At the bench: Understanding group 2 innate lymphoid cells in disease

Journal of Leukocyte Biology

Volumn 97, Issue 3, 2015, Pages 455-467

  Doherty, Taylor A ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Allergy; Asthma; Atopic dermatitis; ILC2

Indexed keywords

ADAPTIVE IMMUNITY; ASTHMA; ATOPIC DERMATITIS; BASIC RESEARCH; CELL FUNCTION; CLINICAL RESEARCH; CYTOKINE RELEASE SYNDROME; DISEASE MODEL; DISEASES; EXPERIMENTAL ASTHMA; EXPERIMENTAL SKIN DISEASE; GROUP 2 INNATE LYMPHOID CELL; HEALTH; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; LUNG DISEASE; LYMPHOID CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TH2 CELL; TRANSLATIONAL RESEARCH; ANIMAL; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE;

MUS; VERMES;

ANIMALS; DISEASE; DISEASE MODELS, ANIMAL; HEALTH; HUMANS; IMMUNITY, INNATE; LYMPHOCYTES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84929152818     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.5BT0814-374R     Document Type: Review

References (113)

1. Busse, W. W., Lemanske, Jr., R. F. (2001) Asthma. N. Engl. J. Med. 344, 350–362.
2. Dulek, D. E., Peebles, R. S., Jr. (2011) Viruses and asthma. Biochim. Biophys. Acta 1810, 1080–1090.
3. Guarnieri, M., Balmes, J. R. (2014) Outdoor air pollution and asthma. Lancet 383, 1581–1592.
4. Silvestri, M., Franchi, S., Pistorio, A., Petecchia, L., Rusconi, F. (2014) Smoke exposure, wheezing, and asthma development: a systematic review and meta-analysis in unselected birth cohorts. Pediatr. Pulmonol. doi: 10.1002/ppul.23037. [Epub ahead of print].
5. Peebles, Jr., S. (2014) At the Bedside: The emergence of group 2 innate lymphoid cells in human disease. J. Leuko. Bio. 97, 469–475.
6. Fort, M. M., Cheung, J., Yen, D., Li, J., Zurawski, S. M., Lo, S., Menon, S., Clifford, T., Hunte, B., Lesley, R., Muchamuel, T., Hurst, S. D., Zurawski, G., Leach, M. W., Gorman, D. M., Rennick, D. M. (2001) IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15, 985–995.
7. Hurst, S. D., Muchamuel, T., Gorman, D. M., Gilbert, J. M., Clifford, T., Kwan, S., Menon, S., Seymour, B., Jackson, C., Kung, T. T., Brieland, J. K., Zurawski, S. M., Chapman, R. W., Zurawski, G., Coffman, R. L. (2002) New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J. Immunol. 169, 443–453.
8. Fallon, P. G., Ballantyne, S. J., Mangan, N. E., Barlow, J. L., Dasvarma, A., Hewett, D. R., McIlgorm, A., Jolin, H. E., McKenzie, A. N. (2006) Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 203, 1105–1116.
9. Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., Bucks, C., Kane, C. M., Fallon, P. G., Pannell, R., Jolin, H. E., McKenzie, A. N. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367–1370.
10. Price, A. E., Liang, H. E., Sullivan, B. M., Reinhardt, R. L., Eisley, C. J., Erle, D. J., Locksley, R. M. (2010) Systemically dispersed innate IL-13- expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA 107, 11489–11494.
11. Moro, K., Yamada, T., Tanabe, M., Takeuchi, T., Ikawa, T., Kawamoto, H., Furusawa, J., Ohtani, M., Fujii, H., Koyasu, S. (2010) Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca- 1(+) lymphoid cells. Nature 463, 540–544.
12. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S., Locksley, R. M., McKenzie, A. N., Mebius, R. E., Powrie, F., Vivier, E. (2013) Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13, 145–149.
13. Yang, Q., Saenz, S. A., Zlotoff, D. A., Artis, D., Bhandoola, A. (2011) Cutting edge: natural helper cells derive from lymphoid progenitors. J. Immunol. 187, 5505–5509.
14. Yokota, Y., Mansouri, A., Mori, S., Sugawara, S., Adachi, S., Nishikawa, S., Gruss, P. (1999) Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397, 702–706.
15. Satoh-Takayama, N., Lesjean-Pottier, S., Vieira, P., Sawa, S., Eberl, G., Vosshenrich, C. A., Di Santo, J. P. (2010) IL-7 and IL-15 independently program the differentiation of intestinal CD32NKp46+ cell subsets from Id2-dependent precursors. J. Exp. Med. 207, 273–280.
16. Bartemes, K. R., Iijima, K., Kobayashi, T., Kephart, G. M., McKenzie, A. N., Kita, H. (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.
17. Doherty, T. A., Khorram, N., Chang, J. E., Kim, H. K., Rosenthal, P., Croft, M., Broide, D. H. (2012) STAT6 regulates natural helper cell proliferation during lung inflammation initiated by Alternaria. Am. J. Physiol. Lung Cell. Mol. Physiol. 303, L577–L588.
18. Siddiqui, S., Secor, Jr., E. R., Silbart, L. K. (2013) Broncho-alveolar macrophages express chemokines associated with leukocyte migration in a mouse model of asthma. Cell. Immunol. 281, 159–169.
19. Kelly, E. A., Koziol-White, C. J., Clay, K. J., Liu, L. Y., Bates, M. E., Bertics, P. J., Jarjour, N. N. (2009) Potential contribution of IL-7 to allergeninduced eosinophilic airway inflammation in asthma. J. Immunol. 182, 1404–1410.
20. Mjösberg, J., Bernink, J., Golebski, K., Karrich, J. J., Peters, C. P., Blom, B., te Velde, A. A., Fokkens, W. J., van Drunen, C. M., Spits, H. (2012) The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37, 649–659.
21. Klein Wolterink, R. G., Serafini, N., van Nimwegen, M., Vosshenrich, C. A., de Bruijn, M. J., Fonseca Pereira, D., Veiga Fernandes, H., Hendriks, R. W., Di Santo, J. P. (2013) 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. USA 110, 10240–10245.
22. Hoyler, T., Klose, C. S., Souabni, A., Turqueti-Neves, A., Pfeifer, D., Rawlins, E. L., Voehringer, D., Busslinger, M., Diefenbach, A. (2012) The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37, 634–648.
23. Yagi, R., Zhong, C., Northrup, D. L., Yu, F., Bouladoux, N., Spencer, S., Hu, G., Barron, L., Sharma, S., Nakayama, T., Belkaid, Y., Zhao, K., Zhu, J. (2014) The transcription factor GATA3 is critical for the development of all IL-7Ra-expressing innate lymphoid cells. Immunity 40, 378–388.
24. Serafini, N., Klein Wolterink, R. G., Satoh-Takayama, N., Xu, W., Vosshenrich, C. A., Hendriks, R. W., Di Santo, J. P. (2014) Gata3 drives development of RORgt+ group 3 innate lymphoid cells. J. Exp. Med. 211, 199–208.
25. Walunas, T. L., Wang, B., Wang, C. R., Leiden, J. M. (2000) Cutting edge: the Ets1 transcription factor is required for the development of NK T cells in mice. J. Immunol. 164, 2857–2860.
26. Barton, K., Muthusamy, N., Fischer, C., Ting, C. N., Walunas, T. L., Lanier, L. L., Leiden, J. M. (1998) The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 9, 555–563.
27. Strempel, J. M., Grenningloh, R., Ho, I. C., Vercelli, D. (2010) Phylogenetic and functional analysis identifies Ets-1 as a novel regulator of the Th2 cytokine gene locus. J. Immunol. 184, 1309–1316.
28. Wong, S. H., Walker, J. A., Jolin, H. E., Drynan, L. F., Hams, E., Camelo, A., Barlow, J. L., Neill, D. R., Panova, V., Koch, U., Radtke, F., Hardman, C. S., Hwang, Y. Y., Fallon, P. G., McKenzie, A. N. (2012) Transcription factor RORa is critical for nuocyte development. Nat. Immunol. 13, 229–236.
29. Halim, T. Y., MacLaren, A., Romanish, M. T., Gold, M. J., McNagny, K. M., Takei, F. (2012) Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37, 463–474.
30. Moffatt, M. F., Gut, I. G., Demenais, F., Strachan, D. P., Bouzigon, E., Heath, S., von Mutius, E., Farrall, M., Lathrop, M., Cookson, W. O.; GABRIEL Consortium. (2010) A large-scale, consortium-based genomewide association study of asthma. N. Engl. J. Med. 363, 1211–1221.
31. Mielke, L. A., Groom, J. R., Rankin, L. C., Seillet, C., Masson, F., Putoczki, T., Belz, G. T. (2013) TCF-1 controls ILC2 and NKp46+ RORgammat+ innate lymphocyte differentiation and protection in intestinal inflammation. J. Immunol. 191, 4383–4391.
32. Constantinides, M. G., McDonald, B. D., Verhoef, P. A., Bendelac, A. (2014) A committed precursor to innate lymphoid cells. Nature 508, 397–401.
33. Mjösberg, J. M., Trifari, S., Crellin, N. K., Peters, C. P., van Drunen, C. M., Piet, B., Fokkens, W. J., Cupedo, T., Spits, H. (2011) Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat. Immunol. 12, 1055–1062.
34. Doherty, T. A., Khorram, N., Lund, S., Mehta, A. K., Croft, M., Broide, D. H. (2013) Lung type 2 innate lymphoid cells express cysteinyl leukotriene receptor 1, which regulates TH2 cytokine production. J. Allergy Clin. Immunol. 132, 205–213.
35. Kurowska-Stolarska, M., Kewin, P., Murphy, G., Russo, R. C., Stolarski, B., Garcia, C. C., Komai-Koma, M., Pitman, N., Li, Y., Niedbala, W., McKenzie, A. N., Teixeira, M. M., Liew, F. Y., Xu, D. (2008) IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. J. Immunol. 181, 4780–4790.
36. Chang, Y. J., Kim, H. Y., Albacker, L. A., Baumgarth, N., McKenzie, A. N., Smith, D. E., Dekruyff, R. H., Umetsu, D. T. (2011) Innate lymphoid cells mediate influenza-induced airway hyperreactivity independently of adaptive immunity. Nat. Immunol. 12, 631–638.
37. Barlow, J. L., Bellosi, A., Hardman, C. S., Drynan, L. F., Wong, S. H., Cruickshank, J. P., McKenzie, A. N. (2012) Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J. Allergy Clin. Immunol. 129, 191-8 e1-4.
38. Nussbaum, J. C., Van Dyken, S. J., von Moltke, J., Cheng, L. E., Mohapatra, A., Molofsky, A. B., Thornton, E. E., Krummel, M. F., Chawla, A., Liang, H. E., Locksley, R. M. (2013) Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502, 245–248.
39. Wilhelm, C., Hirota, K., Stieglitz, B., Van Snick, J., Tolaini, M., Lahl, K., Sparwasser, T., Helmby, H., Stockinger, B. (2011) An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat. Immunol. 12, 1071–1077.
40. Soroosh, P., Doherty, T. A. (2009) Th9 and allergic disease. Immunology 127, 450–458.
41. Monticelli, L. A., Sonnenberg, G. F., Abt, M. C., Alenghat, T., Ziegler, C. G., Doering, T. A., Angelosanto, J. M., Laidlaw, B. J., Yang, C. Y., Sathaliyawala, T., Kubota, M., Turner, D., Diamond, J. M., Goldrath, A. W., Farber, D. L., Collman, R. G., Wherry, E. J., Artis, D. (2011) Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12, 1045–1054.
42. Molofsky, A. B., Nussbaum, J. C., Liang, H. E., Van Dyken, S. J., Cheng, L. E., Mohapatra, A., Chawla, A., Locksley, R. M. (2013) Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 210, 535–549.
43. Hams, E., Locksley, R. M., McKenzie, A. N., Fallon, P. G. (2013) Cutting edge: IL-25 elicits innate lymphoid type 2 and type II NKT cells that regulate obesity in mice. J. Immunol. 191, 5349–5353.
44. Carriere, V., Roussel, L., Ortega, N., Lacorre, D. A., Americh, L., Aguilar, L., Bouche, G., Girard, J. P. (2007) IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. USA 104, 282–287.
45. Lefrançais, E., Roga, S., Gautier, V., Gonzalez-de-Peredo, A., Monsarrat, B., Girard, J. P., Cayrol, C. (2012) IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc. Natl. Acad. Sci. USA 109, 1673–1678.
46. Gu, C., Wu, L., Li, X. (2013) IL-17 family: cytokines, receptors and signaling. Cytokine 64, 477–485.
47. Lloyd, C. M. (2010) IL-33 family members and asthma - bridging innate and adaptive immune responses. Curr. Opin. Immunol. 22, 800–806.
48. Doherty, T. A., Khorram, N., Sugimoto, K., Sheppard, D., Rosenthal, P., Cho, J. Y., Pham, A., Miller, M., Croft, M., Broide, D. H. (2012) Alternaria induces STAT6-dependent acute airway eosinophilia and epithelial FIZZ1 expression that promotes airway fibrosis and epithelial thickness. J. Immunol. 188, 2622–2629.
49. Kouzaki, H., Iijima, K., Kobayashi, T., O’Grady, S. M., Kita, H. (2011) The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J. Immunol. 186, 4375–4387.
50. Tamachi, T., Maezawa, Y., Ikeda, K., Kagami, S., Hatano, M., Seto, Y., Suto, A., Suzuki, K., Watanabe, N., Saito, Y., Tokuhisa, T., Iwamoto, I., Nakajima, H. (2006) IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J. Allergy Clin. Immunol. 118, 606–614.
51. Angkasekwinai, P., Park, H., Wang, Y. H., Wang, Y. H., Chang, S. H., Corry, D. B., Liu, Y. J., Zhu, Z., Dong, C. (2007) Interleukin 25 promotes the initiation of proallergic type 2 responses. J. Exp. Med. 204, 1509–1517.
52. Barlow, J. L., Peel, S., Fox, J., Panova, V., Hardman, C. S., Camelo, A., Bucks, C., Wu, X., Kane, C. M., Neill, D. R., Flynn, R. J., Sayers, I., Hall, I. P., McKenzie, A. N. (2013) IL-33 is more potent than IL-25 in provoking IL-13-producing nuocytes (type 2 innate lymphoid cells) and airway contraction. J. Allergy Clin. Immunol. 132, 933–941.
53. Paul, W. E., Zhu, J. (2010) How are T(H)2-type immune responses initiated and amplified? Nat. Rev. Immunol. 10, 225–235.
54. Ito, T., Wang, Y. H., Duramad, O., Hori, T., Delespesse, G. J., Watanabe, N., Qin, F. X., Yao, Z., Cao, W., Liu, Y. J. (2005) TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202, 1213–1223.
55. Al-Shami, A., Spolski, R., Kelly, J., Keane-Myers, A., Leonard, W. J. (2005) A role for TSLP in the development of inflammation in an asthma model. J. Exp. Med. 202, 829–839.
56. Halim, T. Y., Krauss, R. H., Sun, A. C., Takei, F. (2012) Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36, 451–463.
57. Kim, B. S., Siracusa, M. C., Saenz, S. A., Noti, M., Monticelli, L. A., Sonnenberg, G. F., Hepworth, M. R., Van Voorhees, A. S., Comeau, M. R., Artis, D. (2013) TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci. Transl. Med. 5, 170ra16.
58. Barnig, C., Cernadas, M., Dutile, S., Liu, X., Perrella, M. A., Kazani, S., Wechsler, M. E., Israel, E., Levy, B. D. (2013) Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci. Transl. Med. 5, 174ra26.
59. Boyce, J. A. (2007) Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol. Rev. 217, 168–185.
60. Hirai, H., Tanaka, K., Yoshie, O., Ogawa, K., Kenmotsu, K., Takamori, Y., Ichimasa, M., Sugamura, K., Nakamura, M., Takano, S., Nagata, K. (2001) Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J. Exp. Med. 193, 255–261.
61. Xue, L., Salimi, M., Panse, I., Mjösberg, J. M., McKenzie, A. N., Spits, H., Klenerman, P., Ogg, G. (2014) Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells. J. Allergy Clin. Immunol. 133, 1184–1194.
62. Fajt, M. L., Gelhaus, S. L., Freeman, B., Uvalle, C. E., Trudeau, J. B., Holguin, F., Wenzel, S. E. (2013) Prostaglandin D₂ pathway upregulation: relation to asthma severity, control, and TH2 inflammation. J. Allergy Clin. Immunol. 131, 1504–1512.
63. Xue, L., Gyles, S. L., Wettey, F. R., Gazi, L., Townsend, E., Hunter, M. G., Pettipher, R. (2005) Prostaglandin D2 causes preferential induction of proinflammatory Th2 cytokine production through an action on chemoattractant receptor-like molecule expressed on Th2 cells. J. Immunol. 175, 6531–6536.
64. Xue, L., Barrow, A., Pettipher, R. (2009) Novel function of CRTH2 in preventing apoptosis of human Th2 cells through activation of the phosphatidylinositol 3-kinase pathway. J. Immunol. 182, 7580–7586.
65. Chang, J. E., Doherty, T. A., Baum, R., Broide, D. (2013) Prostaglandin D2 regulates human type 2 innate lymphoid cell chemotaxis. J. Allergy Clin. Immunol. 133, 899–901.e3.
66. Croft, M. (2009) The role of TNF superfamily members in T-cell function and diseases. Nat. Rev. Immunol. 9, 271–285.
67. Ware, C. F. (2003) The TNF superfamily. Cytokine Growth Factor Rev. 14, 181–184.
68. Meylan, F., Davidson, T. S., Kahle, E., Kinder, M., Acharya, K., Jankovic, D., Bundoc, V., Hodges, M., Shevach, E. M., Keane-Myers, A., Wang, E. C., Siegel, R. M. (2008) The TNF-family receptor DR3 is essential for diverse T cell-mediated inflammatory diseases. Immunity 29, 79–89.
69. Meylan, F., Richard, A. C., Siegel, R. M. (2011) TL1A and DR3, a TNF family ligand-receptor pair that promotes lymphocyte costimulation, mucosal hyperplasia, and autoimmune inflammation. Immunol. Rev. 244, 188–196.
70. Yu, X., Pappu, R., Ramirez-Carrozzi, V., Ota, N., Caplazi, P., Zhang, J., Yan, D., Xu, M., Lee, W. P., Grogan, J. L. (2014) TNF superfamily member TL1A elicits type 2 innate lymphoid cells at mucosal barriers. Mucosal Immunol. 7, 730–740.
71. Mirchandani, A. S., Besnard, A. G., Yip, E., Scott, C., Bain, C. C., Cerovic, V., Salmond, R. J., Liew, F. Y. (2014) Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J. Immunol. 192, 2442–2448.
72. Drake, L. Y., Iijima, K., Kita, H. (2014) Group 2 innate lymphoid cells and CD4+ T cells cooperate to mediate type 2 immune response in mice. Allergy 69, 1300–1307.
73. Halim, T. Y., Steer, C. A., Mathä, L., Gold, M. J., Martinez-Gonzalez, I., McNagny, K. M., McKenzie, A. N., Takei, F. (2014) Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cellmediated allergic lung inflammation. Immunity 40, 425–435.
74. Gold, M. J., Antignano, F., Halim, T. Y., Hirota, J. A., Blanchet, M. R., Zaph, C., Takei, F., McNagny, K. M. (2014) Group 2 innate lymphoid cells facilitate sensitization to local, but not systemic, TH2-inducing allergen exposures. J. Allergy Clin. Immunol. 133, 1142–1148.
75. Sokol, C. L., Barton, G. M., Farr, A. G., Medzhitov, R. (2008) A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9, 310–318.
76. Siracusa, M. C., Kim, B. S., Spergel, J. M., Artis, D. (2013) Basophils and allergic inflammation. J. Allergy Clin. Immunol. 132, 789–801, quiz 788.
77. Motomura, Y., Morita, H., Moro, K., Nakae, S., Artis, D., Endo, T. A., Kuroki, Y., Ohara, O., Koyasu, S., Kubo, M. (2014) Basophil-derived interleukin-4 controls the function of natural helper cells, a member of ILC2s, in lung inflammation. Immunity 40, 758–771.
78. Roediger, B., Kyle, R., Yip, K. H., Sumaria, N., Guy, T. V., Kim, B. S., Mitchell, A. J., Tay, S. S., Jain, R., Forbes-Blom, E., Chen, X., Tong, P. L., Bolton, H. A., Artis, D., Paul, W. E., Fazekas de St Groth, B., Grimbaldeston, M. A., Le Gros, G., Weninger, W. (2013) Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat. Immunol. 14, 564–573.
79. Fukuoka, A., Futatsugi-Yumikura, S., Takahashi, S., Kazama, H., Iyoda, T., Yoshimoto, T., Inaba, K., Nakanishi, K., Yonehara, S. (2013) Identification of a novel type 2 innate immunocyte with the ability to enhance IgE production. Int. Immunol. 25, 373–382.
80. Klein Wolterink, R. G., Kleinjan, A., van Nimwegen, M., Bergen, I., de Bruijn, M., Levani, Y., Hendriks, R. W. (2012) Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur. J. Immunol. 42, 1106–1116.
81. Kabata, H., Moro, K., Fukunaga, K., Suzuki, Y., Miyata, J., Masaki, K., Betsuyaku, T., Koyasu, S., Asano, K. (2013) Thymic stromal lymphopoietin induces corticosteroid resistance in natural helper cells during airway inflammation. Nat. Commun. 4, 2675.
82. Kim, B. S., Wang, K., Siracusa, M. C., Saenz, S. A., Brestoff, J. R., Monticelli, L. A., Noti, M., Tait Wojno, E. D., Fung, T. C., Kubo, M., Artis, D. (2014) Basophils promote innate lymphoid cell responses in inflamed skin. J. Immunol. 193, 3717–3725.
83. Salimi, M., Barlow, J. L., Saunders, S. P., Xue, L., Gutowska-Owsiak, D., Wang, X., Huang, L. C., Johnson, D., Scanlon, S. T., McKenzie, A. N., Fallon, P. G., Ogg, G. S. (2013) A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J. Exp. Med. 210, 2939–2950.
84. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T. K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., Gorman, D. M., Bazan, J. F., Kastelein, R. A. (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23, 479–490.
85. Ho, L. H., Ohno, T., Oboki, K., Kajiwara, N., Suto, H., Iikura, M., Okayama, Y., Akira, S., Saito, H., Galli, S. J., Nakae, S. (2007) IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcepsilonRI signals. J. Leukoc. Biol. 82, 1481–1490.
86. Smithgall, M. D., Comeau, M. R., Yoon, B. R., Kaufman, D., Armitage, R., Smith, D. E. (2008) IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int. Immunol. 20, 1019–1030.
87. Suzukawa, M., Iikura, M., Koketsu, R., Nagase, H., Tamura, C., Komiya, A., Nakae, S., Matsushima, K., Ohta, K., Yamamoto, K., Yamaguchi, M. (2008) An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J. Immunol. 181, 5981–5989.
88. Doherty, T. A., Soroosh, P., Broide, D. H., Croft, M. (2009) CD4+ cells are required for chronic eosinophilic lung inflammation but not airway remodeling. Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L229–L235.
89. Kim, H. K., Lund, S., Baum, R., Rosenthal, P., Khorram, N., Doherty, T. A. (2014) Innate type 2 response to Alternaria extract enhances ryegrass-induced lung inflammation. Int. Arch. Allergy Immunol. 163, 92–105.
90. Bush, R. K., Prochnau, J. J. (2004) Alternaria-induced asthma. J. Allergy Clin. Immunol. 113, 227–234.
91. Holt, P. G., Strickland, D. H., Sly, P. D. (2012) Virus infection and allergy in the development of asthma: what is the connection? Curr. Opin. Allergy Clin. Immunol. 12, 151–157.
92. Hong, J. Y., Bentley, J. K., Chung, Y., Lei, J., Steenrod, J. M., Chen, Q., Sajjan, U. S., Hershenson, M. B. (2014) Neonatal rhinovirus induces mucous metaplasia and airways hyperresponsiveness through IL-25 and type 2 innate lymphoid cells. J. Allergy Clin. Immunol. 134, 429–439.
93. Walford, H. H., Doherty, T. A. (2014) Diagnosis and management of eosinophilic asthma: a US perspective. J. Asthma Allergy 7, 53–65.
94. Walford, H. H., Lund, S. J., Baum, R. E., White, A. A., Bergeron, C. M., Husseman, J., Bethel, K. J., Scott, D. R., Khorram, N., Miller, M., Broide, D. H., Doherty, T. A. (2014) Increased ILC2s in the eosinophilic nasal polyp endotype are associated with corticosteroid responsiveness. Clin. Immunol. 155, 126–135.
95. Li, D., Guabiraba, R., Besnard, A. G., Komai-Koma, M., Jabir, M. S., Zhang, L., Graham, G. J., Kurowska-Stolarska, M., Liew, F. Y., McSharry, C., Xu, D. (2014) IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice. J. Allergy Clin. Immunol. pii: S0091-6749(14)00670-8 [Epub ahead of print].
96. Allakhverdi, Z., Comeau, M. R., Smith, D. E., Toy, D., Endam, L. M., Desrosiers, M., Liu, Y. J., Howie, K. J., Denburg, J. A., Gauvreau, G. M., Delespesse, G. (2009) CD34+ hemopoietic progenitor cells are potent effectors of allergic inflammation. J. Allergy Clin. Immunol. 123, 472–478.
97. Bartemes, K. R., Kephart, G. M., Fox, S. J., Kita, H. (2014) Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J. Allergy Clin. Immunol. 134, 671–678 e4.
98. Préfontaine, D., Lajoie-Kadoch, S., Foley, S., Audusseau, S., Olivenstein, R., Halayko, A. J., Lemiére, C., Martin, J. G., Hamid, Q. (2009) Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J. Immunol. 183, 5094–5103.
99. Oshikawa, K., Kuroiwa, K., Tago, K., Iwahana, H., Yanagisawa, K., Ohno, S., Tominaga, S. I., Sugiyama, Y. (2001) Elevated soluble ST2 protein levels in sera of patients with asthma with an acute exacerbation. Am. J. Respir. Crit. Care Med. 164, 277–281.
100. Corrigan, C. J., Wang, W., Meng, Q., Fang, C., Eid, G., Caballero, M. R., Lv, Z., An, Y., Wang, Y. H., Liu, Y. J., Kay, A. B., Lee, T. H., Ying, S. (2011) Allergen-induced expression of IL-25 and IL-25 receptor in atopic asthmatic airways and late-phase cutaneous responses. J. Allergy Clin. Immunol. 128, 116–124.
101. Ying, S., O’Connor, B., Ratoff, J., Meng, Q., Mallett, K., Cousins, D., Robinson, D., Zhang, G., Zhao, J., Lee, T. H., Corrigan, C. (2005) Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J. Immunol. 174, 8183–8190.
102. Hamilos, D. L. (2011) Chronic rhinosinusitis: epidemiology and medical management. J. Allergy Clin. Immunol. 128, 693–707, quiz 708–709.
103. Akdis, C. A., Bachert, C., Cingi, C., Dykewicz, M. S., Hellings, P. W., Naclerio, R. M., Schleimer, R. P., Ledford, D. (2013) Endotypes and phenotypes of chronic rhinosinusitis: a PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J. Allergy Clin. Immunol. 131, 1479–1490.
104. Shaw, J. L., Fakhri, S., Citardi, M. J., Porter, P. C., Corry, D. B., Kheradmand, F., Liu, Y. J., Luong, A. (2013) IL-33-responsive innate lymphoid cells are an important source of IL-13 in chronic rhinosinusitis with nasal polyps. Am. J. Respir. Crit. Care Med. 188, 432–439.
105. Miljkovic, D., Bassiouni, A., Cooksley, C., Ou, J., Hauben, E., Wormald, P. J., Vreugde, S. (2014) Association between group 2 innate lymphoid cells enrichment, nasal polyps and allergy in chronic rhinosinusitis. Allergy 69, 1154–1161.
106. Nagarkar, D. R., Poposki, J. A., Tan, B. K., Comeau, M. R., Peters, A. T., Hulse, K. E., Suh, L. A., Norton, J., Harris, K. E., Grammer, L. C., Chandra, R. K., Conley, D. B., Kern, R. C., Schleimer, R. P., Kato, A. (2013) Thymic stromal lymphopoietin activity is increased in nasal polyps of patients with chronic rhinosinusitis. J. Allergy Clin. Immunol. 132, 593–600 e12.
107. Steinke, J. W., Bradley, D., Arango, P., Crouse, C. D., Frierson, H., Kountakis, S. E., Kraft, M., Borish, L. (2003) Cysteinyl leukotriene expression in chronic hyperplastic sinusitis-nasal polyposis: importance to eosinophilia and asthma. J. Allergy Clin. Immunol. 111, 342–349.
108. Doherty, T. A., Scott, D., Walford, H. H., Khorram, N., Lund, S., Baum, R., Chang, J., Rosenthal, P., Beppu, A., Miller, M., Broide, D. H. (2014) Allergen challenge in allergic rhinitis rapidly induces increased peripheral blood type 2 innate lymphoid cells that express CD84. J. Allergy Clin. Immunol. 133, 1203–1205.
109. Lao-Araya, M., Steveling, E., Scadding, G. W., Durham, S. R., Shamji, M. H. (2014) Seasonal increases in peripheral innate lymphoid type 2 cells are inhibited by subcutaneous grass pollen immunotherapy. J. Allergy Clin. Immunol. pii: S0091-6749(14)01028-8 [Epub ahead of print].
110. Li, M., Hener, P., Zhang, Z., Ganti, K. P., Metzger, D., Chambon, P. (2009) Induction of thymic stromal lymphopoietin expression in keratinocytes is necessary for generating an atopic dermatitis upon application of the active vitamin D3 analogue MC903 on mouse skin. J. Invest. Dermatol. 129, 498–502.
111. Imai, Y., Yasuda, K., Sakaguchi, Y., Haneda, T., Mizutani, H., Yoshimoto, T., Nakanishi, K., Yamanishi, K. (2013) Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. Proc. Natl. Acad. Sci. USA 110, 13921–13926.
112. Soumelis, V., Reche, P. A., Kanzler, H., Yuan, W., Edward, G., Homey, B., Gilliet, M., Ho, S., Antonenko, S., Lauerma, A., Smith, K., Gorman, D., Zurawski, S., Abrams, J., Menon, S., McClanahan, T., de Waal-Malefyt Rd R., Bazan, F., Kastelein, R. A., Liu, Y. J. (2002) Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat. Immunol. 3, 673–680.
113. Savinko, T., Matikainen, S., Saarialho-Kere, U., Lehto, M., Wang, G., Lehtimäki, S., Karisola, P., Reunala, T., Wolff, H., Lauerma, A., Alenius, H. (2012) IL-33 and ST2 in atopic dermatitis: expression profiles and modulation by triggering factors. J. Invest. Dermatol. 132, 1392–1400.