T-bet inhibits innate lymphoid cell–mediated eosinophilic airway inflammation by suppressing IL-9 production

Journal of Allergy and Clinical Immunology

Volumn 139, Issue 4, 2017, Pages 1355-1367.e6

  Matsuki, Ayako ^a   Takatori, Hiroaki ^a   Makita, Sohei ^a   Yokota, Masaya ^a   Tamachi, Tomohiro ^a   Suto, Akira ^a   Suzuki, Kotaro ^a   Hirose, Koichi ^a   Nakajima, Hiroshi ^a  

^a CHIBA UNIVERSITY   (Japan)

Author keywords

eosinophils; IL 9; innate lymphoid cells; T bet

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 33; INTERLEUKIN 9; INTERLEUKIN C2; TRANSCRIPTION FACTOR T BET; TRANSCRIPTOME; UNCLASSIFIED DRUG; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21; THY 1 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION PROFILING; LUNG; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; RNA SEQUENCE; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LOEFFLER PNEUMONIA; LYMPHOCYTE SUBPOPULATION; METABOLISM; PNEUMONIA; POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, THY-1; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNITY, INNATE; INTERLEUKIN-33; INTERLEUKIN-9; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PNEUMONIA; POLYMERASE CHAIN REACTION; PULMONARY EOSINOPHILIA; T-BOX DOMAIN PROTEINS;

EID: 84993949266     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.08.022     Document Type: Article

References (54)

1. 1 Spits, H., Cupedo, T., Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu Rev Immunol 30 (2012), 647–675.
2. 2 Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J.P., Eberl, G., et al. Innate lymphoid cells–a proposal for uniform nomenclature. Nat Rev Immunol 13 (2013), 145–149.
3. 3 Kim, B.S., Wojno, E.D., Artis, D., Innate lymphoid cells and allergic inflammation. Curr Opin Immunol 25 (2013), 738–744.
4. 4 Yu, S., Kim, H.Y., Chang, Y.J., DeKruyff, R.H., Umetsu, D.T., Innate lymphoid cells and asthma. J Allergy Clin Immunol 133 (2014), 943–950.
5. 5 Wong, S.H., Walker, J.A., Jolin, H.E., Drynan, L.F., Hams, E., Camelo, A., et al. Transcription factor RORα is critical for nuocyte development. Nat Immunol 13 (2012), 229–236.
6. 6 Halim, T.Y., MacLaren, A., Romanish, M.T., Gold, M.J., McNagny, K.M., Takei, F., Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37 (2012), 463–474.
7. 7 Hoyler, T., Klose, C.S., Souabni, A., Turqueti-Neves, A., Pfeifer, D., Rawlins, E.L., et al. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37 (2012), 634–648.
8. 8 Klein Wolterink, R.G., Serafini, N., van Nimwegen, M., Vosshenrich, C.A., de Bruijn, M.J., Fonseca Pereira, D., et al. Essential, 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 U S A 110 (2013), 10240–10245.
9. 9 Yang, Q., Monticelli, L.A., Saenz, S.A., Chi, A.W., Sonnenberg, G.F., Tang, J., et al. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 38 (2013), 694–704.
10. 10 Takatori, H., Kanno, Y., Watford, W.T., Tato, C.M., Weiss, G., Ivanov, I.I., et al. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 206 (2009), 35–41.
11. 11 Sanos, S.L., Vonarbourg, C., Mortha, A., Diefenbach, A., Control of epithelial cell function by interleukin-22-producing RORγt+ innate lymphoid cells. Immunology 132 (2011), 453–465.
12. 12 Possot, C., Schmutz, S., Chea, S., Boucontet, L., Louise, A., Cumano, A., et al. Notch signaling is necessary for adult, but not fetal, development of RORγt(+) innate lymphoid cells. Nat Immunol 12 (2011), 949–958.
13. 13 Serafini, N., Klein Wolterink, R.G., Satoh-Takayama, N., Xu, W., Vosshenrich, C.A., Hendriks, R.W., et al. Gata3 drives development of RORγt+ group 3 innate lymphoid cells. J Exp Med 211 (2014), 199–208.
14. 14 Szabo, S.J., Kim, S.T., Costa, G.L., Zhang, X., Fathman, C.G., Glimcher, L.H., A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000), 655–669.
15. 15 Lazarevic, V., Glimcher, L.H., T-bet in disease. Nat Immunol 12 (2011), 597–606.
16. 16 Sciumé, G., Hirahara, K., Takahashi, H., Laurence, A., Villarino, A.V., Singleton, K.L., et al. Distinct requirements for T-bet in gut innate lymphoid cells. J Exp Med 209 (2012), 2331–2338.
17. 17 Klose, C.S., Kiss, E.A., Schwierzeck, V., Ebert, K., Hoyler, T., d'Hargues, Y., et al. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 494 (2013), 261–265.
18. 18 Rankin, L.C., Groom, J.R., Chopin, M., Herold, M.J., Walker, J.A., Mielke, L.A., et al. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat Immunol 14 (2013), 389–395.
19. 19 Lambrecht, B.N., Hammad, H., The immunology of asthma. Nat Immunol 16 (2015), 45–56.
20. 20 Licona-Limón, P., Kim, L.K., Palm, N.W., Flavell, R.A., TH2, allergy and group 2 innate lymphoid cells. Nat Immunol 14 (2013), 536–542.
21. 21 Halim, T.Y., Steer, C.A., Mathä, L., Gold, M.J., Martinez-Gonzalez, I., McNagny, K.M., et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40 (2014), 425–435.
22. 22 Finotto, S., Neurath, M.F., Glickman, J.N., Qin, S., Lehr, H.A., Green, F.H., et al. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 295 (2002), 336–338.
23. 23 Fujiwara, M., Hirose, K., Kagami, S., Takatori, H., Wakashin, H., Tamachi, T., et al. T-bet inhibits both TH2 cell-mediated eosinophil recruitment and TH17 cell-mediated neutrophil recruitment into the airways. J Allergy Clin Immunol 119 (2007), 662–670.
24. 24 Takatori, H., Nakajima, H., Hirose, K., Kagami, S., Tamachi, T., Suto, A., et al. Indispensable role of Stat5a in Stat6-independent Th2 cell differentiation and allergic airway inflammation. J Immunol 174 (2005), 3734–3740.
25. 25 Tanaka, S., Suto, A., Iwamoto, T., Kashiwakuma, D., Kagami, S., Suzuki, K., et al. Sox5 and c-Maf cooperatively induce Th17 cell differentiation via RORγt induction as downstream targets of Stat3. J Exp Med 211 (2014), 1857–1874.
26. 26 Kadota, K., Nakai, Y., Shimizu, K., Ranking differentially expressed genes from Affymetrix gene expression data: methods with reproducibility, sensitivity, and specificity. Algorithms Mol Biol, 4, 2009, 7.
27. 27 Molofsky, A.B., Van Gool, F., Liang, H.E., Van Dyken, S.J., Nussbaum, J.C., Lee, J., et al. Interleukin-33 and interferon-γ counter-regulate group 2 innate lymphoid cell activation during immune perturbation. Immunity 43 (2015), 161–174.
28. 28 Duerr, C.U., McCarthy, C.D., Mindt, B.C., Rubio, M., Meli, A.P., Pothlichet, J., et al. Type I interferon restricts type 2 immunopathology through the regulation of group 2 innate lymphoid cells. Nat Immunol 17 (2016), 65–75.
29. 29 Moro, K., Kabata, H., Tanabe, M., Koga, S., Takeno, N., Mochizuki, M., et al. Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat Immunol 17 (2016), 76–86.
30. 30 Lighvani, A.A., Frucht, D.M., Jankovic, D., Yamane, H., Aliberti, J., Hissong, B.D., et al. T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc Natl Acad Sci U S A 98 (2001), 15137–15142.
31. 31 Zhu, J., Jankovic, D., Oler, A.J., Wei, G., Sharma, S., Hu, G., et al. The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 37 (2012), 660–673.
32. 32 Klein Wolterink, R.G., Kleinjan, A., van Nimwegen, M., Bergen, I., de Bruijn, M., Levani, Y., et al. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol 42 (2012), 1106–1116.
33. 33 Monticelli, L.A., Sonnenberg, G.F., Abt, M.C., Alenghat, T., Ziegler, C.G., Doering, T.A., et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol 12 (2011), 1045–1054.
34. 34 Powell, N., Walker, A.W., Stolarczyk, E., Canavan, J.B., Gökmen, M.R., Marks, E., et al. The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells. Immunity 37 (2012), 674–684.
35. 35 Halim, T.Y., Krauss, R.H., Sun, A.C., Takei, F., Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36 (2012), 451–463.
36. 36 Neill, D.R., Wong, S.H., Bellosi, A., Flynn, R.J., Daly, M., Langford, T.K., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464 (2010), 1367–1370.
37. 37 Ermann, J., Staton, T., Glickman, J.N., de Waal Malefyt, R., Glimcher, L.H., Nod/Ripk2 signaling in dendritic cells activates IL-17A-secreting innate lymphoid cells and drives colitis in T-bet-/-.Rag2-/- (TRUC) mice. Proc Natl Acad Sci U S A 111 (2014), E2559–E2566.
38. 38 Mirchandani, A.S., Besnard, A.G., Yip, E., Scott, C., Bain, C.C., Cerovic, V., et al. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J Immunol 192 (2014), 2442–2448.
39. 39 Morita, H., Arae, K., Unno, H., Miyauchi, K., Toyama, S., Nambu, A., et al. An interleukin-33-mast cell-interleukin-2 axis suppresses papain-induced allergic inflammation by promoting regulatory T cell numbers. Immunity 43 (2015), 175–186.
40. 40 Veldhoen, M., Uyttenhove, C., van Snick, J., Helmby, H., Westendorf, A., Buer, J., et al. Transforming growth factor-beta ‘reprograms’ the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol 9 (2008), 1341–1346.
41. 41 Chang, H.C., Sehra, S., Goswami, R., Yao, W., Yu, Q., Stritesky, G.L., et al. The transcription factor PU.1 is required for the development of IL-9-producing T cells and allergic inflammation. Nat Immunol 11 (2010), 527–534.
42. 42 Staudt, V., Bothur, E., Klein, M., Lingnau, K., Reuter, S., Grebe, N., et al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33 (2010), 192–202.
43. 43 Jabeen, R., Goswami, R., Awe, O., Kulkarni, A., Nguyen, E.T., Attenasio, A., et al. Th9 cell development requires a BATF-regulated transcriptional network. J Clin Invest 123 (2013), 4641–4653.
44. 44 Wilhelm, C., Hirota, K., Stieglitz, B., Van Snick, J., Tolaini, M., Lahl, K., et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat Immunol 12 (2011), 1071–1077.
45. 45 Turner, J.E., Morrison, P.J., Wilhelm, C., Wilson, M., Ahlfors, H., Renauld, J.C., et al. IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J Exp Med 210 (2013), 2951–2965.
46. 46 Tantisira, K.G., Hwang, E.S., Raby, B.A., Silverman, E.S., Lake, S.L., Richter, B.G., et al. TBX21: a functional variant predicts improvement in asthma with the use of inhaled corticosteroids. Proc Natl Acad Sci U S A 101 (2004), 18099–18104.
47. 47 Raby, B.A., Hwang, E.S., Van Steen, K., Tantisira, K., Peng, S., Litonjua, A., et al. T-bet polymorphisms are associated with asthma and airway hyperresponsiveness. Am J Respir Crit Care Med 173 (2006), 64–70.
48. 48 Munthe-Kaas, M.C., Carlsen, K.H., Håland, G., Devulapalli, C.S., Gervin, K., Egeland, T., et al. T cell-specific T-box transcription factor haplotype is associated with allergic asthma in children. J Allergy Clin Immunol 121 (2008), 51–56.
49. 49 Suttner, K., Rosenstiel, P., Depner, M., Schedel, M., Pinto, L.A., Ruether, A., et al. TBX21 gene variants increase childhood asthma risk in combination with HLX1 variants. J Allergy Clin Immunol 123 (2009), 1062–1068 e1-8.
50. 50 Barlow, J.L., Bellosi, A., Hardman, C.S., Drynan, L.F., Wong, S.H., Cruickshank, J.P., et al. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol 129 (2012), 191–198 e1-4.
51. 51 Djuretic, I.M., Levanon, D., Negreanu, V., Groner, Y., Rao, A., Ansel, K.M., Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nat Immunol 8 (2007), 145–153.
52. 52 Yang, X.O., Zhang, H., Kim, B.S., Niu, X., Peng, J., Chen, Y., et al. The signaling suppressor CIS controls proallergic T cell development and allergic airway inflammation. Nat Immunol 14 (2013), 732–740.
53. 53 Mohapatra, A., Van Dyken, S.J., Schneider, C., Nussbaum, J.C., Liang, H.E., Locksley, R.M., Group 2 innate lymphoid cells utilize the IRF4-IL-9 module to coordinate epithelial cell maintenance of lung homeostasis. Mucosal Immunol 9 (2016), 275–286.
54. 54 Kudo, F., Ikutani, M., Seki, Y., Otsubo, T., Kawamura, Y.I., Dohi, T., et al. Interferon-γ constrains cytokine production of group 2 innate lymphoid cells. Immunology 147 (2016), 21–29.