Collaborative interactions between type 2 innate lymphoid cells and antigen-specific CD4+ Th2 cells exacerbate murine allergic airway diseases with prominent eosinophilia

Journal of Immunology

Volumn 194, Issue 8, 2015, Pages 3583-3593

  Liu, Bo ^a   Lee, Jee Boong ^a   Chen, Chun Yu ^b   Hershey, Gurjit K Khurana ^a   Wang, Yui Hsi ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 13; INTERLEUKIN 25; INTERLEUKIN 33; OVALBUMIN; D17WSU104E PROTEIN, MOUSE; IL33 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; STAT6 PROTEIN; STAT6 PROTEIN, MOUSE;

ALLERGENICITY; ALLERGIC AIRWAY INFLAMMATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD4+ TH17 CELL; CD4+ TH2 CELL; CELL CULTURE; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; EOSINOPHIL; EOSINOPHILIA; GOBLET CELL; IMMUNOGLOBULIN BLOOD LEVEL; INNATE IMMUNITY; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH17 CELL; TH2 CELL; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; CELL COMMUNICATION; CHEMICALLY INDUCED; GENETICS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; LOEFFLER PNEUMONIA; PATHOLOGY;

ANIMALS; ASTHMA; CELL COMMUNICATION; IMMUNITY, INNATE; INFLAMMATION; INTERLEUKIN-33; INTERLEUKINS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OVALBUMIN; PULMONARY EOSINOPHILIA; STAT6 TRANSCRIPTION FACTOR; TH17 CELLS; TH2 CELLS;

EID: 84927600817     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400951     Document Type: Article

References (63)

1. McDonald, V. M., and P. G. Gibson. 2012. Exacerbations of severe asthma. Clin. Exp. Allergy. 42:670-677.
2. Galli, S. J., M. Tsai, and A. M. Piliponsky. 2008. The development of allergic inflammation. Nature 454:445-454.
3. Langley, S. J., S. Goldthorpe, M. Craven, J. Morris, A. Woodcock, and A. Custovic. 2003. Exposure and sensitization to indoor allergens: association with lung function, bronchial reactivity, and exhaled nitric oxide measures in asthma. J. Allergy Clin. Immunol. 112:362-368.
4. 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.
5. Mojtabavi, N., G. Dekan, G. Stingl, and M. M. Epstein. 2002. Long-lived Th2 memory in experimental allergic asthma. J. Immunol. 169:4788-4796.
6. Epstein, M. M. 2006. Targeting memory Th2 cells for the treatment of allergic asthma. Pharmacol. Ther. 109:107-136.
7. Wang, Y. H., T. Ito, Y. H. Wang, B. Homey, N. Watanabe, R. Martin, C. J. Barnes, B. W. McIntyre, M. Gilliet, R. Kumar, et al. 2006. Maintenance and polarization of human TH2 central memory T cells by thymic stromal lymphopoietin-activated dendritic cells. Immunity 24:827-838.
8. Wenzel, S. E., L. B. Schwartz, E. L. Langmack, J. L. Halliday, J. B. Trudeau, R. L. Gibbs, and H. W. Chu. 1999. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am. J. Respir. Crit. Care Med. 160:1001-1008.
9. Woodruff, P. G., B. Modrek, D. F. Choy, G. Jia, A. R. Abbas, A. Ellwanger, L. L. Koth, J. R. Arron, and J. V. Fahy. 2009. T-helper type 2-driven inflammation defines major subphenotypes of asthma. Am. J. Respir. Crit. Care Med. 180:388-395.
10. Wang, Y. H., and M. Wills-Karp. 2011. The potential role of interleukin-17 in severe asthma. Curr. Allergy Asthma Rep. 11:388-394.
11. Cosmi, L., F. Liotta, E. Maggi, S. Romagnani, and F. Annunziato. 2011. Th17 cells: new players in asthma pathogenesis. Allergy 66:989-998.
12. H17 cells in asthma and COPD. Annu. Rev. Physiol. 72:495-516.
13. 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.
14. Barczyk, A., W. Pierzchala, and E. Sozañska. 2003. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir. Med. 97:726-733.
15. Wang, Y. H., K. S. Voo, B. Liu, C. Y. Chen, B. Uygungil, W. Spoede, J. A. Bernstein, D. P. Huston, and Y. J. Liu. 2010. A novel subset of CD4 (+) T (H) 2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J. Exp. Med. 207:2479-2491.
16. Lajoie, S., I. P. Lewkowich, Y. Suzuki, J. R. Clark, A. A. Sproles, K. Dienger, A. L. Budelsky, and M. Wills-Karp. 2010. Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat. Immunol. 11:928-935.
17. H17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 178:1023-1032.
18. 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.
19. 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.
20. 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, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464:1367-1370.
21. 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. USA 107:11489-11494.
22. Saenz, S. A., M. C. Siracusa, J. G. Perrigoue, S. P. Spencer, J. F. Urban, Jr., J. E. Tocker, A. L. Budelsky, M. A. Kleinschek, R. A. Kastelein, T. Kambayashi, et al. 2010. IL25 elicits a multipotent progenitor cell population that promotes T (H) 2 cytokine responses. Nature 464:1362-1366.
23. 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, et al. 2012. Transcription factor RORa is critical for nuocyte development. Nat. Immunol. 13:229-236.
24. 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.
25. 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.
26. 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.
27. 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.
28. Kamijo, S., H. Takeda, T. Tokura, M. Suzuki, K. Inui, M. Hara, H. Matsuda, A. Matsuda, K. Oboki, T. Ohno, et al. 2013. IL-33-mediated innate response and adaptive immune cells contribute to maximum responses of protease allergeninduced allergic airway inflammation. J. Immunol. 190:4489-4499.
29. Mintz-Cole, R. A., A. M. Gibson, S. A. Bass, A. L. Budelsky, T. Reponen, and G. K. Hershey. 2012. Dectin-1 and IL-17A suppress murine asthma induced by Aspergillus versicolor but not Cladosporium cladosporioides due to differences in b-glucan surface exposure. J. Immunol. 189:3609-3617.
30. Swaidani, S., K. Bulek, Z. Kang, C. Liu, Y. Lu, W. Yin, M. Aronica, and X. Li. 2009. The critical role of epithelial-derived Act1 in IL-17- and IL-25-mediated pulmonary inflammation. J. Immunol. 182:1631-1640.
31. 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, et al. 2011. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12:1045-1054.
32. Kheradmand, F., A. Kiss, J. Xu, S. H. Lee, P. E. Kolattukudy, and D. B. Corry. 2002. A protease-activated pathway underlying Th cell type 2 activation and allergic lung disease. J. Immunol. 169:5904-5911.
33. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132.
34. Kaplan, M. H., U. Schindler, S. T. Smiley, and M. J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4:313-319.
35. 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.
36. Spits, H., D. Artis, M. Colonna, A. Diefenbach, J. P. Di Santo, G. Eberl, S. Koyasu, R. M. Locksley, A. N. McKenzie, R. E. Mebius, et al. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145-149.
37. + Th2 cell responses. J. Immunol. 192:2442-2448.
38. Chanez, P., S. E. Wenzel, G. P. Anderson, J. M. Anto, E. H. Bel, L. P. Boulet, C. E. Brightling, W. W. Busse, M. Castro, B. Dahlen, et al. 2007. Severe asthma in adults: what are the important questions? J. Allergy Clin. Immunol. 119:1337-1348.
39. Holgate, S. T., and R. Polosa. 2006. The mechanisms, diagnosis, and management of severe asthma in adults. Lancet 368:780-793.
40. Bell, M. C., and W. W. Busse. 2013. Severe asthma: an expanding and mounting clinical challenge. J Allergy Clin Immunol Pract 1:110-121, quiz 122.
41. Haldar, P., I. D. Pavord, D. E. Shaw, M. A. Berry, M. Thomas, C. E. Brightling, A. J. Wardlaw, and R. H. Green. 2008. Cluster analysis and clinical asthma phenotypes. Am. J. Respir. Crit. Care Med. 178:218-224.
42. Green, R. H., C. E. Brightling, S. McKenna, B. Hargadon, D. Parker, P. Bradding, A. J. Wardlaw, and I. D. Pavord. 2002. Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet 360:1715-1721.
43. Haldar, P., C. E. Brightling, B. Hargadon, S. Gupta, W. Monteiro, A. Sousa, R. P. Marshall, P. Bradding, R. H. Green, A. J. Wardlaw, and I. D. Pavord. 2009. Mepolizumab and exacerbations of refractory eosinophilic asthma. N. Engl. J. Med. 360:973-984.
44. Miranda, C., A. Busacker, S. Balzar, J. Trudeau, and S. E. Wenzel. 2004. Distinguishing severe asthma phenotypes: role of age at onset and eosinophilic inflammation. J. Allergy Clin. Immunol. 113:101-108.
45. Saglani, S., and C. M. Lloyd. 2014. Eosinophils in the pathogenesis of paediatric severe asthma. Curr. Opin. Allergy Clin. Immunol. 14:143-148.
46. Phipps, S., C. E. Lam, G. E. Kaiko, S. Y. Foo, A. Collison, J. Mattes, J. Barry, S. Davidson, K. Oreo, L. Smith, et al. 2009. Toll/IL-1 signaling is critical for house dust mite-specific helper T cell type 2 and type 17 [corrected] responses. Am. J. Respir. Crit. Care Med. 179:883-893.
47. Krishnamoorthy, N., T. B. Oriss, M. Paglia, M. Fei, M. Yarlagadda, B. Vanhaesebroeck, A. Ray, and P. Ray. 2008. Activation of c-Kit in dendritic cells regulates T helper cell differentiation and allergic asthma. Nat. Med. 14:565-573.
48. Fattouh, R., M. A. Pouladi, D. Alvarez, J. R. Johnson, T. D. Walker, S. Goncharova, M. D. Inman, and M. Jordana. 2005. House dust mite facilitates ovalbumin-specific allergic sensitization and airway inflammation. Am. J. Respir. Crit. Care Med. 172:314-321.
49. Scanlon, S. T., S. Y. Thomas, C. M. Ferreira, L. Bai, T. Krausz, P. B. Savage, and A. Bendelac. 2011. Airborne lipid antigens mobilize resident intravascular NKT cells to induce allergic airway inflammation. J. Exp. Med. 208:2113-2124.
50. Liu, Y. J., V. Soumelis, N. Watanabe, T. Ito, Y. H. Wang, Rde. W. Malefyt, M. Omori, B. Zhou, and S. F. Ziegler. 2007. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu. Rev. Immunol. 25:193-219.
51. Fort, M. M., J. Cheung, D. Yen, J. Li, S. M. Zurawski, S. Lo, S. Menon, T. Clifford, B. Hunte, R. Lesley, et al. 2001. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15:985-995.
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, et al. 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.
53. Schmitz, J., A. Owyang, E. Oldham, Y. Song, E. Murphy, T. K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, et al. 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.
54. Nussbaum, J. C., S. J. Van Dyken, J. Von Moltke, L. E. Cheng, A. Mohapatra, A. B. Molofsky, E. E. Thornton, M. F. Krummel, A. Chawla, H. E. Liang, and R. M. Locksley. 2013. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502:245-248.
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.
56. Licona-Limón, P., L. K. Kim, N. W. Palm, and R. A. Flavell. 2013. TH2, allergy and group 2 innate lymphoid cells. Nat. Immunol. 14:536-542.
57. Halim, T. Y., and A. N. McKenzie. 2013. New kids on the block: group 2 innate lymphoid cells and type 2 inflammation in the lung. Chest 144:1681-1686.
58. Gold, M. J., F. Antignano, T. Y. Halim, J. A. Hirota, M. R. Blanchet, C. Zaph, F. Takei, and K. M. McNagny. 2014. Group 2 innate lymphoid cells facilitate sensitization to local, but not systemic, TH2-inducing allergen exposures. J. Allergy Clin. Immunol. 133:1142-1148.
59. Halim, T. Y., C. A. Steer, L. Mathä, M. J. Gold, I. Martinez-Gonzalez, K. M. McNagny, A. N. McKenzie, and F. Takei. 2014. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40:425-435.
60. Oliphant, C. J., Y. Y. Hwang, J. A. Walker, M. Salimi, S. H. Wong, J. M. Brewer, A. Englezakis, J. L. Barlow, E. Hams, S. T. Scanlon, et al. 2014. MHCIImediated dialog between group 2 innate lymphoid cells and CD4 (+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41:283-295.
61. Hammad, H., and B. N. Lambrecht. 2008. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat. Rev. Immunol. 8:193-204.
62. Gasteiger, G., and A. Y. Rudensky. 2014. Interactions between innate and adaptive lymphocytes. Nat. Rev. Immunol. 14:631-639.
63. Wenzel, S. 2012. Severe asthma: from characteristics to phenotypes to endotypes. Clin. Exp. Allergy. 42:650-658.