IL4 and IL-17A provide a Th2/Th17-polarized inflammatory milieu in favor of TGF-β1 to induce bronchial epithelial-mesenchymal transition (EMT)

International Journal of Clinical and Experimental Pathology

Volumn 6, Issue 8, 2013, Pages 1481-1492

  Ji, Xiaoying ^a   Li, Jinxiu ^a   Xu, Li ^a   Wang, Wenjing ^a   Luo, Ming ^a   Luo, Shuangling ^a   Ma, Libing ^b   Li, Keng ^a   Gong, Subo ^a   He, Long ^c,d   Zhang, Zhijun ^c,d   Yang, Ping ^c,d   Zhou, Zhiguang ^a   Xiang, Xudong ^a   Wang, Cong Yi ^c,d  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b GUILIN MEDICAL UNIVERSITY   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Airway remodeling; Chronic inflammatory milieu; Epithelial mesenchymal transition (EMT); ERK1 2; Severe asthma

Indexed keywords

IL17A PROTEIN, HUMAN; INTERLEUKIN 17; INTERLEUKIN 4; TRANSFORMING GROWTH FACTOR BETA1;

AIRWAY REMODELING; ARTICLE; ASTHMA; BRONCHUS; CELL LINE; CHRONIC INFLAMMATORY MILIEU; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIAL MESENCHYMAL TRANSITION (EMT); ERK1/2; HUMAN; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SEVERE ASTHMA; TH17 CELL; TH2 CELL; WESTERN BLOTTING;

AIRWAY REMODELING; CHRONIC INFLAMMATORY MILIEU; EPITHELIAL MESENCHYMAL TRANSITION (EMT); ERK1/2; SEVERE ASTHMA;

AIRWAY REMODELING; ASTHMA; BLOTTING, WESTERN; BRONCHI; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-4; REAL-TIME POLYMERASE CHAIN REACTION; TH17 CELLS; TH2 CELLS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84883037022     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Cho SH, Stanciu LA, Holgate ST, Johnston SL. Increased interleukin-4, interleukin-5, and interferon-gamma in airway CD4+ and CD8+ T cells in atopic asthma. Am J Respir Crit Care Med 2005; 171: 224-230.
2. Doe C, Bafadhel M, Siddiqui S, Desai D, Mistry V, Rugman P, McCormick M, Woods J, May R, Sleeman MA, Anderson IK, Brightling CE. Expression of the T helper 17-associated cytokines IL-17A and IL-17F in asthma and COPD. Chest 2010; 138: 1140-1147.
3. Kiwamoto T, Ishii Y, Morishima Y, Yoh K, Maeda A, Ishizaki K, Iizuka T, Hegab AE, Matsuno Y, Homma S, Nomura A, Sakamoto T, Takahashi S, Sekizawa K. Transcription factors T-bet and GATA-3 regulate development of airway remodeling. Am J Respir Crit Care Med 2006; 174: 142-151.
4. Wang Q, Li H, Yao Y, Xia D, Zhou J. The overexpression of heparin-binding epidermal growth factor is responsible for Th17-induced airway remodeling in an experimental asthma model. J Immunol 2010; 185: 834-841.
5. Zhao Y, Yang J, Gao YD, Guo W. Th17 immunity in patients with allergic asthma. Int Arch Allergy Immunol 2010; 151: 297-307.
6. Bai TR. Evidence for airway remodeling in chronic asthma. Curr Opin Allergy Clin Immunol 2010; 10: 82-86.
7. Homer RJ, Elias JA. Consequences of long-term inflammation. Airway remodeling. Clin Chest Med 2000; 21: 331-343, ix.
8. Leigh R, Ellis R, Wattie JN, Hirota JA, Matthaei KI, Foster PS, O'Byrne PM, Inman MD. Type 2 cytokines in the pathogenesis of sustained airway dysfunction and airway remodeling in mice. Am J Respir Crit Care Med 2004; 169: 860-867.
9. Bossley CJ, Fleming L, Gupta A, Regamey N, Frith J, Oates T, Tsartsali L, Lloyd CM, Bush A, Saglani S. Pediatric severe asthma is characterized by eosinophilia and remodeling without T(H)2 cytokines. J Allergy Clin Immunol 2012; 129: 974-982, e913.
10. Lopez-Guisa JM, Powers C, File D, Cochrane E, Jimenez N, Debley JS. Airway epithelial cells from asthmatic children differentially express proremodeling factors. J Allergy Clin Immunol 2012; 129: 990-997, e996.
11. Michalik M, Pierzchalska M, Wlodarczyk A, Wojcik KA, Czyz J, Sanak M, Madeja Z. Transition of asthmatic bronchial fibroblasts to myofibroblasts is inhibited by cell-cell contacts. Respir Med 2011; 105: 1467-1475.
12. Cohen L, E X, Tarsi J, Ramkumar T, Horiuchi TK, Cochran R, DeMartino S, Schechtman KB, Hussain I, Holtzman MJ, Castro M; NHLBI Severe Asthma Research Program (SARP). Epithelial cell proliferation contributes to airway remodeling in severe asthma. Am J Respir Crit Care Med 2007; 176: 138-145.
13. Heijink IH, Postma DS, Noordhoek JA, Broekema M, Kapus A. House dust mite-promoted epithelial-to-mesenchymal transition in human bronchial epithelium. Am J Respir Cell Mol Biol 2010; 42: 69-79.
14. Trautmann A, Kruger K, Akdis M, Muller-Wening D, Akkaya A, Brocker EB, Blaser K, Akdis CA. Apoptosis and loss of adhesion of bronchial epithelial cells in asthma. Int Arch Allergy Immunol 2005; 138: 142-150.
15. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 2009; 119: 1438-1449.
16. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009; 119: 1429-1437.
17. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A. Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 2003; 284: F911-924.
18. Doerner AM, Zuraw BL. TGF-beta1 induced epithelial to mesenchymal transition (EMT) in human bronchial epithelial cells is enhanced by IL-1beta but not abrogated by corticosteroids. Respir Res 2009; 10: 100.
19. Molet S, Hamid Q, Davoine F, Nutku E, Taha R, Page N, Olivenstein R, Elias J, Chakir J. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 2001; 108: 430-438.
20. Redington AE, Madden J, Frew AJ, Djukanovic R, Roche WR, Holgate ST, Howarth PH. Transforming growth factor-beta 1 in asthma. Measurement in bronchoalveolar lavage fluid. Am J Respir Crit Care Med 1997; 156: 642-647.
21. Walker C, Bauer W, Braun RK, Menz G, Braun P, Schwarz F, Hansel TT, Villiger B. Activated T cells and cytokines in bronchoalveolar lavages from patients with various lung diseases associated with eosinophilia. Am J Respir Crit Care Med 1994; 150: 1038-1048.
22. Gal A, Sjoblom T, Fedorova L, Imreh S, Beug H, Moustakas A. Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 2008; 27: 1218-1230.
23. Hackett TL, Warner SM, Stefanowicz D, Shaheen F, Pechkovsky DV, Murray LA, Argentieri R, Kicic A, Stick SM, Bai TR, Knight DA. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-beta1. Am J Respir Crit Care Med 2009; 180: 122-133.
24. Kojima T, Takano K, Yamamoto T, Murata M, Son S, Imamura M, Yamaguchi H, Osanai M, Chiba H, Himi T, Sawada N. Transforming growth factor-beta induces epithelial to mesenchymal transition by down-regulation of claudin-1 expression and the fence function in adult rat hepatocytes. Liver Int 2008; 28: 534-545.
25. Nicolas FJ, Lehmann K, Warne PH, Hill CS, Downward J. Epithelial to mesenchymal transition in Madin-Darby canine kidney cells is accompanied by down-regulation of Smad3 expression, leading to resistance to transforming growth factor-beta-induced growth arrest. J Biol Chem 2003; 278: 3251-3256.
26. Sheppard D. Transforming growth factor beta: a central modulator of pulmonary and airway inflammation and fibrosis. Proc Am Thorac Soc 2006; 3: 413-417.
27. Johnson JR, Roos A, Berg T, Nord M, Fuxe J. Chronic respiratory aeroallergen exposure in mice induces epithelial-mesenchymal transition in the large airways. PLoS One 2011; 6: e16175.
28. Buckley ST, Medina C, Ehrhardt C. Differential susceptibility to epithelial-mesenchymal transition (EMT) of alveolar, bronchial and intestinal epithelial cells in vitro and the effect of angiotensin II receptor inhibition. Cell Tissue Res 2010; 342: 39-51.
29. Yang J, Liu Y. Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 2001; 159: 1465-1475.
30. Ahn JH, Kim CH, Kim YH, Kim SJ, Lee SY, Kim YK, Kim KH, Moon HS, Song JS, Park SH, Kwon SS. Inflammatory and remodeling events in asthma with chronic exposure to house dust mites: a murine model. J Korean Med Sci 2007; 22: 1026-1033.
31. Zhang S, Lv JW, Yang P, Yu Q, Pang J, Wang Z, Guo H, Liu S, Hu J, Li J, Leng J, Huang Y, Ye Z, Wang CY. Loss of dicer exacerbates cyclophosphamide-induced bladder overactivity by enhancing purinergic signaling. Am J Pathol 2012; 181: 937-946.
32. Rao X, Zhong J, Zhang S, Zhang Y, Yu Q, Yang P, Wang MH, Fulton DJ, Shi H, Dong Z, Wang D, Wang CY. Loss of methyl-CpG-binding domain protein 2 enhances endothelial angiogenesis and protects mice against hind-limb ischemic injury. Circulation 2011; 123: 2964-2974.
33. Zhong J, Yang P, Muta K, Dong R, Marrero M, Gong F, Wang CY. Loss of Jak2 selectively suppresses DC-mediated innate immune response and protects mice from lethal dose of LPS-induced septic shock. PLoS One 2010; 5: e9593.
34. Heijink IH, Marcel Kies P, van Oosterhout AJ, Postma DS, Kauffman HF, Vellenga E. Der p, IL-4, and TGF-beta cooperatively induce EGFR-dependent TARC expression in airway epithelium. Am J Respir Cell Mol Biol 2007; 36: 351-359.
35. Ip WK, Wong CK, Lam CW. Interleukin (IL)-4 and IL-13 up-regulate monocyte chemoattractant protein-1 expression in human bronchial epithelial cells: involvement of p38 mitogen-activated protein kinase, extracellular signal-regulated kinase 1/2 and Janus kinase-2 but not c-Jun NH2-terminal kinase 1/2 signalling pathways. Clin Exp Immunol 2006; 145: 162-172.
36. Zijlstra GJ, Ten Hacken NH, Hoffmann RF, van Oosterhout AJ, Heijink IH. Interleukin-17A induces glucocorticoid insensitivity in human bronchial epithelial cells. Eur Respir J 2012; 39: 439-445.
37. Roberts AB, Tian F, Byfield SD, Stuelten C, Ooshima A, Saika S, Flanders KC. Smad3 is key to TGF-beta-mediated epithelial-to-mesenchymal transition, fibrosis, tumor suppression and metastasis. Cytokine Growth Factor Rev 2006; 17: 19-27.
38. Davies M, Robinson M, Smith E, Huntley S, Prime S, Paterson I. Induction of an epithelial to mesenchymal transition in human immortal and malignant keratinocytes by TGF-beta1 involves MAPK, Smad and AP-1 signalling pathways. J Cell Biochem 2005; 95: 918-931.
39. Semlali A, Jacques E, Plante S, Biardel S, Milot J, Laviolette M, Boulet LP, Chakir J. TGF-beta suppresses EGF-induced MAPK signaling and proliferation in asthmatic epithelial cells. Am J Respir Cell Mol Biol 2008; 38: 202-208.
40. Aujla SJ, Alcorn JF. T(H)17 cells in asthma and inflammation. Biochim Biophys Acta 2011; 1810: 1066-1079.
41. Inoue D, Numasaki M, Watanabe M, Kubo H, Sasaki T, Yasuda H, Yamaya M, Sasaki H. IL-17A promotes the growth of airway epithelial cells through ERK-dependent signaling pathway. Biochem Biophys Res Commun 2006; 347: 852-858.
42. Ricciardolo FL, Di Stefano A, van Krieken JH, Sont JK, van Schadewijk A, Rabe KF, Donner CF, Hiemstra PS, Sterk PJ, Mauad T. Proliferation and inflammation in bronchial epithelium after allergen in atopic asthmatics. Clin Exp Allergy 2003; 33: 905-911.
43. Cokugras H, Akcakaya N, Seckin, Camcioglu Y, Sarimurat N, Aksoy F. Ultrastructural examination of bronchial biopsy specimens from children with moderate asthma. Thorax 2001; 56: 25-29.
44. Payne DN, Rogers AV, Adelroth E, Bandi V, Guntupalli KK, Bush A, Jeffery PK. Early thickening of the reticular basement membrane in children with difficult asthma. Am J Respir Crit Care Med 2003; 167: 78-82.
45. Zhang M, Zhang Z, Pan HY, Wang DX, Deng ZT, Ye XL. TGF-beta1 induces human bronchial epithelial cell-to-mesenchymal transition in vitro. Lung 2009; 187: 187-194.
46. Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 2007; 67: 9066-9076.
47. Holz C, Niehr F, Boyko M, Hristozova T, Distel L, Budach V, Tinhofer I. Epithelial-mesenchymal-transition induced by EGFR activation interferes with cell migration and response to irradiation and cetuximab in head and neck cancer cells. Radiother Oncol 2011; 101: 158-164.
48. Hamilton LM, Puddicombe SM, Dearman RJ, Kimber I, Sandstrom T, Wallin A, Howarth PH, Holgate ST, Wilson SJ, Davies DE. Altered protein tyrosine phosphorylation in asthmatic bronchial epithelium. Eur Respir J 2005; 25: 978-985.