Nrf2 protects human alveolar epithelial cells against injury induced by influenza A virus

Respiratory Research

Volumn 13, Issue 1, 2012, Pages

  Kosmider, Beata ^a   Messier, Elise M ^a   Janssen, William J ^a   Nahreini, Piruz ^a   Wang, Jieru ^a   Hartshorn, Kevan L ^b   Mason, Robert J ^a  

^a DEPARTMENT OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alveolar macrophages; Apoptosis; Efferocytosis; Human alveolar epithelial cells; Influenza A virus; Nrf2

Indexed keywords

CASPASE 3; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOPROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; INFLUENZA A; LUNG ALVEOLUS EPITHELIUM CELL; LUNG ALVEOLUS MACROPHAGE; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; VIRUS REPLICATION; WESTERN BLOTTING; ADOLESCENT; CELL CULTURE; CELL SURVIVAL; CHILD; EPITHELIUM CELL; FEMALE; INFLUENZA VIRUS A; LUNG ALVEOLUS; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; VIROLOGY;

ADOLESCENT; CELL SURVIVAL; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; EPITHELIAL CELLS; FEMALE; HUMANS; INFLUENZA A VIRUS; MALE; PULMONARY ALVEOLI;

EID: 84861811046     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-13-43     Document Type: Article

References (49)

1. Tate MD, Schilter HC, Brooks AG, Reading PC: Responses of mouse airway epithelial cells and alveolar macrophages to virulent and avirulent strains of influenza A virus. Viral Immunol 2011,24(2):77-88.
2. Guo H, Kumar P, Moran TM, Garcia-Sastre A, Zhou Y, Malarkannan S: The functional impairment of natural killer cells during influenza virus infection. Immunol Cell Biol 2009,87(8):579-589.
3. Fukuyama S, Kawaoka Y: The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr Opin Immunol 2011,23(4):481-486.
4. Phillips M, Cataneo RN, Chaturvedi A, Danaher PJ, Devadiga A, Legendre DA, Nail KL, Schmitt P, Wai J: Effect of influenza vaccination on oxidative stress products in breath. J Breath Res 2010,4(2):026001.
5. Kesic MJ, Simmons SO, Bauer R, Jaspers I: Nrf2 expression modifies influenza A entry and replication in nasal epithelial cells. Free Radic Biol Med 2011,51(2):444-453.
6. Yageta Y, Ishii Y, Morishima Y, Masuko H, Ano S, Yamadori T, Itoh K, Takeuchi K, Yamamoto M, Hizawa N: Role of Nrf2 in Host Defense against Influenza Virus in Cigarette Smoke-Exposed Mice. J Virol 2011,85(10):4679-4690.
7. Mata M, Morcillo E, Gimeno C, Cortijo J: N-acetyl-l-cysteine (NAC) inhibit mucin synthesis and pro-inflammatory mediators in alveolar type II epithelial cells infected with influenza virus A and B and with respiratory syncytial virus (RSV). Biochem Pharmacol 2011,82(5):548-555.
8. Uchide N, Toyoda H: Antioxidant therapy as a potential approach to severe influenza-associated complications. Molecules 2011,16(3):2032-2052.
9. Wu W, Booth JL, Duggan ES, Wu S, Patel KB, Coggeshall KM, Metcalf JP: Innate immune response to H3N2 and H1N1 influenza virus infection in a human lung organ culture model. Virology 2010,396(2):178-188.
10. Henson PM, Tuder RM: Apoptosis in the lung: induction, clearance and detection. Am J Physiol Lung Cell Mol Physiol 2008,294(4):L601-611.
11. Monks J, Rosner D, Geske FJ, Lehman L, Hanson L, Neville MC, Fadok VA: Epithelial cells as phagocytes: apoptotic epithelial cells are engulfed by mammary alveolar epithelial cells and repress inflammatory mediator release. Cell Death Differ 2005,12(2):107-114.
12. Rosenblatt J, Raff MC, Cramer LP: An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 2001,11(23):1847-1857.
13. Boutten A, Goven D, Boczkowski J, Bonay M: Oxidative stress targets in pulmonary emphysema: focus on the Nrf2 pathway. Expert Opin Ther Targets 2010,14(3):329-346.
14. Cho HY, Imani F, Miller-DeGraff L, Walters D, Melendi GA, Yamamoto M, Polack FP, Kleeberger SR: Antiviral activity of Nrf2 in a murine model of respiratory syncytial virus disease. Am J Respir Crit Care Med 2009,179(2):138-150.
15. Hosakote YM, Jantzi PD, Esham DL, Spratt H, Kurosky A, Casola A, Garofalo RP: Viral-mediated inhibition of antioxidant enzymes contributes to the pathogenesis of severe respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med 2011,183(11):1550-1560.
16. Heikkinen T: Influenza in children. Acta Paediatr 2006,95(7):778-784.
17. Poehling KA, Edwards KM, Weinberg GA, Szilagyi P, Staat MA, Iwane MK, Bridges CB, Grijalva CG, Zhu Y, Bernstein DI, et al.: The underrecognized burden of influenza in young children. N Engl J Med 2006,355(1):31-40.
18. Lines JL, Hoskins S, Hollifield M, Cauley LS, Garvy BA: The migration of T cells in response to influenza virus is altered in neonatal mice. J Immunol 2010,185(5):2980-2988.
19. Wang J, Nikrad MP, Phang T, Gao B, Alford T, Ito Y, Edeen K, Travanty EA, Kosmider B, Hartshorn K, et al.: Innate Immune Response to Influenza A Virus in Differentiated Human Alveolar Type II cells. Am J Respir Cell Mol Biol 2011,45(3):582-591.
20. Wang J, Edeen K, Manzer R, Chang Y, Wang S, Chen X, Funk CJ, Cosgrove GP, Fang X, Mason RJ: Differentiated human alveolar epithelial cells and reversibility of their phenotype in vitro. Am J Respir Cell Mol Biol 2007,36(6):661-668.
21. Manzer R, Wang J, Nishina K, McConville G, Mason RJ: Alveolar epithelial cells secrete chemokines in response to IL-1beta and lipopolysaccharide but not to ozone. Am J Respir Cell Mol Biol 2006,34(2):158-166.
22. Gonzalez R, Yang YH, Griffin C, Allen L, Tigue Z, Dobbs L: Freshly isolated rat alveolar type I cells, type II cells, and cultured type II cells have distinct molecular phenotypes. Am J Physiol Lung Cell Mol Physiol 2005,288(1):L179-189.
23. Kosmider B, Loader JE, Murphy RC, Mason RJ: Apoptosis induced by ozone and oxysterols in human alveolar epithelial cells. Free Radic Biol Med 2010,48(11):1513-1524.
24. Mossel EC, Wang J, Jeffers S, Edeen KE, Wang S, Cosgrove GP, Funk CJ, Manzer R, Miura TA, Pearson LD, et al.: SARS-CoV replicates in primary human alveolar type II cell cultures but not in type I-like cells. Virology 2008,372(1):127-135.
25. 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(3):1296-1304.
26. Hartshorn KL, Collamer M, Auerbach M, Myers JB, Pavlotsky N, Tauber AI: Effects of influenza A virus on human neutrophil calcium metabolism. J Immunol 1988,141(4):1295-1301.
27. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, Johnson JA, Murphy TH: Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 2003,23(8):3394-3406.
28. Singh A, Rangasamy T, Thimmulappa RK, Lee H, Osburn WO, Brigelius-Flohe R, Kensler TW, Yamamoto M, Biswal S: Glutathione peroxidase 2, the major cigarette smoke-inducible isoform of GPX in lungs, is regulated by Nrf2. Am J Respir Cell Mol Biol 2006,35(6):639-650.
29. McPhillips K, Janssen WJ, Ghosh M, Byrne A, Gardai S, Remigio L, Bratton DL, Kang JL, Henson P: TNF-alpha inhibits macrophage clearance of apoptotic cells via cytosolic phospholipase A2 and oxidant-dependent mechanisms. J Immunol 2007,178(12):8117-8126.
30. Kosmider B, Messier EM, Chu HW, Mason RJ: Human alveolar epithelial cell injury induced by cigarette smoke. PLoS One 2011,6(12):e26059.
31. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al.: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009,55(4):611-622.
32. Miura TA, Wang J, Holmes KV, Mason RJ: Rat coronaviruses infect rat alveolar type I epithelial cells and induce expression of CXC chemokines. Virology 2007,369(2):288-298.
33. Votyakova TV, Reynolds IJ: Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch Biochem Biophys 2004,431(1):138-144.
34. Gould NS, Min E, Gauthier S, Martin RJ, Day BJ: Lung glutathione adaptive responses to cigarette smoke exposure. Respir Res 2011, 12:133.
35. Rahman I, Kode A, Biswas SK: Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 2006,1(6):3159-3165.
36. Watanabe Y, Hashimoto Y, Shiratsuchi A, Takizawa T, Nakanishi Y: Augmentation of fatality of influenza in mice by inhibition of phagocytosis. Biochem Biophys Res Commun 2005,337(3):881-886.
37. Hodge S, Hodge G, Brozyna S, Jersmann H, Holmes M, Reynolds PN: Azithromycin increases phagocytosis of apoptotic bronchial epithelial cells by alveolar macrophages. Eur Respir J 2006,28(3):486-495.
38. Cai J, Chen Y, Seth S, Furukawa S, Compans RW, Jones DP: Inhibition of influenza infection by glutathione. Free Radic Biol Med 2003,34(7):928-936.
39. Cho HY, Reddy SP, Kleeberger SR: Nrf2 defends the lung from oxidative stress. Antioxid Redox Signal 2006,8(1-2):76-87.
40. Cho HY, Reddy SP, Debiase A, Yamamoto M, Kleeberger SR: Gene expression profiling of NRF2-mediated protection against oxidative injury. Free Radic Biol Med 2005,38(3):325-343.
41. Zhang X, Chen X, Song H, Chen HZ, Rovin BH: Activation of the Nrf2/antioxidant response pathway increases IL-8 expression. Eur J Immunol 2005,35(11):3258-3267.
42. Sozzani S, Bosisio D, Mantovani A, Ghezzi P: Linking stress, oxidation and the chemokine system. Eur J Immunol 2005,35(11):3095-3098.
43. Lam WY, Tang JW, Yeung AC, Chiu LC, Sung JJ, Chan PK: Avian influenza virus A/HK/483/97(H5N1) NS1 protein induces apoptosis in human airway epithelial cells. J Virol 2008,82(6):2741-2751.
44. Price GE, Smith H, Sweet C: Differential induction of cytotoxicity and apoptosis by influenza virus strains of differing virulence. J Gen Virol 1997,78(Pt 11):2821-2829.
45. Schultz-Cherry S, Dybdahl-Sissoko N, Neumann G, Kawaoka Y, Hinshaw VS: Influenza virus ns1 protein induces apoptosis in cultured cells. J Virol 2001,75(17):7875-7881.
46. Tate MD, Pickett DL, van Rooijen N, Brooks AG, Reading PC: Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 2010,84(15):7569-7580.
47. Eckardt-Michel J, Lorek M, Baxmann D, Grunwald T, Keil GM, Zimmer G: The fusion protein of respiratory syncytial virus triggers p53-dependent apoptosis. J Virol 2008,82(7):3236-3249.
48. Mok CK, Lee DC, Cheung CY, Peiris M, Lau AS: Differential onset of apoptosis in influenza A virus H5N1- and H1N1-infected human blood macrophages. J Gen Virol 2007,88(Pt 4):1275-1280.
49. Maruoka S, Hashimoto S, Gon Y, Nishitoh H, Takeshita I, Asai Y, Mizumura K, Shimizu K, Ichijo H, Horie T: ASK1 regulates influenza virus infection-induced apoptotic cell death. Biochem Biophys Res Commun 2003,307(4):870-876.