DUOX1 mediates persistent epithelial EGFR activation, mucous cell metaplasia, and airway remodeling during allergic asthma

JCI Insight

Volumn 1, Issue 18, 2016, Pages

  Habibovic, Aida ^a   Hristova, Milena ^a   Heppner, David E ^a   Danyal, Karamatullah ^a   Ather, Jennifer L ^a   Janssen Heininger, Yvonne M W ^a   Irvin, Charles G ^a   Poynter, Matthew E ^a   Lundblad, Lennart K ^a   Dixon, Anne E ^a   Geiszt, Miklos ^b   van der Vliet, Albert ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85055611160     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.88811     Document Type: Article

References (65)

1. Fahy JV. Type 2 inflammation in asthma-present in most, absent in many. Nat Rev Immunol. 2015;15(1):57–65.
2. Wenzel SE. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med. 2012;18(5):716–725.
3. Holgate ST. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol Rev. 2011;242(1):205–219.
4. Holtzman MJ, Byers DE, Alexander-Brett J, Wang X. The role of airway epithelial cells and innate immune cells in chronic respiratory disease. Nat Rev Immunol. 2014;14(10):686–698.
5. Xiao C, et al. Defective epithelial barrier function in asthma. J Allergy Clin Immunol. 2011;128(3):549–56.e1.
6. Polosa R, et al. Expression of c-erbB receptors and ligands in the bronchial epithelium of asthmatic subjects. J Allergy Clin Immunol. 2002;109(1):75–81.
7. Puddicombe SM, et al. Involvement of the epidermal growth factor receptor in epithelial repair in asthma. FASEB J. 2000;14(10):1362–1374.
8. Stefanowicz D, et al. Elevated H3K18 acetylation in airway epithelial cells of asthmatic subjects. Respir Res. 2015;16:95.
9. Enomoto Y, et al. Tissue remodeling induced by hypersecreted epidermal growth factor and amphiregulin in the airway after an acute asthma attack. J Allergy Clin Immunol. 2009;124(5):913–20.e1.
10. Hamilton LM, et al. Altered protein tyrosine phosphorylation in asthmatic bronchial epithelium. Eur Respir J. 2005;25(6):978–985.
11. Hamilton LM, et al. The role of the epidermal growth factor receptor in sustaining neutrophil inflammation in severe asthma. Clin Exp Allergy. 2003;33(2):233–240.
12. Vallath S, Hynds RE, Succony L, Janes SM, Giangreco A. Targeting EGFR signalling in chronic lung disease: therapeutic challenges and opportunities. Eur Respir J. 2014;44(2):513–522.
13. Burgel PR, Nadel JA. Epidermal growth factor receptor-mediated innate immune responses and their roles in airway diseases. Eur Respir J. 2008;32(4):1068–1081.
14. Hristova M, et al. Airway epithelial dual oxidase 1 mediates allergen-induced IL-33 secretion and activation of type 2 immune responses. J Allergy Clin Immunol. 2016;137(5):1545–1556.e11.
15. Le Cras TD, et al. Epithelial EGF receptor signaling mediates airway hyperreactivity and remodeling in a mouse model of chronic asthma. Am J Physiol Lung Cell Mol Physiol. 2011;300(3):L414–L421.
16. Siddiqui S, et al. The modulation of large airway smooth muscle phenotype and effects of epidermal growth factor receptor inhibition in the repeatedly allergen-challenged rat. Am J Physiol Lung Cell Mol Physiol. 2013;304(12):L853–L862.
17. Hur GY, et al. Potential use of an anticancer drug gefinitib, an EGFR inhibitor, on allergic airway inflammation. Exp Mol Med. 2007;39(3):367–375.
18. Li T, Perez-Soler R. Skin toxicities associated with epidermal growth factor receptor inhibitors. Target Oncol. 2009;4(2):107–119.
19. Steuer CE, Ramalingam SS. Targeting EGFR in lung cancer: Lessons learned and future perspectives. Mol Aspects Med. 2015;45:67–73.
20. Woodruff PG, et al. Safety and efficacy of an inhaled epidermal growth factor receptor inhibitor (BIBW 2948 BS) in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010;181(5):438–445.
21. Gorissen SH, et al. Dual oxidase-1 is required for airway epithelial cell migration and bronchiolar reepithelialization after injury. Am J Respir Cell Mol Biol. 2013;48(3):337–345.
22. Shao MX, Nadel JA. Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci U S A. 2005;102(3):767–772.
23. Sham D, Wesley UV, Hristova M, van der Vliet A. ATP-mediated transactivation of the epidermal growth factor receptor in airway epithelial cells involves DUOX1-dependent oxidation of Src and ADAM17. PLoS One. 2013;8(1):e54391.
24. Yoo SK, Freisinger CM, LeBert DC, Huttenlocher A. Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J Cell Biol. 2012;199(2):225–234.
25. Paulsen CE, et al. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol. 2012;8(1):57–64.
26. Cho DY, et al. Expression of dual oxidases and secreted cytokines in chronic rhinosinusitis. Int Forum Allergy Rhinol. 2013;3(5):376–383.
27. Koff JL, Shao MX, Ueki IF, Nadel JA. Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium. Am J Physiol Lung Cell Mol Physiol. 2008;294(6):L1068–L1075.
28. Tully JE, et al. Epithelial NF-κB orchestrates house dust mite-induced airway inflammation, hyperresponsiveness, and fibrotic remodeling. J Immunol. 2013;191(12):5811–5821.
29. Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med. 2009;15(4):410–416.
30. Boots AW, Hristova M, Kasahara DI, Haenen GR, Bast A, van der Vliet A. ATP-mediated activation of the NADPH oxidase DUOX1 mediates airway epithelial responses to bacterial stimuli. J Biol Chem. 2009;284(26):17858–17867.
31. Barlow JL, 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. 2013;132(4):933–941.
32. Klein Wolterink RG, et al. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol. 2012;42(5):1106–1116.
33. Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med. 2015;21(7):698–708.
34. Allahverdian S, Harada N, Singhera GK, Knight DA, Dorscheid DR. Secretion of IL-13 by airway epithelial cells enhances epithelial repair via HB-EGF. Am J Respir Cell Mol Biol. 2008;38(2):153–160.
35. Wu CA, Peluso JJ, Zhu L, Lingenheld EG, Walker ST, Puddington L. Bronchial epithelial cells produce IL-5: implications for local immune responses in the airways. Cell Immunol. 2010;264(1):32–41.
36. Altenhöfer S, Radermacher KA, Kleikers PW, Wingler K, Schmidt HH. Evolution of NADPH Oxidase Inhibitors: Selectivity and Mechanisms for Target Engagement. Antioxid Redox Signal. 2015;23(5):406–427.
37. Gianni D, et al. A novel and specific NADPH oxidase-1 (Nox1) small-molecule inhibitor blocks the formation of functional invadopodia in human colon cancer cells. ACS Chem Biol. 2010;5(10):981–993.
38. van der Vliet A. NADPH oxidases in lung biology and pathology: host defense enzymes, and more. Free Radic Biol Med. 2008;44(6):938–955.
39. De Deken X, Corvilain B, Dumont JE, Miot F. Roles of DUOX-mediated hydrogen peroxide in metabolism, host defense, and signaling. Antioxid Redox Signal. 2014;20(17):2776–2793.
40. Chang S, Linderholm A, Franzi L, Kenyon N, Grasberger H, Harper R. Dual oxidase regulates neutrophil recruitment in allergic airways. Free Radic Biol Med. 2013;65:38–46.
41. Gour N, Wills-Karp M. IL-4 and IL-13 signaling in allergic airway disease. Cytokine. 2015;75(1):68–78.
42. Evans CM, et al. The polymeric mucin Muc5ac is required for allergic airway hyperreactivity. Nat Commun. 2015;6:6281.
43. Erle DJ, Sheppard D. The cell biology of asthma. J Cell Biol. 2014;205(5):621–631.
44. Evans CM, Kim K, Tuvim MJ, Dickey BF. Mucus hypersecretion in asthma: causes and effects. Curr Opin Pulm Med. 2009;15(1):4–11.
45. Harper RW, et al. Differential regulation of dual NADPH oxidases/peroxidases, Duox1 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium. FEBS Lett. 2005;579(21):4911–4917.
46. Christianson CA, et al. Persistence of asthma requires multiple feedback circuits involving type 2 innate lymphoid cells and IL-33. J Allergy Clin Immunol. 2015;136(1):59–68.e14.
47. Zaiss DM, Gause WC, Osborne LC, Artis D. Emerging functions of amphiregulin in orchestrating immunity, inflammation, and tissue repair. Immunity. 2015;42(2):216–226.
48. Ooi AT, et al. Identification of an interleukin 13-induced epigenetic signature in allergic airway inflammation. Am J Transl Res. 2012;4(2):219–228.
49. Nicodemus-Johnson J, et al. Genome-Wide Methylation Study Identifies an IL-13-induced Epigenetic Signature in Asthmatic Airways. Am J Respir Crit Care Med. 2016;193(4):376–385.
50. Manzo ND, Foster WM, Stripp BR. Amphiregulin-dependent mucous cell metaplasia in a model of nonallergic lung injury. Am J Respir Cell Mol Biol. 2012;47(3):349–357.
51. Kwon J, et al. The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Sci Signal. 2010;3(133):ra59.
52. Rada B, Park JJ, Sil P, Geiszt M, Leto TL. NLRP3 inflammasome activation and interleukin-1β release in macrophages require calcium but are independent of calcium-activated NADPH oxidases. Inflamm Res. 2014;63(10):821–830.
53. van der Vliet A, Janssen-Heininger YM. Hydrogen peroxide as a damage signal in tissue injury and inflammation: murderer, mediator, or messenger? J Cell Biochem. 2014;115(3):427–435.
54. Nussbaum JC, et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 2013;502(7470):245–248.
55. Doherty TA. At the bench: understanding group 2 innate lymphoid cells in disease. J Leukoc Biol. 2015;97(3):455–467.
56. Truong TH, Ung PM, Palde PB, Paulsen CE, Schlessinger A, Carroll KS. Molecular basis for redox activation of epidermal growth factor receptor kinase. Cell Chem Biol. 2016;23(7):837–848.
57. Hoffman SM, et al. Ablation of glutaredoxin-1 modulates house dust mite-induced allergic airways disease in mice. Am J Respir Cell Mol Biol. 2016;55(3):377–386.
58. Heppner DE, Hristova M, Dustin CM, Danyal K, Habibovic A, van der Vliet A. The NADPH oxidases DUOX1 and NOX2 Play Distinct Roles in Redox Regulation of Epidermal Growth Factor Receptor Signaling [published online ahead of print September 20, 2016]. J Biol Chem. doi: 10.1074/jbc.M116.749028.
59. Yankaskas JR, et al. Papilloma virus immortalized tracheal epithelial cells retain a well-differentiated phenotype. Am J Physiol. 1993;264(5 Pt 1):C1219–C1230.
60. Donkó A, et al. Urothelial cells produce hydrogen peroxide through the activation of Duox1. Free Radic Biol Med. 2010;49(12):2040–2048.
61. Muller L, Brighton LE, Carson JL, Fischer WA 2nd, Jaspers I. Culturing of human nasal epithelial cells at the air liquid interface. J Vis Exp. 2013;80(80):e50646. doi:10.3791/50646.
62. De Deken X, et al. Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J Biol Chem. 2000;275(30):23227–23233.
63. Klomsiri C, et al. Use of dimedone-based chemical probes for sulfenic acid detection evaluation of conditions affecting probe incorporation into redox-sensitive proteins. Meth Enzymol. 2010;473:77–94.
64. Tomioka S, Bates JH, Irvin CG. Airway and tissue mechanics in a murine model of asthma: alveolar capsule vs. forced oscillations. J Appl Physiol. 2002;93(1):263–270.
65. Ather JL, Foley KL, Suratt BT, Boyson JE, Poynter ME. Airway epithelial NF-κB activation promotes the ability to overcome inhalational antigen tolerance. Clin Exp Allergy. 2015;45(7):1245–1258.