1063-1064.
36. Fukakusa, M., C. Bergeron, M. K. Tulic, P. O. Fiset, O. Al Dewachi, M. Laviolette, Q. Hamid, and J. Chakir. 2005. Oral corticosteroids decrease eosinophil and CC chemokine expression but increase neutrophil, IL-8, and IFNgamma- inducible protein 10 expression in asthmatic airway mucosa. J. Allergy Clin. Immunol. 115: 280-286.
37. Adcock, I. M., P. A. Ford, P. Bhavsar, T. Ahmad, and K. F. Chung. 2008. Steroid resistance in asthma: mechanisms and treatment options. Curr. Allergy Asthma Rep. 8: 171-178.
38. Zureik, M., C. Neukirch, B. Leynaert, R. Liard, and J. Bousquet. 2002. Sensitization to airborne moulds and severity of asthma: cross sectional study from European community respiratory health survey. BMJ 325: 411-414.
39. Iijima, K., T. Kobayashi, K. Hara, G. M. Kephart, S. F. Ziegler, A. N. McKenzie, and H. Kita. 2014. IL-33 and thymic stromal lymphopoietin mediate immune pathology in response to chronic airborne allergen exposure. J. Immunol. 193: 1549-1559.
40. Akimoto, T., F. Numata, M. Tamura, Y. Takata, N. Higashida, T. Takashi, K. Takeda, and S. Akira. 1998. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187: 1537-1542.
41. Mathew, A., J. A. MacLean, E. DeHaan, A. M. Tager, F. H. Y. Green, and A. D. Luster. 2001. Signal transducer and activator of transcription 6 controls chemokine production and T helper cell type 2 cell trafficking in allergic pulmonary inflammation. J. Exp. Med. 193: 1087-1096.
42. Walford, H. H., and T. A. Doherty. 2013. STAT6 and lung inflammation. JAKSTAT 2: e25301.
43. 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.
44. Yu, M., M. R. Eckart, A. A. Morgan, K. Mukai, A. J. Butte, M. Tsai, and S. J. Galli. 2011. Identification of an IFN-g/mast cell axis in a mouse model of chronic asthma. J. Clin. Invest. 121: 3133-3143.
45. Yang, M., R. K. Kumar, and P. S. Foster. 2009. Pathogenesis of steroid-resistant airway hyperresponsiveness: interaction between IFN-gamma and TLR4/MyD88 pathways. J. Immunol. 182: 5107-5115.
46. Laan, M., O. Prause, M. Miyamoto, M. Sjöstrand, A. M. Hytönen, T. Kaneko, J. Lötvall, and A. Lindén. 2003. A role of GM-CSF in the accumulation of neutrophils in the airways caused by IL-17 and TNF-alpha. Eur. Respir. J. 21: 387-393.
47. Takaoka, A., Y. Tanaka, T. Tsuji, T. Jinushi, A. Hoshino, Y. Asakura, Y. Mita, K. Watanabe, S. Nakaike, Y. Togashi, et al. 2001. A critical role for mouse CXC chemokine(s) in pulmonary neutrophilia during Th type 1-dependent airway inflammation. J. Immunol. 167: 2349-2353.
48. Suzuki, K., H. Nakajima, K. Ikeda, Y. Maezawa, A. Suto, H. Takatori, Y. Saito, and I. Iwamoto. 2003. IL-4-Stat6 signaling induces tristetraprolin expression and inhibits TNF-alpha production in mast cells. J. Exp. Med. 198: 1717-1727.
49. Yamasaki, S., E. Ishikawa, M. Sakuma, H. Hara, K. Ogata, and T. Saito. 2008. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat. Immunol. 9: 1179-1188.
50. Manni, M. L., J. B. Trudeau, E. V. Scheller, S. Mandalapu, M. M. Elloso, J. K. Kolls, S. E. Wenzel, and J. F. Alcorn. 2014. The complex relationship between inflammation and lung function in severe asthma. Mucosal Immunol. 7: 1186-1198.
51. Manni, M. L., S. Mandalapu, K. J. McHugh, M. M. Elloso, P. L. Dudas, and J. F. Alcorn. 2016. Molecular mechanisms of airway hyperresponsiveness in a murine model of steroid-resistant airway inflammation. J. Immunol. 196: 963-977.
52. Ito, K., C. Herbert, J. S. Siegle, C. Vuppusetty, N. Hansbro, P. S. Thomas, P. S. Foster, P. J. Barnes, and R. K. Kumar. 2008. Steroid-resistant neutrophilic inflammation in a mouse model of an acute exacerbation of asthma. Am. J. Respir. Cell Mol. Biol. 39: 543-550.
53. Corren, J., W. Busse, E. O. Meltzer, L. Mansfield, G. Bensch, J. Fahrenholz, S. E. Wenzel, Y. Chon, M. Dunn, H. H. Weng, and S. L. Lin. 2010. A randomized, controlled, phase 2 study of AMG 317, an IL-4Ralpha antagonist, in patients with asthma. Am. J. Respir. Crit. Care Med. 181: 788-796.
54. Kips, J. C., B. J. O'Connor, S. J. Langley, A. Woodcock, H. A. Kerstjens, D. S. Postma, M. Danzig, F. Cuss, and R. A. Pauwels. 2003. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am. J. Respir. Crit. Care Med. 167: 1655-1659.
55. Ortega, H. G., M. C. Liu, I. D. Pavord, G. G. Brusselle, J. M. FitzGerald, A. Chetta, M. Humbert, L. E. Katz, O. N. Keene, S. W. Yancey, and P. Chanez, MENSA Investigators. 2014. Mepolizumab treatment in patients with severe eosinophilic asthma. N. Engl. J. Med. 371: 1198-1207.
56. Wenzel, S., M. Castro, J. Corren, J. Maspero, L. Wang, B. Zhang, G. Pirozzi, E. R. Sutherland, R. R. Evans, V. N. Joish, et al. 2016. Dupilumab efficacy and safety in adults with uncontrolled persistent asthma despite use of medium-to-highdose inhaled corticosteroids plus a long-acting b2 agonist: a randomised doubleblind placebo-controlled pivotal phase 2b dose-ranging trial. Lancet 388: 31-44.
57. Fajt, M. L., and S. E. Wenzel. 2015. Asthma phenotypes and the use of biologic medications in asthma and allergic disease: the next steps toward personalized care. J. Allergy Clin. Immunol. 135: 299-310, quiz 311.