IL-33 stimulates CXCL8/IL-8 secretion in goblet cells but not normally differentiated airway cells

Clinical and Experimental Allergy

Volumn 44, Issue 4, 2014, Pages 540-552

  Tanabe, T ^a   Shimokawaji, T ^a   Kanoh, S ^a   Rubin, B K ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Airway; Asthma; Goblet cell hyperplasia; IL 13; Mucin; Normal human bronchial epithelial cell; Th2 cytokine

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; INTERLEUKIN 33; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; RECEPTOR ANTIBODY; RECEPTOR PROTEIN; CELL SURFACE RECEPTOR; IL1RL1 PROTEIN, HUMAN; IL33 PROTEIN, HUMAN; INTERLEUKIN 13; INTERLEUKIN DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE 1; ORGANIC COMPOUND; PD 98058;

AIRWAY; ARTICLE; BRONCHUS MUCOSA; CELL CULTURE; CELL DIFFERENTIATION; CYTOKINE RELEASE; EPITHELIUM CELL; GOBLET CELL; HUMAN; HUMAN CELL; LIQUID; METAPLASIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RESPIRATORY TRACT INFLAMMATION; SIGNAL TRANSDUCTION; TH2 CELL; BIOSYNTHESIS; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; PHOSPHORYLATION; RESPIRATORY TRACT MUCOSA;

CELL DIFFERENTIATION; GENE EXPRESSION; GOBLET CELLS; HUMANS; INTERLEUKIN-13; INTERLEUKIN-8; INTERLEUKINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; ORGANIC CHEMICALS; PHOSPHORYLATION; RECEPTORS, CELL SURFACE; RESPIRATORY MUCOSA; RNA, MESSENGER;

EID: 84897833527     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12283     Document Type: Article

References (61)

1. Lambrecht BN, Hammad H. The airway epithelium in asthma. Nat Med 2012; 18:684-92.
2. Izuhara K, Ohta S, Shiraishi H et al. The mechanism of mucus production in bronchial asthma. Curr Med Chem 2009; 16:2867-75.
3. Rogers DF. Airway mucus hypersecretion in asthma: an undervalued pathology? Curr Opin Pharmacol 2004; 4:241-50.
4. Sidebotham HJ, Roche WR. Asthma deaths; persistent and preventable mortality. Histopathology 2003; 43:105-17.
5. Kuyper LM, Pare PD, Hogg JC et al. Characterization of airway plugging in fatal asthma. Am J Med 2003; 115:6-11.
6. Holgate ST. The epidemic of allergy and asthma. Nature 1999; 402:B2-4.
7. Wills-Karp M. IL-12/IL-13 axis in allergic asthma. J Allergy Clin Immunol 2001; 107:9-18.
8. Tanabe T, Kanoh S, Tsushima K, Yamazaki Y, Kubo K, Rubin BK. Clarithromycin inhibits interleukin-13-induced goblet cell hyperplasia in human airway cells. Am J Respir Cell Mol Biol 2011; 45:1075-83.
9. Wills-Karp M, Luyimbazi J, Xu X et al. Interleukin-13: central mediator of allergic asthma. Science 1998; 282:2258-61.
10. Ordonez CL, Khashayar R, Wong HH et al. Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am J Respir Crit Care Med 2001; 163:517-23.
11. Atherton HC, Jones G, Danahay H. IL-13-induced changes in the goblet cell density of human bronchial epithelial cell cultures: MAP kinase and phosphatidylinositol 3-kinase regulation. Am J Physiol Lung Cell Mol Physiol 2003; 285:L730-9.
12. Tanabe T, Fujimoto K, Yasuo M et al. Modulation of mucus production by interleukin-13 receptor alpha2 in the human airway epithelium. Clin Exp Allergy 2008; 38:122-34.
13. Kanoh S, Tanabe T, Rubin BK. IL-13-induced MUC5AC production and goblet cell differentiation is steroid resistant in human airway cells. Clin Exp Allergy 2011; 41:1747-56.
14. Schmitz J, Owyang A, Oldham E et al. 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 2005; 23:479-90.
15. Prefontaine D, Nadigel J, Chouiali F et al. Increased IL-33 expression by epithelial cells in bronchial asthma. J Allergy Clin Immunol 2010; 125:752-4.
16. Fujita J, Kawaguchi M, Kokubu F et al. Interleukin-33 induces interleukin-17F in bronchial epithelial cells. Allergy 2012; 67:744-50.
17. Kearley J, Buckland KF, Mathie SA, Lloyd CM. Resolution of allergic inflammation and airway hyperreactivity is dependent upon disruption of the T1/ST2-IL-33 pathway. Am J Respir Crit Care Med 2009; 179:772-81.
18. Prefontaine D, Lajoie-Kadoch S, Foley S et al. Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J Immunol 2009; 183:5094-103.
19. Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol 2010; 72:495-516.
20. Richman-Eisenstat JB, Jorens PG, Hebert CA, Ueki I, Nadel JA. Interleukin-8: an important chemoattractant in sputum of patients with chronic inflammatory airway diseases. Am J Physiol 1993; 264:L413-8.
21. Ordonez CL, Shaughnessy TE, Matthay MA, Fahy JV. Increased neutrophil numbers and IL-8 levels in airway secretions in acute severe asthma: Clinical and biologic significance. Am J Respir Crit Care Med 2000; 161:1185-90.
22. Gagliardo R, Chanez P, Vignola AM et al. Glucocorticoid receptor alpha and beta in glucocorticoid dependent asthma. Am J Respir Crit Care Med 2000; 162:7-13.
23. Therien AG, Bernier V, Weicker S et al. Adenovirus IL-13-induced airway disease in mice: a corticosteroid-resistant model of severe asthma. Am J Respir Cell Mol Biol 2008; 39:26-35.
24. Lordan JL, Bucchieri F, Richter A et al. Cooperative effects of Th2 cytokines and allergen on normal and asthmatic bronchial epithelial cells. J Immunol 2002; 169:407-14.
25. Kurowska-Stolarska M, Stolarski B, Kewin P et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol 2009; 183:6469-77.
26. Kanoh S, Tanabe T, Rubin BK. Dapsone inhibits IL-8 secretion from human bronchial epithelial cells stimulated with lipopolysaccharide and resolves airway inflammation in the ferret. Chest 2011; 140:980-90.
27. Tanabe T, Kanoh S, Moskowitz WB, Rubin BK. Cardiac asthma: TGF-beta from the failing heart leads to squamous metaplasia in human airway cells and in the murine lung. Chest 2012; 142:1274-83.
28. Yagami A, Orihara K, Morita H et al. IL-33 mediates inflammatory responses in human lung tissue cells. J Immunol 2010; 185:5743-50.
29. Hong YS, Moon SJ, Joo YB et al. Measurement of interleukin-33 (IL-33) and IL-33 receptors (sST2 and ST2L) in patients with rheumatoid arthritis. J Korean Med Sci 2011; 26:1132-9.
30. Thavagnanam S, Parker JC, McBrien ME, Skibinski G, Heaney LG, Shields MD. Effects of IL-13 on mucociliary differentiation of pediatric asthmatic bronchial epithelial cells. Pediatr Res 2011; 69:95-100.
31. Parker J, Sarlang S, Thavagnanam S et al. A 3-D well-differentiated model of pediatric bronchial epithelium demonstrates unstimulated morphological differences between asthmatic and nonasthmatic cells. Pediatr Res 2010; 67:17-22.
32. Kondo Y, Yoshimoto T, Yasuda K et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol 2008; 20:791-800.
33. Sakashita M, Yoshimoto T, Hirota T et al. Association of serum interleukin-33 level and the interleukin-33 genetic variant with Japanese cedar pollinosis. Clin Exp Allergy 2008; 38:1875-81.
34. Pushparaj PN, Tay HK, H'Ng SC et al. The cytokine interleukin-33 mediates anaphylactic shock. Proc Natl Acad Sci U S A 2009; 106:9773-8.
35. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G. Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol 2007; 179:2051-4.
36. Ho LH, Ohno T, Oboki K et al. IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcepsilonRI signals. J Leukoc Biol 2007; 82:1481-90.
37. Pecaric-Petkovic T, Didichenko SA, Kaempfer S, Spiegl N, Dahinden CA. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 2009; 113:1526-34.
38. Iikura M, Suto H, Kajiwara N et al. IL-33 can promote survival, adhesion and cytokine production in human mast cells. Lab Invest 2007; 87:971-8.
39. Allakhverdi Z, Comeau MR, Smith DE et al. CD34+ hemopoietic progenitor cells are potent effectors of allergic inflammation. J Allergy Clin Immunol 2009; 123:472-8.
40. Kamekura R, Kojima T, Takano K, Go M, Sawada N, Himi T. The role of IL-33 and its receptor ST2 in human nasal epithelium with allergic rhinitis. Clin Exp Allergy 2012; 42:218-28.
41. Gudbjartsson DF, Bjornsdottir US, Halapi E et al. Sequence variants affecting eosinophil numbers associate with asthma and myocardial infarction. Nat Genet 2009; 41:342-7.
42. Ho JE, Chen WY, Chen MH et al. Common genetic variation at the IL1RL1 locus regulates IL-33/ST2 signaling. J Clin Invest 2013; 123:4208-18.
43. Kurowska-Stolarska M, Kewin P, Murphy G et al. IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. J Immunol 2008; 181:4780-90.
44. Zhiguang X, Wei C, Steven R et al. Over-expression of IL-33 leads to spontaneous pulmonary inflammation in mIL-33 transgenic mice. Immunol Lett 2010; 131:159-65.
45. Liu X, Li M, Wu Y, Zhou Y, Zeng L, Huang T. Anti-IL-33 antibody treatment inhibits airway inflammation in a murine model of allergic asthma. Biochem Biophys Res Commun 2009; 386:181-5.
46. Coyle AJ, Lloyd C, Tian J et al. Crucial role of the interleukin 1 receptor family member T1/ST2 in T helper cell type 2-mediated lung mucosal immune responses. J Exp Med 1999; 190:895-902.
47. Saetta M, Di Stefano A, Rosina C, Thiene G, Fabbri LM. Quantitative structural analysis of peripheral airways and arteries in sudden fatal asthma. Am Rev Respir Dis 1991; 143:138-43.
48. Aikawa T, Shimura S, Sasaki H, Ebina M, Takishima T. Marked goblet cell hyperplasia with mucus accumulation in the airways of patients who died of severe acute asthma attack. Chest 1992; 101:916-21.
49. Nadel JA, Takeyama K, Agusti C. Role of neutrophil elastase in hypersecretion in asthma. Eur Respir J 1999; 13:190-6.
50. Stoloff SW, Kelly HW. Updates on the use of inhaled corticosteroids in asthma. Curr Opin Allergy Clin Immunol 2011; 11:337-44.
51. Naseer T, Minshall EM, Leung DY et al. Expression of IL-12 and IL-13 mRNA in asthma and their modulation in response to steroid therapy. Am J Respir Crit Care Med 1997; 155:845-51.
52. Kibe A, Inoue H, Fukuyama S et al. Differential regulation by glucocorticoid of interleukin-13-induced eosinophilia, hyperresponsiveness, and goblet cell hyperplasia in mouse airways. Am J Respir Crit Care Med 2003; 167:50-6.
53. Hamzaoui A, Berraies A, Kaabachi W, Haifa M, Ammar J, Kamel H. Induced sputum levels of IL-33 and soluble ST2 in young asthmatic children. J Asthma 2013; 50:803-9.
54. Saglani S, Lui S, Ullmann N et al. IL-33 promotes airway remodeling in pediatric patients with severe steroid-resistant asthma. J Allergy Clin Immunol 2013; 132:676-85. e13.
55. Inoue D, Numasaki M, Watanabe M et al. IL-17A promotes the growth of airway epithelial cells through ERK-dependent signaling pathway. Biochem Biophys Res Commun 2006; 347:852-8.
56. Yadav UC, Aguilera-Aguirre L, Ramana KV, Boldogh I, Srivastava SK. Aldose reductase inhibition prevents metaplasia of airway epithelial cells. PLoS ONE 2010; 5:e14440.
57. Lachowicz-Scroggins ME, Boushey HA, Finkbeiner WE, Widdicombe JH. Interleukin-13-induced mucous metaplasia increases susceptibility of human airway epithelium to rhinovirus infection. Am J Respir Cell Mol Biol 2010; 43:652-61.
58. Mata M, Sarria B, Buenestado A, Cortijo J, Cerda M, Morcillo EJ. Phosphodiesterase 4 inhibition decreases MUC5AC expression induced by epidermal growth factor in human airway epithelial cells. Thorax 2005; 60:144-52.
59. van Wetering S, Zuyderduyn S, Ninaber DK, van Sterkenburg MA, Rabe KF, Hiemstra PS. Epithelial differentiation is a determinant in the production of eotaxin-2 and -3 by bronchial epithelial cells in response to IL-4 and IL-13. Mol Immunol 2007; 44:803-11.
60. Rubin BK, Tomkiewicz R, Fahy JV, Green FH. Histopathology of fatal asthma: drowning in mucus. Pediatr Pulmonol 2001; 23(Suppl):88-9.
61. Carroll N, Carello S, Cooke C, James A. Airway structure and inflammatory cells in fatal attacks of asthma. Eur Respir J 1996; 9:709-15.