T cells are necessary for ILC2 activation in house dust mite-induced allergic airway inflammation in mice

European Journal of Immunology

Volumn 46, Issue 6, 2016, Pages 1392-1403

  Li, Bobby W S ^a   de Bruijn, Marjolein J W ^a   Tindemans, Irma ^a   Lukkes, Melanie ^a   KleinJan, Alex ^a   Hoogsteden, Henk C ^a   Hendriks, Rudi W ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Allergy; Asthma; Group 2 innate lymphoid cells (ILC2s); House dust mite; Th2 cells

Indexed keywords

CYTOKINE;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CELL ACTIVATION; CELL INFILTRATION; DERMATOPHAGOIDES; GROUP 2 INNATE LYMPHOID CELL; IN VITRO STUDY; LYMPHOID CELL; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; SENSITIZATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 84973631241     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201546119     Document Type: Article

References (49)

1. Anderson, G. P., Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 2008. 372: 1107–1119.
2. Fahy, J. V., Type 2 inflammation in asthma—present in most, absent in many. Nat. Rev. Immunol. 2015. 15: 57–65.
3. Lambrecht, B. N. and Hammad, H., The immunology of asthma. Nat. Immunol. 2015. 16: 45–56.
4. Fort, M. M., Cheung, J., Yen, D., Li, J., Zurawski, S. M., Lo, S., Menon, S. et al., IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 2001. 15: 985–995.
5. Moro, K., Yamada, T., Tanabe, M., Takeuchi, T., Ikawa, T., Kawamoto, H., Furusawa, J. et al., Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010. 463: 540–544.
6. Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., Bucks, C. et al., Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010. 464: 1367–1370.
7. Price, A. E., Liang, H. E., Sullivan, B. M., Reinhardt, R. L., Eisley, C. J., Erle, D. J. and Locksley, R. M., Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA 2010. 107: 11489–11494.
8. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S. et al., Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013. 13: 145–149.
9. Hoyler, T., Klose, C. S., Souabni, A., Turqueti-Neves, A., Pfeifer, D., Rawlins, E. L., Voehringer, D. et al., The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012. 37: 634–648.
10. Mjosberg, J., Bernink, J., Golebski, K., Karrich, J. J., Peters, C. P., Blom, B., te Velde, A. A. et al., The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012. 37: 649–659.
11. Klein Wolterink, R. G., Serafini, N., van Nimwegen, M., Vosshenrich, C. A., de Bruijn, M. J., Fonseca Pereira, D., Veiga Fernandes, H. et al., Dose-dependent role for the transcription factor Gata3 in the development of IL-5+ and IL-13+ type 2 innate lymphoid cells. Proc. Natl. Acad. Sci. USA 2013. 110: 10240–10245.
12. Halim, T. Y., Krauss, R. H., Sun, A. C. and Takei, F., Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 2012. 36: 451–463.
13. Halim, T. Y., Steer, C. A., Matha, L., Gold, M. J., Martinez-Gonzalez, I., McNagny, K. M., McKenzie, A. N. et al., Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 2014. 40: 425–435.
14. Doherty, T. A., Khorram, N., Sugimoto, K., Sheppard, D., Rosenthal, P., Cho, J. Y., Pham, A. et al., Alternaria induces STAT6-dependent acute airway eosinophilia and epithelial FIZZ1 expression that promotes airway fibrosis and epithelial thickness. J. Immunol. 2012. 188: 2622–2629.
15. Doherty, T. A., Khorram, N., Chang, J. E., Kim, H. K., Rosenthal, P., Croft, M. and Broide, D. H., STAT6 regulates natural helper cell proliferation during lung inflammation initiated by Alternaria. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012. 303: L577–L588.
16. Mirchandani, A. S., Besnard, A. G., Yip, E., Scott, C., Bain, C. C., Cerovic, V., Salmond, R. J. et al., Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J. Immunol. 2014. 192: 2442–2448.
17. Drake, L. Y., Iijima, K. and Kita, H., Group 2 innate lymphoid cells and CD4+ T cells cooperate to mediate type 2 immune response in mice. Allergy 2014. 69: 1300–1307.
18. Gold, M. J., Antignano, F., Halim, T. Y., Hirota, J. A., Blanchet, M. R., Zaph, C., Takei, F. et al., Group 2 innate lymphoid cells facilitate sensitization to local, but not systemic, TH2-inducing allergen exposures. J. Allergy Clin. Immunol. 2014. 133: 1142–1148.
19. Oliphant, C. J., Hwang, Y. Y., Walker, J. A., Salimi, M., Wong, S. H., Brewer, J. M., Englezakis, A. et al., MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 2014. 41: 283–295.
20. Corry, D. B., Grunig, G., Hadeiba, H., Kurup, V. P., Warnock, M. L., Sheppard, D., Rennick, D. M. et al., Requirements for allergen-induced airway hyperreactivity in T and B cell-deficient mice. Mol. Med. 1998. 4: 344–355.
21. Doherty, T. A., Soroosh, P., Broide, D. H. and Croft, M., CD4+ cells are required for chronic eosinophilic lung inflammation but not airway remodeling. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009. 296: L229–L235.
22. Coquet, J. M., Schuijs, M. J., Smyth, M. J., Deswarte, K., Beyaert, R., Braun, H., Boon, L. et al., Interleukin-21-producing CD4(+) T cells promote type 2 immunity to house dust mites. Immunity 2015. 43: 318–330.
23. Gogishvili, T., Luhder, F., Kirstein, F., Nieuwenhuizen, N. E., Goebbels, S., Beer-Hammer, S., Pfeffer, K. et al., Interruption of CD28-mediated costimulation during allergen challenge protects mice from allergic airway disease. J. Allergy Clin. Immunol. 2012. 130: 1394–1403; e1394.
24. Klein Wolterink, R. G., Kleinjan, A., van Nimwegen, M., Bergen, I., de Bruijn, M., Levani, Y. and Hendriks, R. W., Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur. J. Immunol. 2012. 42: 1106–1116.
25. Ribeiro de Almeida, C., Heath, H., Krpic, S., Dingjan, G. M., van Hamburg, J. P., Bergen, I., van de Nobelen, S. et al., Critical role for the transcription regulator CCCTC-binding factor in the control of Th2 cytokine expression. J. Immunol. 2009. 182: 999–1010.
26. Hobeika, E., Thiemann, S., Storch, B., Jumaa, H., Nielsen, P. J., Pelanda, R. and Reth, M., Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 2006. 103: 13789–13794.
27. Kondo, Y., Yoshimoto, T., Yasuda, K., Futatsugi-Yumikura, S., Morimoto, M., Hayashi, N., Hoshino, T. et al., Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int. Immunol. 2008. 20: 791–800.
28. Bartemes, K. R., Iijima, K., Kobayashi, T., Kephart, G. M., McKenzie, A. N. and Kita, H., IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J. Immunol. 2012. 188: 1503–1513.
29. Kim, H. Y., Chang, Y. J., Subramanian, S., Lee, H. H., Albacker, L. A., Matangkasombut, P., Savage, P. B. et al., Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity. J. Allergy Clin. Immunol. 2012. 129: 216–227; e211–e216.
30. Oboki, K., Ohno, T., Kajiwara, N., Arae, K., Morita, H., Ishii, A., Nambu, A. et al., IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc. Natl. Acad. Sci. USA 2010. 107: 18581–18586.
31. Barnden, M. J., Allison, J., Heath, W. R. and Carbone, F. R., Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 1998. 76: 34–40.
32. Kool, M., Willart, M. A., van Nimwegen, M., Bergen, I., Pouliot, P., Virchow, J. C., Rogers, N. et al., An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 2011. 34: 527–540.
33. Lambrecht, B. N., Salomon, B., Klatzmann, D. and Pauwels, R. A., Dendritic cells are required for the development of chronic eosinophilic airway inflammation in response to inhaled antigen in sensitized mice. J. Immunol. 1998. 160: 4090–4097.
34. Oeser, K., Maxeiner, J., Symowski, C., Stassen, M. and Voehringer, D., T cells are the critical source of IL-4/IL-13 in a mouse model of allergic asthma. Allergy 2015. 70: 1440–1449.
35. Roediger, B., Kyle, R., Tay, S. S., Mitchell, A. J., Bolton, H. A., Guy, T. V., Tan, S. Y. et al., IL-2 is a critical regulator of group 2 innate lymphoid cell function during pulmonary inflammation. J. Allergy Clin. Immunol. 2015. 136: 1653–1663.
36. Van Gool, F., Molofsky, A. B., Morar, M. M., Rosenzwajg, M., Liang, H. E., Klatzmann, D., Locksley, R. M. et al., Interleukin-5-producing group 2 innate lymphoid cells control eosinophilia induced by interleukin-2 therapy. Blood 2014. 124: 3572–3576.
37. Moro, K., Kabata, H., Tanabe, M., Koga, S., Takeno, N., Mochizuki, M., Fukunaga, K. et al., Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat. Immunol. 2016. 17: 76–86.
38. Robinette, M. L., Fuchs, A., Cortez, V. S., Lee, J. S., Wang, Y., Durum, S. K., Gilfillan, S. et al., Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 2015. 16: 306–317.
39. Maazi, H., Patel, N., Sankaranarayanan, I., Suzuki, Y., Rigas, D., Soroosh, P., Freeman, G. J. et al., ICOS:ICOS-ligand interaction is required for type 2 innate lymphoid cell function, homeostasis, and induction of airway hyperreactivity. Immunity 2015. 42: 538–551.
40. Fichtner-Feigl, S., Strober, W., Kawakami, K., Puri, R. K. and Kitani, A., IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat. Med. 2006. 12: 99–106.
41. He, C. H., Lee, C. G., Dela Cruz, C. S., Lee, C. M., Zhou, Y., Ahangari, F., Ma, B. et al., Chitinase 3-like 1 regulates cellular and tissue responses via IL-13 receptor alpha2. Cell Rep. 2013. 4: 830–841.
42. Zhang, Y., Tang, J., Tian, Z., van Velkinburgh, J. C., Song, J., Wu, Y. and Ni, B., Innate lymphoid cells: a promising new regulator in fibrotic diseases. Int. Rev. Immunol. 2015: 1–16.
43. Luzina, I. G., Todd, N. W., Sundararajan, S. and Atamas, S. P., The cytokines of pulmonary fibrosis: much learned, much more to learn. Cytokine 2015. 74: 88–100.
44. Iijima, K., Kobayashi, T., Hara, K., Kephart, G. M., Ziegler, S. F., McKenzie, A. N. and Kita, H., IL-33 and thymic stromal lymphopoietin mediate immune pathology in response to chronic airborne allergen exposure. J. Immunol. 2014. 193: 1549–1559.
45. Bartemes, K. R., Kephart, G. M., Fox, S. J. and Kita, H., Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J. Allergy Clin. Immunol. 2014. 134: 671–678; e674.
46. Smith, S. G., Chen, R., Kjarsgaard, M., Huang, C., Oliveria, J. P., O'Byrne, P. M., Gauvreau, G. M. et al., Increased numbers of activated group 2 innate lymphoid cells in the airways of patients with severe asthma and persistent airway eosinophilia. J. Allergy Clin. Immunol. 2016. 137: 75–86; e78.
47. Kabata, H., Moro, K., Fukunaga, K., Suzuki, Y., Miyata, J., Masaki, K., Betsuyaku, T. et al., Thymic stromal lymphopoietin induces corticosteroid resistance in natural helper cells during airway inflammation. Nat. Commun. 2013. 4: 2675.
48. Lee, P. P., Fitzpatrick, D. R., Beard, C., Jessup, H. K., Lehar, S., Makar, K. W., Perez-Melgosa, M. et al., A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 2001. 15: 763–774.
49. KleinJan, A., Klein Wolterink, R. G., Levani, Y., de Bruijn, M. J., Hoogsteden, H. C., van Nimwegen, M. and Hendriks, R. W., Enforced expression of Gata3 in T cells and group 2 innate lymphoid cells increases susceptibility to allergic airway inflammation in mice. J. Immunol. 2014. 192: 1385–1394.