Biologics and the lung: TSLP and other epithelial cell-derived cytokines in asthma

Pharmacology and Therapeutics

Volumn 169, Issue , 2017, Pages 104-112

  Mitchell, Patrick D ^a   O'Byrne, Paul M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Alarmins; Asthma; Epithelial cell derived cytokines; IL 25; IL 33; TSLP

Indexed keywords

ALARMIN; ALLERGEN; INTERLEUKIN 25; INTERLEUKIN 33; THYMIC STROMAL LYMPHOPOIETIN; BIOLOGICAL PRODUCT; CYTOKINE; INTERLEUKIN 17; MONOCLONAL ANTIBODY;

ASTHMA; HUMAN; INHALATION; LUNG ALVEOLUS EPITHELIUM; LUNG FUNCTION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; REVIEW; ANIMAL; EPITHELIUM CELL; IMMUNOLOGY; PATHOPHYSIOLOGY;

ALLERGENS; ANIMALS; ANTIBODIES, MONOCLONAL; ASTHMA; BIOLOGICAL PRODUCTS; CYTOKINES; EPITHELIAL CELLS; HUMANS; INTERLEUKIN-17; INTERLEUKIN-33;

EID: 85003698513     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2016.06.009     Document Type: Review

References (127)

1. Akamatsu, T., Watanabe, N., Kido, M., Saga, K., Tanaka, J., Kuzushima, K., et al. Human TSLP directly enhances expansion of CD8 + T cells. Clin Exp Immunol 154:1 (2008), 98–106.
2. Allakhverdi, Z., Smith, D.E., Comeau, M.R., Delespesse, G., Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol 179:4 (2007), 2051–2054.
3. Andreakos, E., Papadopoulos, N.G., IL-25: The missing link between allergy, viral infection, and asthma?. Sci Transl Med, 6(256), 2014 (256 fs38).
4. Baatjes, A.J., Smith, S.G., Dua, B., Watson, R., Gauvreau, G.M., O'Byrne, P.M., Treatment with anti-OX40L or anti-TSLP does not alter the frequency of T regulatory cells in allergic asthmatics. Allergy 70:11 (2015), 1505–1508.
5. Barlow, J.L., Peel, S., Fox, J., Panova, V., Hardman, C.S., Camelo, A., et al. 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 132:4 (2013), 933–941.
6. Baughman, R.P., Thorpe, J.E., Staneck, J., Rashkin, M., Frame, P.T., Use of the protected specimen brush in patients with endotracheal or tracheostomy tubes. Chest 91:2 (1987), 233–236.
7. Beale, J., Jayaraman, A., Jackson, D.J., Macintyre, J.D., Edwards, M.R., Walton, R.P., et al. Rhinovirus-induced IL-25 in asthma exacerbation drives type 2 immunity and allergic pulmonary inflammation. Sci Transl Med, 6(256), 2014 (256ra134).
8. Beauchamp, N.M., Busick, R.Y., Alexander-Miller, M.A., Functional divergence among CD103 + dendritic cell subpopulations following pulmonary poxvirus infection. J Virol 84:19 (2010), 10191–10199.
9. Bernatchez, E., Gold, M.J., Langlois, A., Lemay, A.M., Brassard, J., Flamand, N., et al. Pulmonary CD103 expression regulates airway inflammation in asthma. Am J Physiol Lung Cell Mol Physiol 308:8 (2015), L816–L826.
10. Bonilla, W.V., Frohlich, A., Senn, K., Kallert, S., Fernandez, M., Johnson, S., et al. The alarmin interleukin-33 drives protective antiviral CD8(+) T cell responses. Science 335:6071 (2012), 984–989.
11. Brandelius, A., Yudina, Y., Calven, J., Bjermer, L., Andersson, M., Persson, C., et al. dsRNA-induced expression of thymic stromal lymphopoietin (TSLP) in asthmatic epithelial cells is inhibited by a small airway relaxant. Pulm Pharmacol Ther 24:1 (2011), 59–66.
12. Byers, D.E., Alexander-Brett, J., Patel, A.C., Agapov, E., Dang-Vu, G., Jin, X., et al. Long-term IL-33-producing epithelial progenitor cells in chronic obstructive lung disease. J Clin Invest 123:9 (2013), 3967–3982.
13. Carayol, N., Campbell, A., Vachier, I., Mainprice, B., Bousquet, J., Godard, P., et al. Modulation of cadherin and catenins expression by tumor necrosis factor-alpha and dexamethasone in human bronchial epithelial cells. Am J Respir Cell Mol Biol 26:3 (2002), 341–347.
14. Carriere, V., Roussel, L., Ortega, N., Lacorre, D.A., Americh, L., Aguilar, L., et al. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc Natl Acad Sci U S A 104:1 (2007), 282–287.
15. Chang, Y.J., Kim, H.Y., Albacker, L.A., Baumgarth, N., McKenzie, A.N., Smith, D.E., et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 12:7 (2011), 631–638.
16. Charlson, E.S., Bittinger, K., Haas, A.R., Fitzgerald, A.S., Frank, I., Yadav, A., et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 184:8 (2011), 957–963.
17. Cheng, D., Xue, Z., Yi, L., Shi, H., Zhang, K., Huo, X., et al. Epithelial interleukin-25 is a key mediator in Th2-high, corticosteroid-responsive asthma. Am J Respir Crit Care Med 190:6 (2014), 639–648.
18. Cherry, W.B., Yoon, J., Bartemes, K.R., Iijima, K., Kita, H., A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol 121:6 (2008), 1484–1490.
19. Chow, J.Y., Wong, C.K., Cheung, P.F., Lam, C.W., Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: Implications for allergic inflammation. Cell Mol Immunol 7:1 (2010), 26–34.
20. Cohen, E.S., Scott, I.C., Majithiya, J.B., Rapley, L., Kemp, B.P., England, E., et al. Oxidation of the alarmin IL-33 regulates ST2-dependent inflammation. Nat Commun, 6, 2015, 8327.
21. Cook, E.B., Stahl, J.L., Schwantes, E.A., Fox, K.E., Mathur, S.K., IL-3 and TNFalpha increase thymic stromal lymphopoietin receptor (TSLPR) expression on eosinophils and enhance TSLP-stimulated degranulation. Clin Mol Allergy, 10(1), 2012, 8.
22. Corrigan, C.J., Wang, W., Meng, Q., Fang, C., Eid, G., Caballero, M.R., et al. Allergen-induced expression of IL-25 and IL-25 receptor in atopic asthmatic airways and late-phase cutaneous responses. J Allergy Clin Immunol 128:1 (2011), 116–124.
23. Corrigan, C.J., Wang, W., Meng, Q., Fang, C., Wu, H., Reay, V., et al. T-helper cell type 2 (Th2) memory T cell-potentiating cytokine IL-25 has the potential to promote angiogenesis in asthma. Proc Natl Acad Sci U S A 108:4 (2011), 1579–1584.
24. Davies, D.E., Epithelial barrier function and immunity in asthma. Ann Am Thorac Soc 11:Suppl. 5 (2014), S244–S251.
25. Edelson, B.T., Kc, W., Juang, R., Kohyama, M., Benoit, L.A., Klekotka, P.A., et al. Peripheral CD103 + dendritic cells form a unified subset developmentally related to CD8alpha + conventional dendritic cells. J Exp Med 207:4 (2010), 823–836.
26. Erb-Downward, J.R., Thompson, D.L., Han, M.K., Freeman, C.M., McCloskey, L., Schmidt, L.A., et al. Analysis of the lung microbiome in the “healthy” smoker and in COPD. PLoS One, 6(2), 2011, e16384.
27. Fux, M., Pecaric-Petkovic, T., Odermatt, A., Hausmann, O.V., Lorentz, A., Bischoff, S.C., et al. IL-33 is a mediator rather than a trigger of the acute allergic response in humans. Allergy 69:2 (2014), 216–222.
28. Gauvreau, G.M., El-Gammal, A.I., O'Byrne, P.M., Allergen-induced airway responses. Eur Respir J 46:3 (2015), 819–831.
29. Gauvreau, G.M., Lee, J.M., Watson, R.M., Irani, A.M., Schwartz, L.B., O'Byrne, P.M., Increased numbers of both airway basophils and mast cells in sputum after allergen inhalation challenge of atopic asthmatics. Am J Respir Crit Care Med 161:5 (2000), 1473–1478.
30. Gauvreau, G.M., O'Byrne, P.M., Boulet, L.P., Wang, Y., Cockcroft, D., Bigler, J., et al. Effects of an anti-TSLP antibody on allergen-induced asthmatic responses. N Engl J Med 370:22 (2014), 2102–2110.
31. Gavala, M.L., Bashir, H., Gern, J.E., Virus/allergen interactions in asthma. Curr Allergy Asthma Rep 13:3 (2013), 298–307.
32. Gibson, P.G., Simpson, J.L., Saltos, N., Heterogeneity of airway inflammation in persistent asthma: Evidence of neutrophilic inflammation and increased sputum interleukin-8. Chest 119:5 (2001), 1329–1336.
33. 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 36:3 (2012), 451–463.
34. Hammad, H., Chieppa, M., Perros, F., Willart, M.A., Germain, R.N., Lambrecht, B.N., House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 15:4 (2009), 410–416.
35. Hams, E., Armstrong, M.E., Barlow, J.L., Saunders, S.P., Schwartz, C., Cooke, G., et al. IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci U S A 111:1 (2014), 367–372.
36. Harada, M., Hirota, T., Jodo, A.I., Doi, S., Kameda, M., Fujita, K., et al. Functional analysis of the thymic stromal lymphopoietin variants in human bronchial epithelial cells. Am J Respir Cell Mol Biol 40:3 (2009), 368–374.
37. Harada, M., Hirota, T., Jodo, A.I., Hitomi, Y., Sakashita, M., Tsunoda, T., et al. Thymic stromal lymphopoietin gene promoter polymorphisms are associated with susceptibility to bronchial asthma. Am J Respir Cell Mol Biol 44:6 (2011), 787–793.
38. Hardman, C.S., Panova, V., McKenzie, A.N., IL-33 citrine reporter mice reveal the temporal and spatial expression of IL-33 during allergic lung inflammation. Eur J Immunol 43:2 (2013), 488–498.
39. Heijink, I.H., Brandenburg, S.M., Noordhoek, J.A., Postma, D.S., Slebos, D.J., van Oosterhout, A.J., Characterisation of cell adhesion in airway epithelial cell types using electric cell-substrate impedance sensing. Eur Respir J 35:4 (2010), 894–903.
40. Hilty, M., Burke, C., Pedro, H., Cardenas, P., Bush, A., Bossley, C., et al. Disordered microbial communities in asthmatic airways. PLoS One, 5(1), 2010, e8578.
41. Ho, J.E., Chen, W.Y., Chen, M.H., Larson, M.G., McCabe, E.L., Cheng, S., et al. Common genetic variation at the IL1RL1 locus regulates IL-33/ST2 signaling. J Clin Invest 123:10 (2013), 4208–4218.
42. Holt, P.G., Schon-Hegrad, M.A., Oliver, J., Holt, B.J., McMenamin, P.G., A contiguous network of dendritic antigen-presenting cells within the respiratory epithelium. Int Arch Allergy Appl Immunol 91:2 (1990), 155–159.
43. Hsu, C.L., Bryce, P.J., Inducible IL-33 expression by mast cells is regulated by a calcium-dependent pathway. J Immunol 189:7 (2012), 3421–3429.
44. Humphreys, N.E., Xu, D., Hepworth, M.R., Liew, F.Y., Grencis, R.K., IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J Immunol 180:4 (2008), 2443–2449.
45. Hurst, S.D., Muchamuel, T., Gorman, D.M., Gilbert, J.M., Clifford, T., Kwan, S., et al. New IL-17 family members promote Th1 or Th2 responses in the lung: In vivo function of the novel cytokine IL-25. J Immunol 169:1 (2002), 443–453.
46. Iseki, M., Omori-Miyake, M., Xu, W., Sun, X., Takaki, S., Rawlings, D.J., et al. Thymic stromal lymphopoietin (TSLP)-induced polyclonal B-cell activation and autoimmunity are mediated by CD4 + T cells and IL-4. Int Immunol 24:3 (2012), 183–195.
47. Ito, T., Wang, Y.H., Duramad, O., Hori, T., Delespesse, G.J., Watanabe, N., et al. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med 202:9 (2005), 1213–1223.
48. Jackson, D.J., Makrinioti, H., Rana, B.M., Shamji, B.W., Trujillo-Torralbo, M.B., Footitt, J., et al. IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. Am J Respir Crit Care Med 190:12 (2014), 1373–1382.
49. Jiang, A., Bloom, O., Ono, S., Cui, W., Unternaehrer, J., Jiang, S., et al. Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27:4 (2007), 610–624.
50. Johnston, S.L., Natural and experimental rhinovirus infections of the lower respiratory tract. Am J Respir Crit Care Med 152:4 Pt 2 (1995), S46–S52.
51. Jung, J.S., Park, B.L., Cheong, H.S., Bae, J.S., Kim, J.H., Chang, H.S., et al. Association of IL-17RB gene polymorphism with asthma. Chest 135:5 (2009), 1173–1180.
52. Kamijo, S., Takeda, H., Tokura, T., Suzuki, M., Inui, K., Hara, M., et al. IL-33-mediated innate response and adaptive immune cells contribute to maximum responses of protease allergen-induced allergic airway inflammation. J Immunol 190:9 (2013), 4489–4499.
53. Kato, A., Favoreto, S. Jr., Avila, P.C., Schleimer, R.P., TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J Immunol 179:2 (2007), 1080–1087.
54. Kaur, D., Gomez, E., Doe, C., Berair, R., Woodman, L., Saunders, R., et al. IL-33 drives airway hyper-responsiveness through IL-13-mediated mast cell: Airway smooth muscle crosstalk. Allergy 70:5 (2015), 556–567.
55. Kawaguchi, M., Kokubu, F., Fujita, J., Huang, S.K., Hizawa, N., Role of interleukin-17F in asthma. Inflamm Allergy Drug Targets 8:5 (2009), 383–389.
56. Kearley, J., Silver, J.S., Sanden, C., Liu, Z., Berlin, A.A., White, N., et al. Cigarette smoke silences innate lymphoid cell function and facilitates an exacerbated type I interleukin-33-dependent response to infection. Immunity 42:3 (2015), 566–579.
57. Kim, M.R., Manoukian, R., Yeh, R., Silbiger, S.M., Danilenko, D.M., Scully, S., et al. Transgenic overexpression of human IL-17E results in eosinophilia, B-lymphocyte hyperplasia, and altered antibody production. Blood 100:7 (2002), 2330–2340.
58. Kirby, J.G., Hargreave, F.E., Gleich, G.J., O'Byrne, P.M., Bronchoalveolar cell profiles of asthmatic and nonasthmatic subjects. Am Rev Respir Dis 136:2 (1987), 379–383.
59. Kouzaki, H., O'Grady, S.M., Lawrence, C.B., Kita, H., Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J Immunol 183:2 (2009), 1427–1434.
60. Kouzaki, H., Tojima, I., Kita, H., Shimizu, T., Transcription of interleukin-25 and extracellular release of the protein is regulated by allergen proteases in airway epithelial cells. Am J Respir Cell Mol Biol 49:5 (2013), 741–750.
61. Lawrence, T., The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol, 1(6), 2009, a001651.
62. Lee, H.Y., Rhee, C.K., Kang, J.Y., Byun, J.H., Choi, J.Y., Kim, S.J., et al. Blockade of IL-33/ST2 ameliorates airway inflammation in a murine model of allergic asthma. Exp Lung Res 40:2 (2014), 66–76.
63. Lefrancais, E., Roga, S., Gautier, V., Gonzalez-de-Peredo, A., Monsarrat, B., Girard, J.P., et al. IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc Natl Acad Sci U S A 109:5 (2012), 1673–1678.
64. Levin, S.D., Koelling, R.M., Friend, S.L., Isaksen, D.E., Ziegler, S.F., Perlmutter, R.M., et al. Thymic stromal lymphopoietin: A cytokine that promotes the development of IgM + B cells in vitro and signals via a novel mechanism. J Immunol 162:2 (1999), 677–683.
65. Lin, J., Zhao, G.Q., Wang, Q., Xu, Q., Che, C.Y., Hu, L.T., et al. Regulation of interleukin 33/ST2 signaling of human corneal epithelium in allergic diseases. Int J Ophthalmol 6:1 (2013), 23–29.
66. Liu, Y.J., Thymic stromal lymphopoietin: Master switch for allergic inflammation. J Exp Med 203:2 (2006), 269–273.
67. Lloyd, C.M., Saglani, S., Epithelial cytokines and pulmonary allergic inflammation. Curr Opin Immunol 34c (2015), 52–58.
68. Martin, M.U., Special aspects of interleukin-33 and the IL-33 receptor complex. Semin Immunol 25:6 (2013), 449–457.
69. Martinez-Gonzalez, I., Steer, C.A., Takei, F., Lung ILC2s link innate and adaptive responses in allergic inflammation. Trends Immunol 36:3 (2015), 189–195.
70. Mattila, P., Joenvaara, S., Renkonen, J., Toppila-Salmi, S., Renkonen, R., Allergy as an epithelial barrier disease. Clin Transl Allergy, 1(1), 2011, 5.
71. Mattoli, S., Marini, M., Fasoli, A., Expression of the potent inflammatory cytokines, GM-CSF, IL6, and IL8, in bronchial epithelial cells of asthmatic patients. Chest 101:3 Suppl. (1992), 27s–29s.
72. Mease, P.J., Genovese, M.C., Greenwald, M.W., Ritchlin, C.T., Beaulieu, A.D., Deodhar, A., et al. Brodalumab, an anti-IL17RA monoclonal antibody, in psoriatic arthritis. N Engl J Med 370:24 (2014), 2295–2306.
73. Mizutani, N., Nabe, T., Yoshino, S., Interleukin-33 and alveolar macrophages contribute to the mechanisms underlying the exacerbation of IgE-mediated airway inflammation and remodelling in mice. Immunology 139:2 (2013), 205–218.
74. Mjosberg, J.M., Trifari, S., Crellin, N.K., Peters, C.P., van Drunen, C.M., Piet, B., et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol 12:11 (2011), 1055–1062.
75. Moffatt, M.F., Gut, I.G., Demenais, F., Strachan, D.P., Bouzigon, E., Heath, S., et al. A large-scale, consortium-based genomewide association study of asthma. N Engl J Med 363:13 (2010), 1211–1221.
76. 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 12:11 (2011), 1045–1054.
77. Moussion, C., Ortega, N., Girard, J.P., The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'?. PLoS One, 3(10), 2008, e3331.
78. Murray, C.S., Poletti, G., Kebadze, T., Morris, J., Woodcock, A., Johnston, S.L., et al. Study of modifiable risk factors for asthma exacerbations: virus infection and allergen exposure increase the risk of asthma hospital admissions in children. Thorax 61:5 (2006), 376–382.
79. 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 464:7293 (2010), 1367–1370.
80. Nygaard, U., Vestergaard, C., Johansen, C., Deleuran, M., Hvid, M., Measuring serum concentrations of interleukin-33 in atopic dermatitis is associated with potential false positive results. SpringerPlus, 5, 2016, 33.
81. Okayama, Y., Okumura, S., Sagara, H., Yuki, K., Sasaki, T., Watanabe, N., et al. FcepsilonRI-mediated thymic stromal lymphopoietin production by interleukin-4-primed human mast cells. Eur Respir J 34:2 (2009), 425–435.
82. Omori, M., Ziegler, S., Induction of IL-4 expression in CD4(+) T cells by thymic stromal lymphopoietin. J Immunol 178:3 (2007), 1396–1404.
83. Oyoshi, M.K., Larson, R.P., Ziegler, S.F., Geha, R.S., Mechanical injury polarizes skin dendritic cells to elicit a T(H)2 response by inducing cutaneous thymic stromal lymphopoietin expression. J Allergy Clin Immunol 126:5 (2010), 976–984 (84.e1–5).
84. Palmer, G., Gabay, C., Interleukin-33 biology with potential insights into human diseases. Nat Rev Rheumatol 7:6 (2011), 321–329.
85. Palmer, G., Lipsky, B.P., Smithgall, M.D., Meininger, D., Siu, S., Talabot-Ayer, D., et al. The IL-1 receptor accessory protein (AcP) is required for IL-33 signaling and soluble AcP enhances the ability of soluble ST2 to inhibit IL-33. Cytokine 42:3 (2008), 358–364.
86. Papazian, D., Hansen, S., Wurtzen, P.A., Airway responses towards allergens — From the airway epithelium to T cells. Clin Exp Allergy, 2014.
87. Park, J.S., Park, B.L., Kim, M.O., Heo, J.S., Jung, J.S., Bae, D.J., et al. Association of single nucleotide polymorphisms on Interleukin 17 receptor A (IL17RA) gene with aspirin hypersensitivity in asthmatics. Hum Immunol 74:5 (2013), 598–606.
88. Pecaric-Petkovic, T., Didichenko, S.A., Kaempfer, S., Spiegl, N., Dahinden, C.A., Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 113:7 (2009), 1526–1534.
89. Prefontaine, D., Lajoie-Kadoch, S., Foley, S., Audusseau, S., Olivenstein, R., Halayko, A.J., et al. Increased expression of IL-33 in severe asthma: Evidence of expression by airway smooth muscle cells. J Immunol 183:8 (2009), 5094–5103.
90. Prefontaine, D., Nadigel, J., Chouiali, F., Audusseau, S., Semlali, A., Chakir, J., et al. Increased IL-33 expression by epithelial cells in bronchial asthma. J Allergy Clin Immunol 125:3 (2010), 752–754.
91. Probst, H.C., Muth, S., Schild, H., Regulation of the tolerogenic function of steady-state DCs. Eur J Immunol 44:4 (2014), 927–933.
92. Raeiszadeh Jahromi, S., Mahesh, P.A., Jayaraj, B.S., Madhunapantula, S.R., Holla, A.D., Vishweswaraiah, S., et al. Serum levels of IL-10, IL-17F and IL-33 in patients with asthma: A case–control study. J Asthma 51:10 (2014), 1004–1013.
93. Reche, P.A., Soumelis, V., Gorman, D.M., Clifford, T., Liu, M., Travis, M., et al. Human thymic stromal lymphopoietin preferentially stimulates myeloid cells. J Immunol 167:1 (2001), 336–343.
94. Reddel, H.K., Bateman, E.D., Becker, A., Boulet, L.P., Cruz, A.A., Drazen, J.M., et al. A summary of the new GINA strategy: A roadmap to asthma control. Eur Respir J 46:3 (2015), 622–639.
95. Riviere, E., Ly, B., Boudaoud, S., Chavez, H., Nocturne, G., Chanson, P., et al. Pitfalls for detecting interleukin-33 by ELISA in the serum of patients with primary Sjogren syndrome: comparison of different kits. Ann Rheum Dis 75:3 (2016), 633–635.
96. Robinson, D.S., Hamid, Q., Ying, S., Tsicopoulos, A., Barkans, J., Bentley, A.M., et al. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med 326:5 (1992), 298–304.
97. Roggen, E.L., Lindstedt, M., Borrebaeck, C., Verheyen, G.R., Interactions between dendritic cells and epithelial cells in allergic disease. Toxicol Lett 162:1 (2006), 71–82.
98. Salter, B.M., Oliveria, J.P., Nusca, G., Smith, S.G., Watson, R.M., Comeau, M., et al. Thymic stromal lymphopoietin activation of basophils in patients with allergic asthma is IL-3 dependent. J Allergy Clin Immunol, 2015.
99. Savenije, O.E., Mahachie John, J.M., Granell, R., Kerkhof, M., Dijk, F.N., de Jongste, J.C., et al. Association of IL33-IL-1 receptor-like 1 (IL1RL1) pathway polymorphisms with wheezing phenotypes and asthma in childhood. J Allergy Clin Immunol 134:1 (2014), 170–177.
100. Schiering, C., Krausgruber, T., Chomka, A., Frohlich, A., Adelmann, K., Wohlfert, E.A., et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513:7519 (2014), 564–568.
101. Sedhom, M.A., Pichery, M., Murdoch, J.R., Foligne, B., Ortega, N., Normand, S., et al. Neutralisation of the interleukin-33/ST2 pathway ameliorates experimental colitis through enhancement of mucosal healing in mice. Gut 62:12 (2013), 1714–1723.
102. Semlali, A., Jacques, E., Koussih, L., Gounni, A.S., Chakir, J., Thymic stromal lymphopoietin-induced human asthmatic airway epithelial cell proliferation through an IL-13-dependent pathway. J Allergy Clin Immunol 125:4 (2010), 844–850.
103. Shin, H.W., Kim, D.K., Park, M.H., Eun, K.M., Lee, M., So, D., et al. IL-25 as a novel therapeutic target in nasal polyps of patients with chronic rhinosinusitis. J Allergy Clin Immunol, 2015.
104. Simpson, J.L., Scott, R., Boyle, M.J., Gibson, P.G., Inflammatory subtypes in asthma: Assessment and identification using induced sputum. Respirology 11:1 (2006), 54–61.
105. Smith, S.G., Gugilla, A., Mukherjee, M., Merim, K., Irshad, A., Tang, W., et al. Thymic stromal lymphopoietin and IL-33 modulate migration of hematopoietic progenitor cells in patients with allergic asthma. J Allergy Clin Immunol, 2015.
106. Smithgall, M.D., Comeau, M.R., Yoon, B.R., Kaufman, D., Armitage, R., Smith, D.E., 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 20:8 (2008), 1019–1030.
107. Sokol, C.L., Barton, G.M., Farr, A.G., Medzhitov, R., A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat Immunol 9:3 (2008), 310–318.
108. Sont, J.K., Han, J., van Krieken, J.M., Evertse, C.E., Hooijer, R., Willems, L.N., et al. Relationship between the inflammatory infiltrate in bronchial biopsy specimens and clinical severity of asthma in patients treated with inhaled steroids. Thorax 51:5 (1996), 496–502.
109. Soumelis, V., Thymic stromal lymphopoietin (TSLP): A pivotal role in allergic immune responses. Med Sci 23:8–9 (2007), 692–694.
110. Suzukawa, M., Iikura, M., Koketsu, R., Nagase, H., Tamura, C., Komiya, A., et al. An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J Immunol 181:9 (2008), 5981–5989.
111. Tang, W., Smith, S.G., Beaudin, S., Dua, B., Howie, K., Gauvreau, G., et al. IL-25 and IL-25 receptor expression on eosinophils from subjects with allergic asthma. Int Arch Allergy Immunol 163:1 (2014), 5–10.
112. Tarlo, S.M., Lemiere, C., Occupational asthma. N Engl J Med 370:7 (2014), 640–649.
113. Theoharides, T.C., Petra, A.I., Taracanova, A., Panagiotidou, S., Conti, P., Targeting IL-33 in autoimmunity and inflammation. J Pharmacol Exp Ther 354:1 (2015), 24–31.
114. Uller, L., Leino, M., Bedke, N., Sammut, D., Green, B., Lau, L., et al. Double-stranded RNA induces disproportionate expression of thymic stromal lymphopoietin versus interferon-beta in bronchial epithelial cells from donors with asthma. Thorax 65:7 (2010), 626–632.
115. Villarreal, D.O., Wise, M.C., Walters, J.N., Reuschel, E.L., Choi, M.J., Obeng-Adjei, N., et al. Alarmin IL-33 acts as an immunoadjuvant to enhance antigen-specific tumor immunity. Cancer Res 74:6 (2014), 1789–1800.
116. Watson, B., Gauvreau, G.M., Thymic stromal lymphopoietin: A central regulator of allergic asthma. Expert Opin Ther Targets 18:7 (2014), 771–785.
117. Willis, C.R., IL-17RA signaling drives airway inflammation and bronchial hyper reactivity in allergic asthma. Am J Respir Cell Mol Biol, 2015.
118. Wong, C.K., Hu, S., Cheung, P.F., Lam, C.W., Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: implications in allergic inflammation. Am J Respir Cell Mol Biol 43:3 (2010), 305–315.
119. Wu, W.H., Park, C.O., Oh, S.H., Kim, H.J., Kwon, Y.S., Bae, B.G., et al. Thymic stromal lymphopoietin-activated invariant natural killer T cells trigger an innate allergic immune response in atopic dermatitis. J Allergy Clin Immunol 126:2 (2010), 290–299 (9.e1–4).
120. Xiao, C., Puddicombe, S.M., Field, S., Haywood, J., Broughton-Head, V., Puxeddu, I., et al. Defective epithelial barrier function in asthma. J Allergy Clin Immunol 128:3 (2011), 549–556 (.e1–12.
121. Yagami, A., Orihara, K., Morita, H., Futamura, K., Hashimoto, N., Matsumoto, K., et al. IL-33 mediates inflammatory responses in human lung tissue cells. J Immunol 185:10 (2010), 5743–5750.
122. Yang, Q., Li, G., Zhu, Y., Liu, L., Chen, E., Turnquist, H., et al. IL-33 synergizes with TCR and IL-12 signaling to promote the effector function of CD8 + T cells. Eur J Immunol 41:11 (2011), 3351–3360.
123. Ying, S., O'Connor, B., Ratoff, J., Meng, Q., Fang, C., Cousins, D., et al. Expression and cellular provenance of thymic stromal lymphopoietin and chemokines in patients with severe asthma and chronic obstructive pulmonary disease. J Immunol 181:4 (2008), 2790–2798.
124. Ying, S., O'Connor, B., Ratoff, J., Meng, Q., Mallett, K., Cousins, D., et al. Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J Immunol 174:12 (2005), 8183–8190.
125. Zhang, J., Ramadan, A.M., Griesenauer, B., Li, W., Turner, M.J., Liu, C., et al. ST2 blockade reduces sST2-producing T cells while maintaining protective mST2-expressing T cells during graft-versus-host disease. Sci Transl Med, 7(308), 2015 (308ra160).
126. Zhang, K., Shan, L., Rahman, M.S., Unruh, H., Halayko, A.J., Gounni, A.S., Constitutive and inducible thymic stromal lymphopoietin expression in human airway smooth muscle cells: Role in chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 293:2 (2007), L375–L382.
127. Zoltowska, A.M., Lei, Y., Fuchs, B., Rask, C., Adner, M., Nilsson, G.P., The interleukin-33 receptor ST2 is important for the development of peripheral airway hyperresponsiveness and inflammation in a house dust mite mouse model of asthma. Clin Exp Allergy 46:3 (2016), 479–490.