IMMUNE NETWORK

The Korean Association of Immunobiologists (대한면역학회)
권호 표지
DOI QR코드

DOI QR Code

The Roles of Innate Lymphoid Cells in the Development of Asthma

  • Woo, Yeonduk (Laboratory of Immune Regulation, Department of Biomedical Sciences, Seoul National University College of Medicine) ;
  • Jeong, Dongjin (Laboratory of Immune Regulation, Department of Biomedical Sciences, Seoul National University College of Medicine) ;
  • Chung, Doo Hyun (Laboratory of Immune Regulation, Department of Biomedical Sciences, Seoul National University College of Medicine) ;
  • Kim, Hye Young (Department of Medical Science, Seoul National University College of Medicine and Hospital)
  • Received : 2014.06.16
  • Accepted : 2014.07.30
  • Published : 2014.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

Asthma is a common pulmonary disease with several different forms. The most studied form of asthma is the allergic form, which is mainly related to the function of Th2 cells and their production of cytokines (IL-4, IL-5, and IL-13) in association with allergen sensitization and adaptive immunity. Recently, there have been many advances in understanding non-allergic asthma, which seems to be related to environmental factors such as air pollution, infection, or even obesity. Cells of the innate immune system, including macrophages, neutrophils, and natural killer T cells as well as the newly described innate lymphoid cells, are effective producers of a variety of cytokines and seem to play important roles in the development of non-allergic asthma. In this review, we focus on recent findings regarding innate lymphoid cells and their roles in asthma.

Keywords

References

  1. 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. https://doi.org/10.1056/NEJM199201303260504
  2. Kim, H. Y., R. H. DeKruyff, and D. T. Umetsu. 2010. The many paths to asthma: phenotype shaped by innate and adaptive immunity. Nat. Immunol. 11: 577-584. https://doi.org/10.1038/ni.1892
  3. Corren, J., R. F. Lemanske, N. A. Hanania, P. E. Korenblat, M. V. Parsey, J. R. Arron, J. M. Harris, H. Scheerens, L. C. Wu, Z. Su, S. Mosesova, M. D. Eisner, S. P. Bohen, and J. G. Matthews. 2011. Lebrikizumab Treatment in Adults with Asthma. N. Engl. J. Med. 365: 1038-1098.
  4. Johnston, R. A., M. Zhu, Y. M. Rivera-Sanchez, F. L. Lu, T. A. Theman, L. Flynt, and S. A. Shore. 2007. Allergic airway responses in obese mice. Am. J. Respir. Crit. Care Med. 176: 650-658. https://doi.org/10.1164/rccm.200702-323OC
  5. Pichavant, M., S. Goya, E. H. Meyer, R. A. Johnston, H. Y. Kim, P. Matangkasombut, M. Zhu, Y. Iwakura, P. B. Savage, R. H. Dekruyff, S. A. Shore, and D. T. Umetsu. 2008. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J. Exp. Med. 205: 385-393. https://doi.org/10.1084/jem.20071507
  6. Kim, E. Y., J. T. Battaile, A. C. Patel, Y. You, E. Agapov, M. H. Grayson, L. A. Benoit, D. E. Byers, Y. Alevy, J. Tucker, S. Swanson, R. Tidwell, J. W. Tyner, J. D. Morton, M Castro, D. Polineni, G. A. Patterson, R. A. Schwendener, J. D. Allard, G. Peltz, and M. J. Holtzman. 2008. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14: 633-640. https://doi.org/10.1038/nm1770
  7. Wright, R. J. 2005. Stress and atopic disorders. J. Allergy Clin. Immunol. 116: 1301-1306. https://doi.org/10.1016/j.jaci.2005.09.050
  8. Moro, K., T. Yamada, M. Tanabe, T. Takeuchi, T. Ikawa, H. Kawamoto, J. Furusawa, M. Ohtani, H. Fujii, and S. Koyasu. 2010. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463: 540-544. https://doi.org/10.1038/nature08636
  9. Neill, D. R., S. H. Wong, A. Bellosi, R. J. Flynn, M. Daly, T. K. Langford, C. Bucks, C. M. Kane, P. G. Fallon, R. Pannell, H. E. Jolin, and A. N. McKenzie. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370. https://doi.org/10.1038/nature08900
  10. Buonocore, S., P. P. Ahern, H. H. Uhlig, I. I. Ivanov, D. R. Littman, K. J. Maloy, and F. Powrie. 2010. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464: 1371-1375. https://doi.org/10.1038/nature08949
  11. Chang, Y. J., H. Y. Kim, L. A. Albacker, N. Baumgarth, A. N. McKenzie, D. E. Smith, R. H. Dekruyff, and D. T. Umetsu. 2011. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 12: 631-638. https://doi.org/10.1038/ni.2045
  12. Kim, H. Y., H. J. Lee, Y. J. Chang, M. Pichavant, S. A. Shore, K. A. Fitzgerald, Y. Iwakura, E. Israel, K. Bolger, J. Faul, R. H. DeKruyff, and D. T. Umetsu. 2014. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat. Med. 20: 54-61.
  13. Monticelli, L. A., G. F. Sonnenberg, M. C. Abt, T. Alenghat, C. G. Ziegler, T. A. Doering, J. M. Angelosanto, B. J. Laidlaw, C. Y. Yang, T. Sathaliyawala, M. Kubota, D. Turner, J. M. Diamond, A. W. Goldrath, D. L. Farber, R. G. Collman, E. J. Wherry, and D. Artis. 2011. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12: 1045-1054. https://doi.org/10.1038/ni.2131
  14. Spits, H., and J. P. Di Santo. 2011. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 12: 21-27.
  15. Bernink, J., J. Mjosberg, and H. Spits. 2013. Th1- and Th2-like subsets of innate lymphoid cells. Immunol. Rev. 252: 133-138. https://doi.org/10.1111/imr.12034
  16. Strowig, T., F. Brilot, and C. Munz. 2008. Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J. Immunol. 180: 7785-7791. https://doi.org/10.4049/jimmunol.180.12.7785
  17. Vivier, E., D. H. Raulet, A. Moretta, M. A. Caligiuri, L. Zitvogel, L. L. Lanier, W. M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49. https://doi.org/10.1126/science.1198687
  18. Halim, T. Y., A. MacLaren, M. T. Romanish, M. J. Gold, K. M. McNagny, and F. Takei. 2012. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37: 463-474. https://doi.org/10.1016/j.immuni.2012.06.012
  19. Wong, S. H., J. A. Walker, H. E. Jolin, L. F. Drynan, E. Hams, A. Camelo, J. L. Barlow, D. R. Neill, V. Panova, U. Koch, F. Radtke, C. S. Hardman, Y. Y. Hwang, P. G. Fallon, and A. N. McKenzie. 2012. Transcription factor RORalpha is critical for nuocyte development. Nat. Immunol. 13: 229-236. https://doi.org/10.1038/ni.2208
  20. Hoyler, T., C. S. Klose, A. Souabni, A. Turqueti-Neves, D. Pfeifer, E. L. Rawlins, D. Voehringer, M. Busslinger, and A. Diefenbach. 2012. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37: 634-648. https://doi.org/10.1016/j.immuni.2012.06.020
  21. Sonnenberg, G. F., L. A. Monticelli, M. M. Elloso, L. A. Fouser, and D. Artis. 2011. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 34: 122-134. https://doi.org/10.1016/j.immuni.2010.12.009
  22. Coccia, M., O. J. Harrison, C. Schiering, M. J. Asquith, B. Becher, F. Powrie, and K. J. Maloy. 2012. IL-1beta mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J. Exp. Med. 209: 1595-1609. https://doi.org/10.1084/jem.20111453
  23. Kim, H. Y., H. J. Lee, Y.-J. Chang, M. Pichavant, S. A. Shore, K. A. Fitzgerald, Y. Iwakura, E. Israel, K. Bolger, J. Faul, R. H. DeKruyff, and D. T. Umetsu. 2013. IL-17 producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nature Med. doi:10.1038/nm.3423
  24. Villanova, F., B. Flutter, I. Tosi, K. Grys, H. Sreeneebus, G. K. Perera, A. Chapman, C. H. Smith, P. Di Meglio, and F. O. Nestle. 2014. Characterization of innate lymphoid cells in human skin and blood demonstrates increase of $NKp44^+$ ILC3 in psoriasis. J. Invest. Dermatol. 134: 984-991. https://doi.org/10.1038/jid.2013.477
  25. Teunissen, M. B., J. M. Munneke, J. H. Bernink, P. I. Spuls, P. C. Res, A. Te Velde, S. Cheuk, M. W. Brouwer, S. P. Menting, L. Eidsmo, H. Spits, M. D. Hazenberg, and J. Mjosberg. 2014. Composition of Innate Lymphoid Cell Subsets in the Human Skin: Enrichment of NCR ILC3 in Lesional Skin and Blood of Psoriasis Patients. J. Invest. Dermatol. doi: 10.1038/jid.2014.146
  26. Tumanov, A. V., E. P. Koroleva, X. Guo, Y. Wang, A. Kruglov, S. Nedospasov, and Y. X. Fu. 2011. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe 10: 44-53. https://doi.org/10.1016/j.chom.2011.06.002
  27. Zhou, L. 2012. Striking similarity: GATA-3 regulates ILC2 and Th2 cells. Immunity 37: 589-591. https://doi.org/10.1016/j.immuni.2012.10.002
  28. Satoh-Takayama, N., S. Lesjean-Pottier, P. Vieira, S. Sawa, G. Eberl, C. A. Vosshenrich, and J. P. Di Santo. 2010. IL-7 and IL-15 independently program the differentiation of intestinal CD3-$NKp46^+$ cell subsets from Id2-dependent precursors. J. Exp. Med. 207: 273-280. https://doi.org/10.1084/jem.20092029
  29. Cherrier, M., S. Sawa, and G. Eberl. 2012. Notch, Id2, and $ROR\gamma{t}$ sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 209: 729-740. https://doi.org/10.1084/jem.20111594
  30. Possot, C. 2011. Notch signaling is necessary for adult, but not fetal, development of $ROR\gamma{t}^{+}$ innate lymphoid cells. Nat. Immunol. 12: 949-958. https://doi.org/10.1038/ni.2105
  31. Hughes, T., E. L. Briercheck, A. G. Freud, R. Trotta, S. McClory, S. D. Scoville, K. Keller, Y. Deng, J. Cole, N. Harrison, C. Mao, J. Zhang, D. M. Benson, J. Yu, and M. A. Caligiuri. 2014. The transcription factor AHR prevents the differentiation of a stage 3 innate lymphoid cell subset to natural killer cells. Cell Rep. doi: 10.1016/j.celrep.2014.05.042
  32. Klose, C. S., M. Flach, L. Mohle, L. Rogell, T. Hoyler, K. Ebert, C. Fabiunke, D. Pfeifer, V. Sexl, D. Fonseca-Pereira, R. G. Domingues, H. Veiga-Fernandes, S. J. Arnold, M. Busslinger, I. R. Dunay, Y. Tanriver, and A. Diefenbach. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157: 340-356. https://doi.org/10.1016/j.cell.2014.03.030
  33. Malhotra, A., and A. Shanker. 2011. NK cells: immune cross-talk and therapeutic implications. Immunotherapy 3: 1143-1166. https://doi.org/10.2217/imt.11.102
  34. Li, F., H. Zhu, R. Sun, H. Wei, and Z. Tian. 2012. Natural killer cells are involved in acute lung immune injury caused by respiratory syncytial virus infection. J. Virol. 86: 2251-2258. https://doi.org/10.1128/JVI.06209-11
  35. Jayaraman, A., D. J. Jackson, S. D. Message, R. M. Pearson, J. Aniscenko, G. Caramori, P. Mallia, A. Papi, B. Shamji, M. Edwards, J. Westwick, T. Hansel, L. A. Stanciu, S. L. Johnston, and N. W. Bartlett. 2014. IL-15 complexes induce NK- and T-cell responses independent of type I IFN signaling during rhinovirus infection. Mucosal Immunol. doi: 10.1038/mi.2014.2.
  36. Korsgren, M., C. G. Persson, F. Sundler, T. Bjerke, T. Hansson, B. J. Chambers, S. Hong, L. Van Kaer, H. G. Ljunggren, and O. Korsgren. 1999. Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J. Exp. Med. 189: 553-562. https://doi.org/10.1084/jem.189.3.553
  37. Mathias, C. B., L. A. Guernsey, D. Zammit, C. Brammer, C. A. Wu, R. S. Thrall, and H. L. Aguila. 2014. Pro-inflammatory role of natural killer cells in the development of allergic airway disease. Clin. Exp. Allergy 44: 589-601. https://doi.org/10.1111/cea.12271
  38. Farhadi, N., L. Lambert, C. Triulzi, P. J. Openshaw, N. Guerra, and F. J. Culley. 2014. Natural killer cell NKG2D and granzyme B are critical for allergic pulmonary inflammation. J. Allergy Clin. Immunol. 133: 827-835. https://doi.org/10.1016/j.jaci.2013.09.048
  39. Fort, M. M., J. Cheung, D. Yen, J. Li, S. M. Zurawski, S. Lo, S. Menon, T. Clifford, B. Hunte, R. Lesley, T. Muchamuel, S. D. Hurst, G. Zurawski, M. W. Leach, D. M. Gorman, and D. M. Rennick. 2001. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15: 985-995. https://doi.org/10.1016/S1074-7613(01)00243-6
  40. Fallon, P. G., S. J. Ballantyne, N. E. Mangan, J. L. Barlow, A. Dasvarma, D. R. Hewett, A. McIlgorm, H. E. Jolin, and A. N. McKenzie. 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. https://doi.org/10.1084/jem.20051615
  41. Allakhverdi, Z., M. R. Comeau, D. E. Smith, D. Toy, L. M. Endam, M. Desrosiers, Y. J. Liu, K. J. Howie, J. A. Denburg, G. M. Gauvreau, and G. Delespesse. 2009. $CD34^+$ hemopoietic progenitor cells are potent effectors of allergic inflammation. J. Allergy Clin. Immunol. 123: 472-478. https://doi.org/10.1016/j.jaci.2008.10.022
  42. Saenz, S. A., M. C. Siracusa, J. G. Perrigoue, S. P. Spencer, J. F. Jr. Urban, J. E. Tocker, A. L. Budelsky, M. A. Kleinschek, R. A. Kastelein, T. Kambayashi, A. Bhandoola, and D. Artis. 2010. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464: 1362-1366. https://doi.org/10.1038/nature08901
  43. Spits, H., and T. Cupedo. 2012. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 30: 647-675. https://doi.org/10.1146/annurev-immunol-020711-075053
  44. Price, A. E., H. E. Liang, B. M. Sullivan, R. L. Reinhardt, C. J. Eisley, D. J. Erle, and R. M. Locksley. 2010. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. U. S. A. 107: 11489-11494. https://doi.org/10.1073/pnas.1003988107
  45. Hong, J. Y., J. K. Bentley, Y. Chung, J. Lei, J. M. Steenrod, Q. Chen, U. S. Sajjan, and M. B. Hershenson. 2014. Neonatal rhinovirus induces mucous metaplasia and airways hyperresponsiveness through IL-25 and type 2 innate lymphoid cells. J. Allergy Clin. Immunol. 134(2): 429-439. https://doi.org/10.1016/j.jaci.2014.04.020
  46. Blanken, M. O., M. M. Rovers, J. M. Molenaar, P. L. Winkler-Seinstra, A. Meijer, J. L. Kimpen, L. Bont, and Dutch RSV Neonatal Network. 2013. Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. N. Engl. J. Med. 368: 1791-1799. https://doi.org/10.1056/NEJMoa1211917
  47. Monticelli, L. A., G. F. Sonnenberg, M. C. Abt, T. Alenghat, C. G. Ziegler, T. A. Doering, J. M. Angelosanto, B. J. Laidlaw, C. Y. Yang, T. Sathaliyawala, M. Kubota, D. Turner, J. M. Diamond, A. W. Goldrath, D. L. Farber, R. G. Collman, E. J. Wherry, and D. Artis. 2011. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. doi: 10.1031/ni.2131.
  48. Kearley, J., K. F. Buckland, S. A. Mathie, and C. M. Lloyd. 2009. Resolution of allergic inflammation and airway hyperreactivity is dependent upon disruption of the T1/ST2-IL-33 pathway. Am. J. Respir. Crit. Care Med. 179: 772-781. https://doi.org/10.1164/rccm.200805-666OC
  49. Barlow, J. L., A. Bellosi, C. S. Hardman, L. F. Drynan, S. H. Wong, J. P. Cruickshank, and A. N. McKenzie. 2012. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J. Allergy Clin. Immunol. 129: 191-198. https://doi.org/10.1016/j.jaci.2011.09.041
  50. 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. https://doi.org/10.4049/jimmunol.1102832
  51. Schmitz, J., A. Owyang, E. Oldham, Y. Song, E. Murphy, T. K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, D. M. Gorman, J. F. Bazan, and R. A. Kastelein. 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. https://doi.org/10.1016/j.immuni.2005.09.015
  52. Hurst, S. D., T. Muchamuel, D. M. Gorman, J. M. Gilbert, T. Clifford, S. Kwan, S. Menon, B. Seymour, C. Jackson, T. T. Kung, J. K. Brieland, S. M. Zurawski, R. W. Chapman, G. Zurawski, and R. L. Coffman. 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. https://doi.org/10.4049/jimmunol.169.1.443
  53. Klein Wolterink, R. G., A. Kleinjan, M. van Nimwegen, I. Bergen, M. de Bruijn, Y. Levani, and R. W. Hendriks. 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. https://doi.org/10.1002/eji.201142018
  54. Halim, T. Y., R. H. Krauss, A. C. Sun, and F. Takei. 2012. Lung natural helper cells are a critical source of th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36: 451-463. https://doi.org/10.1016/j.immuni.2011.12.020
  55. Wilhelm, C., K. Hirota, B. Stieglitz, J. van Snick, M. Tolaini, K. Lahl, T. Sparwasser, H. Helmby, and B. Stockinger. 2011. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nat. Immunol. 12: 1071-1077. https://doi.org/10.1038/ni.2133
  56. Kurebayashi, S., E. Ueda, M. Sakaue, D. D. Patel, A. Medvedev, F. Zhang, and A. M. Jetten. 2000. Retinoid-related orphan receptor gamma $(ROR\gamma)$ is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc. Natl. Acad. Sci. U. S. A. 97: 10132-10137. https://doi.org/10.1073/pnas.97.18.10132
  57. Eberl, G., S. Marmon, M. J. Sunshine, P. D. Rennert, Y. Choi, and D. R. Littman. 2004. An essential function for the nuclear receptor $ROR\gamma{t}$ in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5: 64-73. https://doi.org/10.1038/ni1022
  58. Mebius, R. E., P. Rennert, and I. L. Weissman. 1997. Developing lymph nodes collect $CD4^+$$CD3^-$ $LTbeta^+$ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7: 493-504. https://doi.org/10.1016/S1074-7613(00)80371-4
  59. Finke, D. 2005. Fate and function of lymphoid tissue inducer cells. Curr. Opin. Immunol. 17: 144-150. https://doi.org/10.1016/j.coi.2005.01.006
  60. Yoshida, H., K. Honda, R. Shinkura, S. Adachi, S. Nishikawa, K. Maki, K. Ikuta, and S. I. Nishikawa. 1999. IL-7 receptor $alpha^+$ CD3(-) cells in the embryonic intestine induces the organizing center of Peyer's patches. Int. Immunol. 11: 643-655. https://doi.org/10.1093/intimm/11.5.643
  61. Sawa, S., M. Lochner, N. Satoh-Takayama, S. Dulauroy, M. Berard, M. Kleinschek, D. Cua, J. P. Di Santo, and G. Eberl. 2011. $ROR\gamma{t}^+$ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 12: 320-326.
  62. Cupedo, T., N. K. Crellin, N. Papazian, E. J. Rombouts, K. Weijer, J. L. Grogan, W. E. Fibbe, J. J. Cornelissen, and H. Spits. 2009. Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to $RORC^+$ $CD127^+$ natural killer-like cells. Nat. Immunol. 10: 66-74. https://doi.org/10.1038/ni.1668
  63. Geremia, A., C. V. Arancibia-Carcamo, M. P. Fleming, N. Rust, B. Singh, N. J. Mortensen, S. P. Travis, and F. Powrie. 2011. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 208: 1127-1133. https://doi.org/10.1084/jem.20101712
  64. Crellin, N. K., S. Trifari, C. D. Kaplan, N. Satoh-Takayama, J. P. Di Santo, and H. Spits. 2010. Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 33: 752-764. https://doi.org/10.1016/j.immuni.2010.10.012
  65. Sanos, S. L., V. L. Bui, A. Mortha, K. Oberle, C. Heners, C. Johner, and A. Diefenbach. 2009. $ROR\gamma{t}$ and commensal microflora are required for the differentiation of mucosal interleukin 22-producing $NKp46^+$ cells. Nat. Immunol. 10: 83-91.
  66. Satoh-Takayama, N., C. A. Vosshenrich, S. Lesjean-Pottier, S. Sawa, M. Lochner, F. Rattis, J. J. Mention, K. Thiam, N. Cerf-Bensussan, O. Mandelboim, G. Eberl, and J. P. Di Santo. 2008. Microbial flora drives interleukin 22 production in intestinal $NKp46^+$ cells that provide innate mucosal immune defense. Immunity 29: 958-970. https://doi.org/10.1016/j.immuni.2008.11.001
  67. 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. https://doi.org/10.1084/jem.20061401
  68. Kudo, M., A. C. Melton, C. Chen, M. B. Engler, K. E. Huang, X. Ren, Y. Wang, X. Bernstein, J. T. Li, K. Atabai, X. Huang, and D. Sheppard. 2012. IL-17A produced by alphabeta T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat. Med. 18: 547-554. https://doi.org/10.1038/nm.2684
  69. 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. https://doi.org/10.4049/jimmunol.181.6.4089
  70. Osborn, O., and J. M. Olefsky. 2012. The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 18: 363-374. https://doi.org/10.1038/nm.2627
  71. Holguin, F., E. R. Bleecker, W. W. Busse, W. J. Calhoun, M. Castro, S. C. Erzurum, A. M. Fitzpatrick, B. Gaston, E. Israel, N. N. Jarjour, W. C. Moore, S. P. Peters, M. Yonas, W. G. Teague, and S. E. Wenzel. 2011. Obesity and asthma: an association modified by age of asthma onset. J Allergy Clin. Immunol. 127: 1486-1493. https://doi.org/10.1016/j.jaci.2011.03.036
  72. Camargo, C. A., Jr., S. T. Weiss, S. Zhang, W. C. Willett, and F. E. Speizer. 1999. Prospective study of body mass index, weight change, and risk of adult-onset asthma in women. Arch. Intern. Med. 159: 2582-2588. https://doi.org/10.1001/archinte.159.21.2582
  73. Fuchs, A., W. Vermi, J. S. Lee, S. Lonardi, S. Gilfillan, R. D. Newberry, M. Cella, and M. Colonna. 2013. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12-and IL-15-responsive IFN-gamma-producing cells. Immunity 38: 769-781. https://doi.org/10.1016/j.immuni.2013.02.010
  74. Bernink, J. H., C. P. Peters, M. Munneke, A. A. te Velde, S. L. Meijer, K. Weijer, H. S. Hreggvidsdottir, S. E. Heinsbroek, N. Legrand, C. J. Buskens, W. A. Bemelman, J. M. Mjosberg, and H. Spits. 2013. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14: 221-229. https://doi.org/10.1038/ni.2534
  75. Prefontaine, D., S. Lajoie-Kadoch, S. Foley, S. Audusseau, R. Olivenstein, A. J. Halayko, C. Lemiere, J. G. Martin, and Q. Hamid. 2009. Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J. Immunol. 183: 5094-5103. https://doi.org/10.4049/jimmunol.0802387
  76. Mjosberg, J. M., S. Trifari, N. K. Crellin, C. P. Peters, C. M. van Drunen, B. Piet, W. J. Fokkens, T. Cupedo, and H. Spits. 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. https://doi.org/10.1038/ni.2104
  77. Kwon, B. I., S. Hong, K. Shin, E. H. Choi, J. J. Hwang, and S. H. Lee. 2013. Innate type 2 immunity is associated with eosinophilic pleural effusion in primary spontaneous pneumothorax. Am. J. Respir. Crit. Care Med. 188: 577-585. https://doi.org/10.1164/rccm.201302-0295OC
  78. Kim, B. S., M. C. Siracusa, S. A. Saenz, M. Noti, L. A. Monticelli, G. F. Sonnenberg, M. R. Hepworth, A. S. van Voorhees, M. R. Comeau, and D. Artis D. 2013. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci. Transl. Med. 5: 170ra16.
  79. Nagarkar, D. R., J. A. Poposki, B. K. Tan, M. R. Comeau, A. T. Peters, K. E. Hulse, L. A. Suh, J. Norton, K. E. Harris, L. C. Grammer, R. K. Chandra, D. B. Conley, R. C. Kern, R. P. Schleimer, and A. Kato. 2013. Thymic stromal lymphopoietin activity is increased in nasal polyps of patients with chronic rhinosinusitis. J. Allergy Clin. Immunol. 132: 593-600. https://doi.org/10.1016/j.jaci.2013.04.005
  80. Kamekura, R., T. Kojima, K. Takano, M. Go, N. Sawada, and T. Himi. 2012. The role of IL-33 and its receptor ST2 in human nasal epithelium with allergic rhinitis. Clin. Exp. Allergy 42: 218-228. https://doi.org/10.1111/j.1365-2222.2011.03867.x
  81. Dyring-Andersen, B., C. Geisler, C. Agerbeck, J. P. Lauritsen, S. D. Gudjonsdottir, L. Skov, and C. M. Bonefeld. 2014. Increased number and frequency of group 3 innate lymphoid cells in nonlesional psoriatic skin. Br. J. Dermatol. 170: 609-616. https://doi.org/10.1111/bjd.12658

Cited by

  1. Allergic Inflammation in Aspergillus fumigatus-Induced Fungal Asthma vol.15, pp.10, 2014, https://doi.org/10.1007/s11882-015-0561-x
  2. MAPK/AP-1-Targeted Anti-Inflammatory Activities of Xanthium strumarium vol.44, pp.6, 2014, https://doi.org/10.1142/s0192415x16500622
  3. Natural Killer Receptor 1 Dampens the Development of Allergic Eosinophilic Airway Inflammation vol.11, pp.8, 2014, https://doi.org/10.1371/journal.pone.0160779
  4. Cutaneous exposure to clinically-relevant pigeon pea (Cajanus cajan) proteins promote TH2-dependent sensitization and IgE-mediated anaphylaxis in Balb/c mice vol.13, pp.6, 2014, https://doi.org/10.1080/1547691x.2016.1205159
  5. Dendritic Cell-Mediated Th2 Immunity and Immune Disorders vol.20, pp.9, 2014, https://doi.org/10.3390/ijms20092159
  6. Mediators of the homeostasis and effector functions of memory Th2 cells as novel drug targets in intractable chronic allergic diseases vol.42, pp.9, 2014, https://doi.org/10.1007/s12272-019-01159-4
  7. IL-17A-Producing Innate Lymphoid Cells Promote Skin Inflammation by Inducing IL-33-Driven Type 2 Immune Responses vol.140, pp.4, 2020, https://doi.org/10.1016/j.jid.2019.08.447
  8. Interactions between NCR+ILC3s and the Microbiome in the Airways Shape Asthma Severity vol.21, pp.4, 2014, https://doi.org/10.4110/in.2021.21.e25