The induction of pattern-recognition receptor expression against influenza a virus through Duox2-derived reactive oxygen species in nasal mucosa

American Journal of Respiratory Cell and Molecular Biology

Volumn 53, Issue 4, 2015, Pages 525-535

  Kim, Hyun Jik ^a,e   Kim, Chang Hoon ^d,e   Kim, Min Ji ^d   Ryu, Ji Hwan ^d   Seong, Sang Yeop ^d   Kim, Sujin ^d   Lim, Su Jin ^a   Holtzman, Michael J ^b,c   Yoon, Joo Heon ^d,e,f  

^a Seoul National University College of Medicine   (South Korea)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Department of Thoracic Surgery   (United States)

^d Yonsei University College of Medicine   (South Korea)

^e Airway Mucus Institute   (South Korea)

^f BK21 Project for Medical Science   (South Korea)

Author keywords

Duox2; Influenza A virus; Melanoma differentiation associated protein 5; Reactive oxygen species; Retinoic acid inducible gene I

Indexed keywords

MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; MESSENGER RNA; PATTERN RECOGNITION RECEPTOR; PROTEIN; REACTIVE OXYGEN METABOLITE; RETINOIC ACID INDUCIBLE PROTEIN I; SHORT HAIRPIN RNA; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; DUOX1 PROTEIN, MOUSE; IFIH1 PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROBO3 PROTEIN, MOUSE; TLR3 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CELL LYSATE; CONTROLLED STUDY; DUOX2 GENE; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HOST RESISTANCE; HUMAN; HUMAN CELL; INFLUENZA A; INFLUENZA A VIRUS; INOCULATION; MALE; MOLECULAR RECOGNITION; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NOSE MUCOSA; PLAQUE ASSAY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA VIRUS; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL LINE; GENETICS; IMMUNOLOGY; INFLUENZA; METABOLISM; TRANSCRIPTION INITIATION; VIROLOGY;

ANIMALS; CELL LINE; DEAD-BOX RNA HELICASES; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; NADPH OXIDASE; NASAL MUCOSA; NERVE TISSUE PROTEINS; REACTIVE OXYGEN SPECIES; TOLL-LIKE RECEPTOR 3; TRANSCRIPTIONAL ACTIVATION;

EID: 84942903130     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0334OC     Document Type: Article

References (39)

1. Kawai T, Akira S. Pathogen recognition with Toll-like receptors. Curr Opin Immunol 2005;17:338-344.
2. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004;5:730-737.
3. Gitlin L, Benoit L, Song C, Cella M, Gilfillan S, Holtzman MJ, Colonna M. Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog 2010;6:e1000734.
4. García-Sastre A, Biron CA. Type 1 interferons and the virus-host relationship: a lesson in détente. Science 2006;312:879-882.
5. Wu S, Metcalf JP, Wu W. Innate immune response to influenza virus. Curr Opin Infect Dis 2011;24:235-240.
6. Levy DE, Darnell JE Jr. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 2002;3:651-662.
7. Horimoto T, Kawaoka Y. Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 2005;3:591-600.
8. Liu T, Castro S, Brasier AR, Jamaluddin M, Garofalo RP, Casola A. Reactive oxygen species mediate virus-induced STAT activation: role of tyrosine phosphatases. J Biol Chem 2004;279: 2461-2469.
9. van der Vliet A. NADPH oxidases in lung biology and pathology: host defense enzymes, and more. Free Radic Biol Med 2008;44:938-955.
10. Kim HJ, Kim CH, Ryu JH, Joo JH, Lee SN, Kim MJ, Lee JG, Bae YS, Yoon JH. Crosstalk between platelet-derived growth factor-induced Nox4 activation and MUC8 gene overexpression in human airway epithelial cells. Free Radic Biol Med 2011;50:1039-1052.
11. Haller O, Kochs G, Weber F. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 2006;344:119-130.
12. Mellqvist UH, Hansson M, Brune M, Dahlgren C, Hermodsson S, Hellstrand K. Natural killer cell dysfunction and apoptosis induced by chronic myelogenous leukemia cells: role of reactive oxygen species and regulation by histiamine. Blood 1999;65:196-204.
13. Lipinski S, Till A, Sina C, Arlt A, Grasberger H, Schreiber S, Rosenstiel P. DUOX2-derived reactive oxygen species are effectors of NOD2- mediated antibacterial responses. J Cell Sci 2009;122:3522-3530.
14. Kim HJ, Kim CH, Ryu JH, Kim MJ, Park CY, Lee JM, Holtzman MJ, Yoon JH. Reactive oxygen species induce antiviral innate immune response through IFN-l regulation in human nasal epithelial cells. Am J Respir Cell Mol Biol 2013;49:855-865.
15. Wang J, Oberley-Deegan R, Wang S, Nikrad M, Funk CJ, Hartshorn KL, Mason RJ. Differentiated human alveolar type II cells secrete antiviral IL-29 (IFN-lambda 1) in response to influenza A infection. J Immunol 2009;182:1296-1304.
16. Yoon JH, Gray T, Guzman K, Koo JS, Nettesheim P. Regulation of the secretory phenotype of human airway epithelium by retinoic acid, triiodothyronine, and extracellular matrix. Am J Respir Cell Mol Biol 1997;16:724-731.
17. Kim MJ, Ryu JC, Kwon Y, Lee S, Bae YS, Yoon JH, Ryu JH. Dual oxidase 2 in lung epithelia is essential for hyperoxia-induced acute lung injury in mice. Antioxid Redox Signal 2014;21:1803-1818.
18. Johnson KR, Marden CC, Ward-Bailey P, Gagnon LH, Bronson RT, Donahue LR. Congenital hypothyroidism, dwarfism, and hearing impairment caused by a missense mutation in the mouse dual oxidase 2 gene, Duox2. Mol Endocrinol 2007;21:1593-1602.
19. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 2006;312:1882-1883.
20. Koarai A, Sugiura H, Yanagisawa S, Ichikawa T, Minakata Y, Matsunaga K, Hirano T, Akamatsu K, Ichinose M. Oxidative stress enhances Tolllike receptor 3 response to double-stranded RNA in airway epithelial cells. Am J Respir Cell Mol Biol 2010;42:651-660.
21. Vlahos R, Stambas J, Bozinovski S, Broughton BR, Drummond GR, Selemidis S. Inhibition of Nox2 oxidase activity ameliorates influenza A virus-induced lung inflammation. PLoS Pathog 2011;7:e1001271.
22. Vlahos R, Stambas J, Selemidis S. Suppressing production of reactive oxygen species (ROS) for influenza A virus therapy. Trends Pharmacol Sci 2012;33:3-8.
23. Pollock JD, Williams DA, Gifford MA, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 1995;9:202-209.
24. Gao XP, Standiford TJ, Rahman A, Newstead M, Holland SM, Dinauer MC, Liu QH, Malik AB. Role of NADPH oxidase in the mechanism of lung neutrophil sequestration and microvessel injury induced by Gram-negative sepsis: studies in p47phox2/2 and gp91phox2/2 mice. J Immunol 2002;168:3974-3982.
25. Zmijewski JW, Lorne E, Zhao X, Tsuruta Y, Sha Y, Liu G, Abraham E. Antiinflammatory effects of hydrogen peroxide in neutrophil activation and acute lung injury. Am J Respir Crit Care Med 2009; 179:694-704.
26. Bae YS, Choi MK, Lee WJ. Dual oxidase in mucosal immunity and hostmicrobe homeostasis. Trends Immunol 2010;31:278-287.
27. Park HS, Jin DK, Shin SM, Jang MK, Longo N, Park JW, Bae DS, Bae YS. Impaired generation of reactive oxygen species in leprechaunism through downregulation of Nox4. Diabetes 2005;54: 3175-3181.
28. Mahadev K, Motoshima H, Wu X, Ruddy JM, Arnold RS, Cheng G, Lambeth JD, Goldstein BJ. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol 2004;24: 1844-1854.
29. Lambeth JD, Kawahara T, Diebold B. Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 2007;43: 319-331.
30. Schwarzer C, Machen TE, Illek B, Fischer H. NADPH oxidase-dependent acid production in airway epithelial cells. J Biol Chem 2004;279: 36454-36461.
31. Ris-Stalpers C. Physiology and pathophysiology of the DUOXes. Antioxid Redox Signal 2006;8:1563-1572.
32. Weichart D, Gobom J, Klopfleisch S, Häsler R, Gustavsson N, Billmann S, Lehrach H, Seegert D, Schreiber S, Rosenstiel P. Analysis of NOD2-mediated proteome response to muramyl dipeptide in HEK293 cells. J Biol Chem 2006;281:2380-2389.
33. Snelgrove RJ, Edwards L, Rae AJ, Hussell T. An absence of reactive oxygen species improves the resolution of lung influenza infection. Eur J Immunol 2006;36:1364-1373.
34. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S, Finberg RW, Gack MU. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 2013;38:437-449.
35. Slater L, Bartlett NW, Haas JJ, Zhu J, Message SD, Walton RP, Sykes A, Dahdaleh S, Clarke DL, Belvisi MG, et al. Co-ordinated role of TLR3, RIG-I and MDA5 in the innate response to rhinovirus in bronchial epithelium. PLoS Pathog 2010;6: e1001178.
36. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, Taxman DJ, Guthrie EH, Pickles RJ, Ting JP. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009;30:556-565.
37. Li H, Willingham SB, Ting JP, Re F. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J Immunol 2008;181:17-21.
38. Tal MC, Sasai M, Lee HK, Yordy B, Shadel GS, Iwasaki A. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci USA 2009;106: 2770-2775.
39. Soucy-Faulkner A, Mukawera E, Fink K, Martel A, Jouan L, Nzengue Y, Lamarre D, Vande Velde C, Grandvaux N. Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression. PLoS Pathog 2010;6:e1000930.