Dual oxidase regulates neutrophil recruitment in allergic airways

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 38-46

  Chang, Sandra ^a   Linderholm, Angela ^a   Franzi, Lisa ^a   Kenyon, Nicholas ^a   Grasberger, Helmut ^b   Harper, Richart ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Asthma; Dual oxidase; DUOX; Free radicals; Lung; Murine; Neutrophil

Indexed keywords

DUOX1 PROTEIN; DUOX2 PROTEIN; HYDROGEN PEROXIDE; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; METHACHOLINE; MUCIN; OVALBUMIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; DUOX1 PROTEIN, MOUSE;

AIRWAY RESISTANCE; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DENSITOMETRY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REGULATION; EOSINOPHIL; EPITHELIUM CELL; HISTOLOGY; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; LUNG ALVEOLUS MACROPHAGE; LUNG FUNCTION; LUNG LAVAGE; LUNG PARENCHYMA; LYMPHOCYTE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT ALLERGY; SIGNAL TRANSDUCTION; WOUND HEALING; 129 MOUSE; ANIMAL; ASTHMA; DISEASE MODEL; ENZYMOLOGY; HYPERSENSITIVITY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA; WESTERN BLOTTING;

ANIMALS; ASTHMA; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HYDROGEN PEROXIDE; HYPERSENSITIVITY; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; NADPH OXIDASE; NEUTROPHIL INFILTRATION; RESPIRATORY MUCOSA;

EID: 84884560968     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.06.012     Document Type: Article

References (56)

1. S.T. Holgate Innate and adaptive immune responses in asthma Nat. Med. 18 2012 673 683
2. C.M. Lloyd, and E.M. Hessel Functions of T cells in asthma: more than just T(H)2 cells Nat. Rev. Immunol. 10 2010 838 848
3. H. Hammad, and B.N. Lambrecht Dendritic cells and airway epithelial cells at the interface between innate and adaptive immune responses Allergy 66 2011 579 587
4. M. Larche Regulatory T cells in allergy and asthma Chest 132 2007 1007 1014
5. S. Reuter, N. Dehzad, H. Martin, L. Bohm, M. Becker, R. Buhl, M. Stassen, and C. Taube TLR3 but not TLR7/8 ligand induces allergic sensitization to inhaled allergen J. Immunol. 188 2012 5123 5131
6. R.H. Wilson, S. Maruoka, G.S. Whitehead, J.F. Foley, G.P. Flake, M.L. Sever, D.C. Zeldin, M. Kraft, S. Garantziotis, H. Nakano, and D.N. Cook The Toll-like receptor 5 ligand flagellin promotes asthma by priming allergic responses to indoor allergens Nat. Med. 18 2012 1705 1710
7. H. Hammad, M. Chieppa, F. Perros, M.A. Willart, R.N. Germain, and B.N. Lambrecht House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells Nat. Med. 15 2009 410 416
8. A.M. Tan, H.C. Chen, P. Pochard, S.C. Eisenbarth, C.A. Herrick, and H.K. Bottomly TLR4 signaling in stromal cells is critical for the initiation of allergic Th2 responses to inhaled antigen J. Immunol. 184 2010 3535 3544
9. L. Aguilera-Aguirre, A. Bacsi, A. Saavedra-Molina, A. Kurosky, S. Sur, and I. Boldogh Mitochondrial dysfunction increases allergic airway inflammation J. Immunol. 183 2009 5379 5387
10. T. Rangasamy, J. Guo, W.A. Mitzner, J. Roman, A. Singh, A.D. Fryer, M. Yamamoto, T.W. Kensler, R.M. Tuder, S.N. Georas, and S. Biswal Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice J. Exp. Med. 202 2005 47 59 (Pubitemid 41002909)
11. K. Ckless, S.R. Hodgkins, J.L. Ather, R. Martin, and M.E. Poynter Epithelial, dendritic, and CD4(+) T cell regulation of and by reactive oxygen and nitrogen species in allergic sensitization Biochim. Biophys. Acta 1810 2011 1025 1034
12. I. Rahman, D. Morrison, K. Donaldson, and W. MacNee Systemic oxidative stress in asthma, COPD, and smokers Am. J. Respir. Crit. Care Med. 154 1996 1055 1060
13. S.A. Comhair, and S.C. Erzurum Redox control of asthma: molecular mechanisms and therapeutic opportunities Antioxid. Redox Signaling 12 2010 93 124
14. H. Sugiura, and M. Ichinose Oxidative and nitrative stress in bronchial asthma Antioxid. Redox Signaling 10 2008 785 797 (Pubitemid 351225897)
15. Lambeth J.D. Kawahara, and T. Diebold B. Regulation of Nox and Duox enzymatic activity and expression Free Radic. Biol. Med. 43 2007 319 331
16. R. Forteza, M. Salathe, F. Miot, and G.E. Conner Regulated hydrogen peroxide production by Duox in human airway epithelial cells Am. J. Respir. Cell Mol. Biol. 32 2005 462 469 (Pubitemid 40629332)
17. H. Fischer, L.K. Gonzales, V. Kolla, C. Schwarzer, F. Miot, B. Illek, and P.L. Ballard Developmental regulation of DUOX1 expression and function in human fetal lung epithelial cells Am. J. Physiol. Lung Cell. Mol. Physiol 292 2007 L1506 1514
18. J.H. Ryu, J.Y. Yoo, M.J. Kim, S.G. Hwang, K.C. Ahn, J.C. Ryu, M.K. Choi, J.H. Joo, C.H. Kim, S.N. Lee, W.J. Lee, J. Kim, D.M. Shin, M.N. Kweon, Y.S. Bae, and J.H. Yoon Distinct TLR-mediated pathways regulate house dust mite-induced allergic disease in the upper and lower airways J. Allergy Clin. Immunol. 131 2013 549 561
19. J.H. Joo, J.H. Ryu, C.H. Kim, H.J. Kim, M.S. Suh, J.O. Kim, S.Y. Chung, S.N. Lee, H.M. Kim, Y.S. Bae, and J.H. Yoon Dual oxidase 2 is essential for the toll-like receptor 5-mediated inflammatory response in airway mucosa Antioxid. Redox Signaling 16 2012 57 70
20. M. Yu, J. Lam, B. Rada, T.L. Leto, S.J. Levine, and R.N.A. Double-stranded induces shedding of the 34-kDa soluble TNFR1 from human airway epithelial cells via TLR3-TRIF-RIP1-dependent signaling: roles for dual oxidase 2- and caspase-dependent pathways J. Immunol 186 2011 1180 1188
21. J.L. Koff, M.X. Shao, I.F. Ueki, and J.A. Nadel Multiple TLRs activate EGFR via a signaling cascade to produce innate immune responses in airway epithelium Am. J. Physiol. Lung Cell. Mol. Physiol 294 2008 L1068 1075
22. M.X. Shao, and J.A. Nadel Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells Proc. Natl. Acad. Sci. USA 102 2005 767 772 (Pubitemid 40282740)
23. I. Kuwahara, E.P. Lillehoj, T. Koga, Y. Isohama, T. Miyata, and K.C. Kim The signaling pathway involved in neutrophil elastase stimulated MUC1 transcription Am. J. Respir. Cell Mol. Biol. 37 2007 691 698 (Pubitemid 350211639)
24. U.V. Wesley, P.F. Bove, M. Hristova, S. McCarthy, and A. van der Vliet Airway epithelial cell migration and wound repair by ATP-mediated activation of dual oxidase 1 J. Biol. Chem. 282 2007 3213 3220 (Pubitemid 47084365)
25. S.H. Gorissen, M. Hristova, A. Habibovic, L.M. Sipsey, P.C. Spiess, Y.M. Janssen-Heininger, and A. van der Vliet Dual oxidase-1 is required for airway epithelial cell migration and bronchiolar reepithelialization after injury Am. J. Respir. Cell Mol. Biol. 48 2013 337 345
26. R.W. Harper, C. Xu, J.P. Eiserich, Y. Chen, C.Y. Kao, P. Thai, H. Setiadi, and R. Wu Differential regulation of dual NADPH oxidases/peroxidases, Duox1 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium FEBS Lett. 579 2005 4911 4917 (Pubitemid 41218684)
27. B. Rada, K. Lekstrom, S. Damian, C. Dupuy, and T.L. Leto The Pseudomonas toxin pyocyanin inhibits the dual oxidase-based antimicrobial system as it imposes oxidative stress on airway epithelial cells J. Immunol. 181 2008 4883 4893
28. H. Grasberger, X. De Deken, O.B. Mayo, H. Raad, M. Weiss, X.H. Liao, and S. Refetoff Mice deficient in dual oxidase maturation factors are severely hypothyroid Mol. Endocrinol. 26 2012 481 492
29. J.M. Bratt, L.M. Franzi, A.L. Linderholm, M.S. Last, N.J. Kenyon, and J.A. Last Arginase enzymes in isolated airways from normal and nitric oxide synthase 2-knockout mice exposed to ovalbumin Toxicol. Appl. Pharmacol. 234 2009 273 280
30. N.J. Kenyon, R.W. Ward, and J.A. Last Airway fibrosis in a mouse model of airway inflammation Toxicol. Appl. Pharmacol. 186 2003 90 100 (Pubitemid 36298618)
31. P. Ashwood, P. Krakowiak, I. Hertz-Picciotto, R. Hansen, and I. Pessah Van de Water, J. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome Brain Behav. Immun 25 2011 40 45
32. N.J. Kenyon, J.M. Bratt, A.L. Linderholm, M.S. Last, J.A. Last, and I. Arginases II in lungs of ovalbumin-sensitized mice exposed to ovalbumin: sources and consequences Toxicol. Appl. Pharmacol. 230 2008 269 275
33. N.J. Kenyon, R. Liu, E.M. O'Roark, W. Huang, L. Peng, and K.S. Lam An alpha4beta1 integrin antagonist decreases airway inflammation in ovalbumin-exposed mice Eur. J. Pharmacol. 603 2009 138 146
34. J.L. Lomas, C.S. Chung, P.S. Grutkoski, B.W. LeBlanc, L. Lavigne, J. Reichner, S.H. Gregory, L.A. Doughty, W.G. Cioffi, and A. Ayala Differential effects of macrophage inflammatory chemokine-2 and keratinocyte-derived chemokine on hemorrhage-induced neutrophil priming for lung inflammation: assessment by adoptive cells transfer in mice Shock 19 2003 358 365
35. D.R. Call, J.A. Nemzek, S.J. Ebong, G.R. Bolgos, D.E. Newcomb, G.K. Wollenberg, and D.G. Remick Differential local and systemic regulation of the murine chemokines KC and MIP2 Shock 15 2001 278 284 (Pubitemid 33596719)
36. C.D. Sadik, N.D. Kim, and A.D. Luster Neutrophils cascading their way to inflammation Trends Immunol. 32 2011 452 460
37. L. Ramakrishna, V.C. de Vries, and M.A. Curotto de Lafaille Cross-roads in the lung: immune cells and tissue interactions as determinants of allergic asthma Immunol. Res. 53 2012 213 228
38. H. Grasberger, and S. Refetoff Identification of the maturation factor for dual oxidase: evolution of an eukaryotic operon equivalent J. Biol. Chem. 281 2006 18269 18272 (Pubitemid 44035482)
39. H. Fischer Mechanisms and function of DUOX in epithelia of the lung Antioxid. Redox Signaling 11 2009 2453 2465
40. J.H. Widdicombe, and C.B. Basbaum Highland, E. Ion contents and other properties of isolated cells from dog tracheal epithelium Am. J. Physiol. 241 1981 C184 192 (Pubitemid 12216077)
41. R.W. Harper The role of DUOX isozymes in the respiratory tract epithelium G. Valacchi, P. Davis, Oxidants in Biology: a Question of Balance 2008 Springer Houten, The Netherlands 267 278
42. J. Kwon, K.E. Shatynski, H. Chen, S. Morand, X. de Deken, F. Miot, T.L. Leto, and M.S. Williams The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling Sci. Signaling 3 2010 ra59
43. A.A. Zeki, L. Franzi, J. Last, and N.J. Kenyon Simvastatin inhibits airway hyperreactivity: implications for the mevalonate pathway and beyond Am. J. Respir. Crit. Care Med. 180 2009 731 740
44. Y. Yang, J. Loy, R.P. Ryseck, D. Carrasco, and R. Bravo Antigen-induced eosinophilic lung inflammation develops in mice deficient in chemokine eotaxin Blood 92 1998 3912 3923 (Pubitemid 28525218)
45. V.J. Thannickal, and B.L. Fanburg Reactive oxygen species in cell signaling Am. J. Physiol. Lung Cell. Mol. Physiol 279 2000 L1005 1028
46. J.D. Lambeth NOX enzymes and the biology of reactive oxygen Nat. Rev. Immunol. 4 2004 181 189 (Pubitemid 38339084)
47. P. Niethammer, C. Grabher, A.T. Look, and T.J. Mitchison A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish Nature 459 2009 996 999
48. H. Hattori, K.K. Subramanian, J. Sakai, Y. Jia, Y. Li, T.F. Porter, F. Loison, B. Sarraj, A. Kasorn, H. Jo, C. Blanchard, D. Zirkle, D. McDonald, S.Y. Pai, C.N. Serhan, and H.R. Luo Small-molecule screen identifies reactive oxygen species as key regulators of neutrophil chemotaxis Proc. Natl. Acad. Sci. USA 107 2010 3546 3551
49. I.V. Klyubin, K.M. Kirpichnikova, and I.A. Gamaley Hydrogen peroxide-induced chemotaxis of mouse peritoneal neutrophils Eur. J. Cell Biol. 70 1996 347 351 (Pubitemid 26268238)
50. T. Nakanaga, J.A. Nadel, I.F. Ueki, J.L. Koff, and M.X. Shao Regulation of interleukin-8 via an airway epithelial signaling cascade Am. J. Physiol. Lung Cell. Mol. Physiol 292 2007 L1289 1296
51. P.R. Mangan, L.E. Harrington, D.B. O'Quinn, W.S. Helms, D.C. Bullard, C.O. Elson, R.D. Hatton, S.M. Wahl, T.R. Schoeb, and C.T. Weaver Transforming growth factor-beta induces development of the T(H)17 lineage Nature 441 2006 231 234
52. D.Y. Cho, J.V. Nayak, D.T. Bravo, W. Le, A. Nguyen, J.A. Edward, P.H. Hwang, B. Illek, and H. Fischer Expression of dual oxidases and secreted cytokines in chronic rhinosinusitis Int. Forum Allergy Rhinol 3 2013 376 383
53. R.G. Stirling, and K.F. Chung Severe asthma: definition and mechanisms Allergy 56 2001 825 840 (Pubitemid 32800389)
54. J.V. Fahy, K.W. Kim, J. Liu, and H.A. Boushey Prominent neutrophilic inflammation in sputum from subjects with asthma exacerbation J. Allergy Clin. Immunol. 95 1995 843 852
55. K.F. Chung, P. Godard, E. Adelroth, J. Ayres, N. Barnes, P. Barnes, E. Bel, P. Burney, P. Chanez, G. Connett, C. Corrigan, J. de Blic, L. Fabbri, S.T. Holgate, P. Ind, G. Joos, H. Kerstjens, P. Leuenberger, C.G. Lofdahl, S. McKenzie, H. Magnussen, D. Postma, M. Saetta, S. Salmeron, and P. Sterk Difficult/therapy-resistant asthma: the need for an integrated approach to define clinical phenotypes, evaluate risk factors, understand pathophysiology and find novel therapies. ERS Task Force on Difficult/Therapy-Resistant Asthma Eur. Respir. J. 13 1999 1198 1208 (Pubitemid 29288952)
56. V.M. Keatings, A. Jatakanon, Y.M. Worsdell, and P.J. Barnes Effects of inhaled and oral glucocorticoids on inflammatory indices in asthma and COPD Am. J. Respir. Crit. Care Med. 155 1997 542 548 (Pubitemid 27085799)