Redox Biology of Respiratory Viral Infections

Viruses - Tập 10 Số 8 - Trang 392
Olga A. Khomich1,2, Sergey N. Kochetkov1, Birke Bartosch3,2, Alexander V. Ivanov1
1ISTC - Engelhardt Institute of Molecular Biology (32, ul. Vavilova, 119991 Moscow - Russia)
2UNICANCER/CRCL - Centre de Recherche en Cancérologie de Lyon (28, rue Laennec - 69373 Lyon - France)
3LabEx DEVweCAN - Développement Cancer et Thérapies Ciblées [Lyon] (28 rue Laennec 69008 Lyon - France)

Tóm tắt

Respiratory viruses cause infections of the upper or lower respiratory tract and they are responsible for the common cold—the most prevalent disease in the world. In many cases the common cold results in severe illness due to complications, such as fever or pneumonia. Children, old people, and immunosuppressed patients are at the highest risk and require fast diagnosis and therapeutic intervention. However, the availability and efficiencies of existing therapeutic approaches vary depending on the virus. Investigation of the pathologies that are associated with infection by respiratory viruses will be paramount for diagnosis, treatment modalities, and the development of new therapies. Changes in redox homeostasis in infected cells are one of the key events that is linked to infection with respiratory viruses and linked to inflammation and subsequent tissue damage. Our review summarizes current knowledge on changes to redox homeostasis, as induced by the different respiratory viruses.

Từ khóa


Tài liệu tham khảo

2014, Hydrogen peroxide as a damage signal in tissue injury and inflammation: Murderer, mediator, or messenger?, J. Cell. Biochem., 115, 427, 10.1002/jcb.24683

Mittal, 2014, Reactive oxygen species in inflammation and tissue injury, Antioxid. Redox Signal., 20, 1126, 10.1089/ars.2012.5149

Circu, 2010, Reactive oxygen species, cellular redox systems, and apoptosis, Free Radic. Biol. Med., 48, 749, 10.1016/j.freeradbiomed.2009.12.022

Birben, 2012, Oxidative stress and antioxidant defense, World Allergy Organ. J., 5, 9, 10.1097/WOX.0b013e3182439613

Fukai, 2011, Superoxide dismutases: Role in redox signaling, vascular function, and diseases, Antioxid. Redox Signal., 15, 1583, 10.1089/ars.2011.3999

Cox, 2009, Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling, Biochem. J., 425, 313, 10.1042/BJ20091541

Winterbourn, 2008, Reconciling the chemistry and biology of reactive oxygen species, Nat. Chem. Biol., 4, 278, 10.1038/nchembio.85

Trachootham, 2008, Redox regulation of cell survival, Antioxid. Redox Signal., 10, 1343, 10.1089/ars.2007.1957

Ivanov, 2017, Oxidative stress, a trigger of hepatitis C and B virus-induced liver carcinogenesis, Oncotarget, 8, 3895, 10.18632/oncotarget.13904

Jones, 2015, The Redox Code, Antioxid. Redox Signal., 23, 734, 10.1089/ars.2015.6247

Sies, 2015, Oxidative stress: A concept in redox biology and medicine, Redox Biol., 4, 180, 10.1016/j.redox.2015.01.002

Hoffman, 2015, Thiol redox chemistry: Role of protein cysteine oxidation and altered redox homeostasis in allergic inflammation and asthma, J. Cell. Biochem., 116, 884, 10.1002/jcb.25017

Knipe, D.M., and Howley, P.M. (2013). Fields Virology, Wolters Kluwer/Lippincott Williams & Wilkins Health. [6th ed.]. 2 volumes.

World Health Organization (2016). Influenza (Seasonal) Fact Sheet No 211, World Health Organization.

Colman, 1994, Influenza virus neuraminidase: Structure, antibodies, and inhibitors, Protein Sci., 3, 1687, 10.1002/pro.5560031007

Pielak, 2009, Mechanism of drug inhibition and drug resistance of influenza A M2 channel, Proc. Natl. Acad. Sci. USA, 106, 7379, 10.1073/pnas.0902548106

Afonso, 2016, Taxonomy of the order Mononegavirales: Update 2016, Arch. Virol., 161, 2351, 10.1007/s00705-016-2880-1

Falsey, 2000, Respiratory syncytial virus infection in adults, Clin. Microbiol. Rev., 13, 371, 10.1128/CMR.13.3.371

Nair, 2010, Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: A systematic review and meta-analysis, Lancet, 375, 1545, 10.1016/S0140-6736(10)60206-1

Bont, 2016, Defining the Epidemiology and Burden of Severe Respiratory Syncytial Virus Infection Among Infants and Children in Western Countries, Infect. Dis. Ther., 5, 271, 10.1007/s40121-016-0123-0

Turner, 2014, Respiratory syncytial virus: Current and emerging treatment options, Clinicoecon. Outcomes Res., 6, 217, 10.2147/CEOR.S60710

Jacobs, 2013, Human rhinoviruses, Clin. Microbiol. Rev., 26, 135, 10.1128/CMR.00077-12

Lim, 2014, Enhanced oxidative damage to DNA, lipids, and proteins and levels of some antioxidant enzymes, cytokines, and heat shock proteins in patients infected with influenza H1N1 virus, Acta Virol., 58, 253, 10.4149/av_2014_03_253

Ng, 2014, Does influenza A infection increase oxidative damage?, Antioxid. Redox Signal., 21, 1025, 10.1089/ars.2014.5907

Erkekoglu, 2013, Selenium levels, selenoenzyme activities and oxidant/antioxidant parameters in H1N1-infected children, Turk. J. Pediatr., 55, 271

Nin, 2012, Lung histopathological findings in fatal pandemic influenza A (H1N1), Med. Intensiv., 36, 24, 10.1016/j.medin.2011.10.005

Buffinton, 1992, Oxidative stress in lungs of mice infected with influenza A virus, Free Radic. Res. Commun., 16, 99, 10.3109/10715769209049163

Hennet, 1992, Alterations in antioxidant defences in lung and liver of mice infected with influenza A virus, J. Gen. Virol., 73, 39, 10.1099/0022-1317-73-1-39

Amatore, 2015, Influenza virus replication in lung epithelial cells depends on redox-sensitive pathways activated by NOX4-derived ROS, Cell. Microbiol., 17, 131, 10.1111/cmi.12343

Ye, 2015, Inhibition of reactive oxygen species production ameliorates inflammation induced by influenza A viruses via upregulation of SOCS1 and SOCS3, J. Virol., 89, 2672, 10.1128/JVI.03529-14

Casola, 2001, Oxidant tone regulates RANTES gene expression in airway epithelial cells infected with respiratory syncytial virus. Role in viral-induced interferon regulatory factor activation, J. Biol. Chem., 276, 19715, 10.1074/jbc.M101526200

Martinez, 2016, Induction of DNA double-strand breaks and cellular senescence by human respiratory syncytial virus, Virulence, 7, 427, 10.1080/21505594.2016.1144001

Gao, 2016, Inactivated Sendai virus induces apoptosis mediated by reactive oxygen species in murine melanoma cells, Biomed. Environ. Sci., 29, 877

Qian, 2018, Inactivated Sendai Virus Induces ROS-dependent Apoptosis and Autophagy in Human Prostate Cancer Cells, Biomed. Environ. Sci., 31, 280

2015, Oxidative Stress and Inflamatory Plasma Biomarkers in Respiratory Syncytial Virus Bronchiolitis, Clin. Respir. J., 11, 839

Akaike, 2003, 8-nitroguanosine formation in viral pneumonia and its implication for pathogenesis, Proc. Natl. Acad. Sci. USA, 100, 685, 10.1073/pnas.0235623100

Hosakote, 2011, Viral-mediated inhibition of antioxidant enzymes contributes to the pathogenesis of severe respiratory syncytial virus bronchiolitis, Am. J. Respir. Crit. Care Med., 183, 1550, 10.1164/rccm.201010-1755OC

Hosakote, 2009, Respiratory syncytial virus induces oxidative stress by modulating antioxidant enzymes, Am. J. Respir. Cell. Mol. Biol., 41, 348, 10.1165/rcmb.2008-0330OC

Jamaluddin, 2009, Respiratory syncytial virus infection induces a reactive oxygen species-MSK1-phospho-Ser-276 RelA pathway required for cytokine expression, J. Virol., 83, 10605, 10.1128/JVI.01090-09

Mochizuki, 2009, RS virus-induced inflammation and the intracellular glutathione redox state in cultured human airway epithelial cells, Inflammation, 32, 252, 10.1007/s10753-009-9128-0

Bao, 2008, Identification of human metapneumovirus-induced gene networks in airway epithelial cells by microarray analysis, Virology, 374, 114, 10.1016/j.virol.2007.12.024

Biagioli, 1999, The role of oxidative stress in rhinovirus induced elaboration of IL-8 by respiratory epithelial cells, Free Radic. Biol. Med., 26, 454, 10.1016/S0891-5849(98)00233-0

Papi, 2008, Role of xanthine oxidase activation and reduced glutathione depletion in rhinovirus induction of inflammation in respiratory epithelial cells, J. Biol. Chem., 283, 28595, 10.1074/jbc.M805766200

Kaul, 2000, Rhinovirus-induced oxidative stress and interleukin-8 elaboration involves p47-phox but is independent of attachment to intercellular adhesion molecule-1 and viral replication, J. Infect. Dis., 181, 1885, 10.1086/315504

Funchal, G.A., Jaeger, N., Czepielewski, R.S., Machado, M.S., Muraro, S.P., Stein, R.T., Bonorino, C.B., and Porto, B.N. (2015). Respiratory syncytial virus fusion protein promotes TLR-4-dependent neutrophil extracellular trap formation by human neutrophils. PLoS ONE, 10.

Segovia, J., Sabbah, A., Mgbemena, V., Tsai, S.Y., Chang, T.H., Berton, M.T., Morris, I.R., Allen, I.C., Ting, J.P., and Bose, S. (2012). TLR2/MyD88/NF-κB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS ONE, 7.

Altenhofer, 2015, Evolution of NADPH Oxidase Inhibitors: Selectivity and Mechanisms for Target Engagement, Antioxid. Redox Signal., 23, 406, 10.1089/ars.2013.5814

Vlahos, R., Stambas, J., Bozinovski, S., Broughton, B.R., Drummond, G.R., and Selemidis, S. (2011). Inhibition of Nox2 oxidase activity ameliorates influenza A virus-induced lung inflammation. PLoS Pathog., 7.

To, 2014, Influenza A virus and TLR7 activation potentiate NOX2 oxidase-dependent ROS production in macrophages, Free Radic. Res., 48, 940, 10.3109/10715762.2014.927579

To, 2017, Endosomal NOX2 oxidase exacerbates virus pathogenicity and is a target for antiviral therapy, Nat. Commun., 8, 69, 10.1038/s41467-017-00057-x

Fink, 2008, Dual role of NOX2 in respiratory syncytial virus- and sendai virus-induced activation of NF-κB in airway epithelial cells, J. Immunol., 180, 6911, 10.4049/jimmunol.180.10.6911

Snelgrove, 2006, An absence of reactive oxygen species improves the resolution of lung influenza infection, Eur. J. Immunol., 36, 1364, 10.1002/eji.200635977

Bedard, 2007, The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology, Physiol. Rev., 87, 245, 10.1152/physrev.00044.2005

Imai, 2008, Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury, Cell, 133, 235, 10.1016/j.cell.2008.02.043

Trocme, 2015, Macrophage-specific NOX2 contributes to the development of lung emphysema through modulation of SIRT1/MMP-9 pathways, J. Pathol., 235, 65, 10.1002/path.4423

Soucy-Faulkner, A., Mukawera, E., Fink, K., Martel, A., Jouan, L., Nzengue, Y., Lamarre, D., Vande Velde, C., and Grandvaux, N. (2010). Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression. PLoS Pathog., 6.

Grandvaux, 2015, Lung epithelial NOX/DUOX and respiratory virus infections, Clin. Sci. (Lond.), 128, 337, 10.1042/CS20140321

Van den Brand, J.M., Stittelaar, K.J., van Amerongen, G., Reperant, L., de Waal, L., Osterhaus, A.D., and Kuiken, T. (2012). Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian influenza H5N1 virus infections in ferrets. PLoS ONE, 7.

Camp, 2015, Lower Respiratory Tract Infection of the Ferret by 2009 H1N1 Pandemic Influenza A Virus Triggers Biphasic, Systemic, and Local Recruitment of Neutrophils, J. Virol., 89, 8733, 10.1128/JVI.00817-15

Geerdink, 2015, Neutrophils in respiratory syncytial virus infection: A target for asthma prevention, J. Allergy Clin. Immunol., 136, 838, 10.1016/j.jaci.2015.06.034

Kim, 2013, Reactive oxygen species induce antiviral innate immune response through IFN-λ regulation in human nasal epithelial cells, Am. J. Respir. Cell. Mol. Biol., 49, 855, 10.1165/rcmb.2013-0003OC

Selemidis, S., Seow, H.J., Broughton, B.R., Vinh, A., Bozinovski, S., Sobey, C.G., Drummond, G.R., and Vlahos, R. (2013). NOX1 oxidase suppresses influenza a virus-induced lung inflammation and oxidative stress. PLoS ONE, 8.

Hofstetter, A.R., De La Cruz, J.A., Cao, W., Patel, J., Belser, J.A., McCoy, J., Liepkalns, J.S., Amoah, S., Cheng, G., and Ranjan, P. (2016). NADPH Oxidase 1 Is Associated with Altered Host Survival and T Cell Phenotypes after Influenza A Virus Infection in Mice. PLoS ONE, 11.

Comstock, 2011, Rhinovirus-induced barrier dysfunction in polarized airway epithelial cells is mediated by NADPH oxidase 1, J. Virol., 85, 6795, 10.1128/JVI.02074-10

Unger, 2014, Nod-like receptor X-1 is required for rhinovirus-induced barrier dysfunction in airway epithelial cells, J. Virol., 88, 3705, 10.1128/JVI.03039-13

Tattoli, 2008, NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-κB and JNK pathways by inducing reactive oxygen species production, EMBO Rep., 9, 293, 10.1038/sj.embor.7401161

Surh, 2005, Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals, J. Nutr., 135, S2993, 10.1093/jn/135.12.2993S

Kim, 2015, The Induction of Pattern-Recognition Receptor Expression against Influenza A Virus through Duox2-Derived Reactive Oxygen Species in Nasal Mucosa, Am. J. Respir. Cell Mol. Biol., 53, 525, 10.1165/rcmb.2014-0334OC

Strengert, 2014, Mucosal reactive oxygen species are required for antiviral response: Role of Duox in influenza a virus infection, Antioxid. Redox Signal., 20, 2695, 10.1089/ars.2013.5353

Hong, 2016, Duox2 is required for the transcription of pattern recognition receptors in acute viral lung infection: An interferon-independent regulatory mechanism, Antivir. Res., 134, 1, 10.1016/j.antiviral.2016.08.017

Harper, 2005, Differential regulation of dual NADPH oxidases/peroxidases, Duox1 and Duox2, by Th1 and Th2 cytokines in respiratory tract epithelium, FEBS Lett., 579, 4911, 10.1016/j.febslet.2005.08.002

Schneider, 2010, Increased cytokine response of rhinovirus-infected airway epithelial cells in chronic obstructive pulmonary disease, Am. J. Respir. Crit. Care Med., 182, 332, 10.1164/rccm.200911-1673OC

Akaike, 1990, Dependence on O2− generation by xanthine oxidase of pathogenesis of influenza virus infection in mice, J. Clin. Investig., 85, 739, 10.1172/JCI114499

Oda, 1989, Oxygen radicals in influenza-induced pathogenesis and treatment with pyran polymer-conjugated SOD, Science, 244, 974, 10.1126/science.2543070

Kelley, 2013, Xanthine oxidoreductase-catalyzed reactive species generation: A process in critical need of reevaluation, Redox Biol., 1, 353, 10.1016/j.redox.2013.05.002

Kim, 2015, Mitochondrial reactive oxygen species modulate innate immune response to influenza A virus in human nasal epithelium, Antivir. Res., 119, 78, 10.1016/j.antiviral.2015.04.011

Dikalov, 2011, Cross talk between mitochondria and NADPH oxidases, Free Radic. Biol. Med., 51, 1289, 10.1016/j.freeradbiomed.2011.06.033

Daiber, 2017, Crosstalk of mitochondria with NADPH oxidase via reactive oxygen and nitrogen species signalling and its role for vascular function, Br. J. Pharmacol., 174, 1670, 10.1111/bph.13403

Bitzer, 2002, Caspase-8 and Apaf-1-independent caspase-9 activation in Sendai virus-infected cells, J. Biol. Chem., 277, 29817, 10.1074/jbc.M111898200

Sawa, 2003, Superoxide generation mediated by 8-nitroguanosine, a highly redox-active nucleic acid derivative, Biochem. Biophys. Res. Commun., 311, 300, 10.1016/j.bbrc.2003.10.003

Ivanov, 2016, Oxidative Stress during HIV Infection: Mechanisms and Consequences, Oxid. Med. Cell. Longev., 2016, 8910396, 10.1155/2016/8910396

Lazrak, 2009, Influenza virus M2 protein inhibits epithelial sodium channels by increasing reactive oxygen species, FASEB J., 23, 3829, 10.1096/fj.09-135590

Shin, 2015, Influenza A virus PB1-F2 is involved in regulation of cellular redox state in alveolar epithelial cells, Biochem. Biophys. Res. Commun., 459, 699, 10.1016/j.bbrc.2015.03.010

Flory, 2000, Influenza virus-induced NF-κB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IκB kinase, J. Biol. Chem., 275, 8307, 10.1074/jbc.275.12.8307

Lin, 2006, Severe acute respiratory syndrome coronavirus 3C-like protease-induced apoptosis, FEMS Immunol. Med. Microbiol., 46, 375, 10.1111/j.1574-695X.2006.00045.x

Nguyen, 2009, The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress, J. Biol. Chem., 284, 13291, 10.1074/jbc.R900010200

Kwak, 2002, Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: Role of antioxidant response element-like sequences in the nrf2 promoter, Mol. Cell. Biol., 22, 2883, 10.1128/MCB.22.9.2883-2892.2002

Manevich, 2009, Binding of peroxiredoxin 6 to substrate determines differential phospholipid hydroperoxide peroxidase and phospholipase A(2) activities, Arch. Biochem. Biophys., 485, 139, 10.1016/j.abb.2009.02.008

Yang, 2016, Ferroptosis: Death by Lipid Peroxidation, Trends Cell Biol., 26, 165, 10.1016/j.tcb.2015.10.014

Kosmider, 2012, Nrf2 protects human alveolar epithelial cells against injury induced by influenza A virus, Respir. Res., 13, 43, 10.1186/1465-9921-13-43

Yamada, Y., Limmon, G.V., Zheng, D., Li, N., Li, L., Yin, L., Chow, V.T., Chen, J., and Engelward, B.P. (2012). Major shifts in the spatio-temporal distribution of lung antioxidant enzymes during influenza pneumonia. PLoS ONE, 7.

Simon, 2015, Highly Pathogenic H5N1 and Novel H7N9 Influenza A Viruses Induce More Profound Proteomic Host Responses than Seasonal and Pandemic H1N1 Strains, J. Proteome Res., 14, 4511, 10.1021/acs.jproteome.5b00196

Jacoby, 1994, Influenza virus induces expression of antioxidant genes in human epithelial cells, Free Radic. Biol. Med., 16, 821, 10.1016/0891-5849(94)90198-8

Pyo, 2014, Alteration of copper-zinc superoxide dismutase 1 expression by influenza A virus is correlated with virus replication, Biochem. Biophys. Res. Commun., 450, 711, 10.1016/j.bbrc.2014.06.037

Lin, X., Wang, R., Zou, W., Sun, X., Liu, X., Zhao, L., Wang, S., and Jin, M. (2016). The Influenza Virus H5N1 Infection Can Induce ROS Production for Viral Replication and Host Cell Death in A549 Cells Modulated by Human Cu/Zn Superoxide Dismutase (SOD1) Overexpression. Viruses, 8.

Huang, Y., Zaas, A.K., Rao, A., Dobigeon, N., Woolf, P.J., Veldman, T., Oien, N.C., McClain, M.T., Varkey, J.B., and Nicholson, B. (2011). Temporal dynamics of host molecular responses differentiate symptomatic and asymptomatic influenza a infection. PLoS Genet., 7.

Soliman, 2010, Indoleamine 2,3-dioxygenase: Is it an immune suppressor?, Cancer J., 16, 354, 10.1097/PPO.0b013e3181eb3343

Choi, 1996, Oxidant stress responses in influenza virus pneumonia: Gene expression and transcription factor activation, Am. J. Physiol., 271, L383

Komaravelli, 2015, Respiratory syncytial virus infection down-regulates antioxidant enzyme expression by triggering deacetylation-proteasomal degradation of Nrf2, Free Radic. Biol. Med., 88, 391, 10.1016/j.freeradbiomed.2015.05.043

Cho, 2009, Antiviral activity of Nrf2 in a murine model of respiratory syncytial virus disease, Am. J. Respir. Crit. Care Med., 179, 138, 10.1164/rccm.200804-535OC

Garofalo, 2013, Respiratory syncytial virus infection: Mechanisms of redox control and novel therapeutic opportunities, Antioxid. Redox Signal., 18, 186, 10.1089/ars.2011.4307

Jamaluddin, 2010, Role of peroxiredoxin 1 and peroxiredoxin 4 in protection of respiratory syncytial virus-induced cysteinyl oxidation of nuclear cytoskeletal proteins, J. Virol., 84, 9533, 10.1128/JVI.01005-10

Hastie, 2012, The human respiratory syncytial virus nonstructural protein 1 regulates type I and type II interferon pathways, Mol. Cell. Proteom., 11, 108, 10.1074/mcp.M111.015909

Darville, 2000, NF-κB is required for cytokine-induced manganese superoxide dismutase expression in insulin-producing cells, Endocrinology, 141, 153, 10.1210/endo.141.1.7268

Kaul, 2002, Effect of rhinovirus challenge on antioxidant enzymes in respiratory epithelial cells, Free Radic. Res., 36, 1085, 10.1080/1071576021000028316

Ciriolo, 1997, Loss of GSH, oxidative stress, and decrease of intracellular pH as sequential steps in viral infection, J. Biol. Chem., 272, 2700, 10.1074/jbc.272.5.2700

Biswas, 2010, Role of Nrf1 in antioxidant response element-mediated gene expression and beyond, Toxicol. Appl. Pharmacol., 244, 16, 10.1016/j.taap.2009.07.034

Cai, 2003, Inhibition of influenza infection by glutathione, Free Radic. Biol. Med., 34, 928, 10.1016/S0891-5849(03)00023-6

Nencioni, 2003, Influenza A virus replication is dependent on an antioxidant pathway that involves GSH and Bcl-2, FASEB J., 17, 758, 10.1096/fj.02-0508fje

Kesic, 2011, Nrf2 expression modifies influenza A entry and replication in nasal epithelial cells, Free Radic. Biol. Med., 51, 444, 10.1016/j.freeradbiomed.2011.04.027

Pauli, E.K., Schmolke, M., Wolff, T., Viemann, D., Roth, J., Bode, J.G., and Ludwig, S. (2008). Influenza A virus inhibits type I IFN signaling via NF-κB-dependent induction of SOCS-3 expression. PLoS Pathog., 4.

Pinto, 2011, Inhibition of influenza virus-induced NF-κB and Raf/MEK/ERK activation can reduce both virus titers and cytokine expression simultaneously in vitro and in vivo, Antivir. Res., 92, 45, 10.1016/j.antiviral.2011.05.009

Hillesheim, 2014, β-catenin promotes the type I IFN synthesis and the IFN-dependent signaling response but is suppressed by influenza A virus-induced RIG-I/NF-κB signaling, Cell Commun. Signal., 12, 29, 10.1186/1478-811X-12-29

Gao, 2012, Influenza A virus-encoded NS1 virulence factor protein inhibits innate immune response by targeting IKK, Cell. Microbiol., 14, 1849, 10.1111/cmi.12005

Fink, 2013, IFNβ/TNFalpha synergism induces a non-canonical STAT2/IRF9-dependent pathway triggering a novel DUOX2 NADPH oxidase-mediated airway antiviral response, Cell. Res., 23, 673, 10.1038/cr.2013.47

Liu, 2004, Reactive oxygen species mediate virus-induced STAT activation: Role of tyrosine phosphatases, J. Biol. Chem., 279, 2461, 10.1074/jbc.M307251200

Yoboua, 2010, Respiratory syncytial virus-mediated NF-κB p65 phosphorylation at serine 536 is dependent on RIG-I, TRAF6, and IKKβ, J. Virol., 84, 7267, 10.1128/JVI.00142-10

Grandvaux, 2014, Sustained activation of interferon regulatory factor 3 during infection by paramyxoviruses requires MDA5, J. Innate Immun., 6, 650, 10.1159/000360764

Spann, 2005, Effects of nonstructural proteins NS1 and NS2 of human respiratory syncytial virus on interferon regulatory factor 3, NF-κB, and proinflammatory cytokines, J. Virol., 79, 5353, 10.1128/JVI.79.9.5353-5362.2005

Ren, 2011, A novel mechanism for the inhibition of interferon regulatory factor-3-dependent gene expression by human respiratory syncytial virus NS1 protein, J. Gen. Virol., 92, 2153, 10.1099/vir.0.032987-0

Barik, 2013, Respiratory syncytial virus mechanisms to interfere with type 1 interferons, Curr. Top. Microbiol. Immunol., 372, 173

Boyapalle, S., Wong, T., Garay, J., Teng, M., San Juan-Vergara, H., Mohapatra, S., and Mohapatra, S. (2012). Respiratory syncytial virus NS1 protein colocalizes with mitochondrial antiviral signaling protein MAVS following infection. PLoS ONE, 7.

Swedan, 2009, Respiratory syncytial virus nonstructural proteins decrease levels of multiple members of the cellular interferon pathways, J. Virol., 83, 9682, 10.1128/JVI.00715-09

Papi, 2002, Reducing agents inhibit rhinovirus-induced up-regulation of the rhinovirus receptor intercellular adhesion molecule-1 (ICAM-1) in respiratory epithelial cells, FASEB J., 16, 1934, 10.1096/fj.02-0118fje

Palamara, 1996, Cocaine increases Sendai virus replication in cultured epithelial cells: Critical role of the intracellular redox status, Biochem. Biophys. Res. Commun., 228, 579, 10.1006/bbrc.1996.1701

Horan, 2012, Mitochondria-derived reactive oxygen species negatively regulates immune innate signaling pathways triggered by a DNA virus, but not by an RNA virus, Biochem Biophys. Res. Commun., 418, 806, 10.1016/j.bbrc.2012.01.108

Vendemiale, 2001, Oxidative stress in symptom-free HCV carriers: Relation with ALT flare-up, Eur. J. Clin. Investig., 31, 54, 10.1046/j.1365-2362.2001.00747.x

Jain, 2002, Oxidative stress in chronic hepatitis C: Not just a feature of late stage disease, J. Hepatol., 36, 805, 10.1016/S0168-8278(02)00060-0

Bolukbas, C., Bolukbas, F.F., Horoz, M., Aslan, M., Celik, H., and Erel, O. (2005). Increased oxidative stress associated with the severity of the liver disease in various forms of hepatitis B virus infection. BMC Infect. Dis., 5.

Li, 2015, Influenza infection induces host DNA damage and dynamic DNA damage responses during tissue regeneration, Cell. Mol. Life Sci., 72, 2973, 10.1007/s00018-015-1879-1

Kash, 2014, Treatment with the reactive oxygen species scavenger EUK-207 reduces lung damage and increases survival during 1918 influenza virus infection in mice, Free Radic. Biol. Med., 67, 235, 10.1016/j.freeradbiomed.2013.10.014

Uchide, 2003, Antiviral function of pyrrolidine dithiocarbamate against influenza virus: The inhibition of viral gene replication and transcription, J. Antimicrob. Chemother., 52, 8, 10.1093/jac/dkg282

Yatmaz, 2013, Glutathione peroxidase-1 reduces influenza A virus-induced lung inflammation, Am. J. Respir. Cell Mol. Biol., 48, 17, 10.1165/rcmb.2011-0345OC

Jaspers, 2007, Selenium deficiency alters epithelial cell morphology and responses to influenza, Free Radic. Biol. Med., 42, 1826, 10.1016/j.freeradbiomed.2007.03.017

Zhang, 2007, SARS-CoV nucleocapsid protein induced apoptosis of COS-1 mediated by the mitochondrial pathway, Artif. Cells Blood Substit Immobil. Biotechnol., 35, 237, 10.1080/10731190601188422

Olsen, 1996, The influence of calcium and reactive oxygen species on influenza virus-induced apoptosis, Cell Death Differ., 3, 191

Blume, 2017, Cellular crosstalk between airway epithelial and endothelial cells regulates barrier functions during exposure to double-stranded RNA, Immun. Inflamm. Dis., 5, 45, 10.1002/iid3.139

Moldoveanu, 2009, Inflammatory mechanisms in the lung, J. Inflamm. Res., 2, 1

Go, Y.M., Kang, S.M., Roede, J.R., Orr, M., and Jones, D.P. (2011). Increased inflammatory signaling and lethality of influenza H1N1 by nuclear thioredoxin-1. PLoS ONE, 6.

Mastronarde, 1995, Oxidant tone regulates IL-8 production in epithelium infected with respiratory syncytial virus, Am. J. Respir. Cell. Mol. Biol., 13, 237, 10.1165/ajrcmb.13.2.7626291

Tisoncik, 2012, Into the eye of the cytokine storm, Microbiol. Mol. Biol. Rev., 76, 16, 10.1128/MMBR.05015-11

Wong, 2009, Roles of NF-κB in health and disease: Mechanisms and therapeutic potential, Clin. Sci. (Lond.), 116, 451, 10.1042/CS20080502

Mata, 2011, 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., 82, 548, 10.1016/j.bcp.2011.05.014

Mastronarde, 1998, Activator protein-1 is the preferred transcription factor for cooperative interaction with nuclear factor-κB in respiratory syncytial virus-induced interleukin-8 gene expression in airway epithelium, J. Infect. Dis., 177, 1275, 10.1086/515279

Kim, 2000, Role of NF-κB in cytokine production induced from human airway epithelial cells by rhinovirus infection, J. Immunol., 165, 3384, 10.4049/jimmunol.165.6.3384

Bao, 2008, Human metapneumovirus small hydrophobic protein inhibits NF-κB transcriptional activity, J. Virol., 82, 8224, 10.1128/JVI.02584-07

Carpenter, L.R., Moy, J.N., and Roebuck, K.A. (2002). Respiratory syncytial virus and TNF alpha induction of chemokine gene expression involves differential activation of Rel A and NF-κB1. BMC Infect. Dis., 2.

Indukuri, 2006, Ikkepsilon regulates viral-induced interferon regulatory factor-3 activation via a redox-sensitive pathway, Virology, 353, 155, 10.1016/j.virol.2006.05.022

Hosakote, 2016, Respiratory Syncytial Virus Infection Triggers Epithelial HMGB1 Release as a Damage-Associated Molecular Pattern Promoting a Monocytic Inflammatory Response, J. Virol., 90, 9618, 10.1128/JVI.01279-16

Ren, 2016, Suppression of IRG-1 Reduces Inflammatory Cell Infiltration and Lung Injury in Respiratory Syncytial Virus Infection by Reducing Production of Reactive Oxygen Species, J. Virol., 90, 7313, 10.1128/JVI.00563-16

Michelucci, 2013, Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production, Proc. Natl. Acad. Sci. USA, 110, 7820, 10.1073/pnas.1218599110

Liu, 2017, IRG1 increases MHC class I level in macrophages through STAT-TAP1 axis depending on NADPH oxidase mediated reactive oxygen species, Int. Immunopharmacol., 48, 76, 10.1016/j.intimp.2017.04.012

Lampropoulou, 2016, Itaconate Links Inhibition of Succinate Dehydrogenase with Macrophage Metabolic Remodeling and Regulation of Inflammation, Cell Metab., 24, 158, 10.1016/j.cmet.2016.06.004

Mills, 2018, Itaconate is an anti-inflammatory metabolite that activates Nrf2 via alkylation of KEAP1, Nature, 556, 113, 10.1038/nature25986

Latz, 2013, Activation and regulation of the inflammasomes, Nat. Rev. Immunol., 13, 397, 10.1038/nri3452

Schroder, 2010, The inflammasomes, Cell, 140, 821, 10.1016/j.cell.2010.01.040

Harijith, 2014, Reactive oxygen species at the crossroads of inflammasome and inflammation, Front. Physiol., 5, 352, 10.3389/fphys.2014.00352

Allen, 2009, The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA, Immunity, 30, 556, 10.1016/j.immuni.2009.02.005

Ichinohe, 2013, Mitochondrial protein mitofusin 2 is required for NLRP3 inflammasome activation after RNA virus infection, Proc. Natl. Acad. Sci. USA, 110, 17963, 10.1073/pnas.1312571110

Triantafilou, 2013, Rhinovirus-induced calcium flux triggers NLRP3 and NLRC5 activation in bronchial cells, Am. J. Respir. Cell Mol. Biol., 49, 923, 10.1165/rcmb.2013-0032OC

Torres, 2015, Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome, Virology, 485, 330, 10.1016/j.virol.2015.08.010

Mekahli, 2011, Endoplasmic-reticulum calcium depletion and disease, Cold Spring Harb. Perspect. Biol., 3, a004317, 10.1101/cshperspect.a004317

Marciniak, 2006, Endoplasmic reticulum stress signaling in disease, Physiol. Rev., 86, 1133, 10.1152/physrev.00015.2006

Darling, 2014, The role of MAPK signalling pathways in the response to endoplasmic reticulum stress, Biochim. Biophys. Acta, 1843, 2150, 10.1016/j.bbamcr.2014.01.009

Newton, 2012, Signaling in innate immunity and inflammation, Cold Spring Harb. Perspect. Biol., 4, a006049, 10.1101/cshperspect.a006049

Roberson, 2012, Influenza induces endoplasmic reticulum stress, caspase-12-dependent apoptosis, and c-Jun N-terminal kinase-mediated transforming growth factor-β release in lung epithelial cells, Am. J. Respir. Cell Mol. Biol., 46, 573, 10.1165/rcmb.2010-0460OC

Sajjan, 2008, Rhinovirus disrupts the barrier function of polarized airway epithelial cells, Am. J. Respir. Crit. Care Med., 178, 1271, 10.1164/rccm.200801-136OC

Rezaee, 2013, Sustained protein kinase D activation mediates respiratory syncytial virus-induced airway barrier disruption, J. Virol., 87, 11088, 10.1128/JVI.01573-13

Waldron, 2004, Oxidative stress induces protein kinase C-mediated activation loop phosphorylation and nuclear redistribution of protein kinase D, J. Biol. Chem., 279, 27482, 10.1074/jbc.M402875200

Waldron, 2000, Oxidative stress induces protein kinase D activation in intact cells. Involvement of Src and dependence on protein kinase C, J. Biol. Chem., 275, 17114, 10.1074/jbc.M908959199

Wu, 2016, The differentiated airway epithelium infected by influenza viruses maintains the barrier function despite a dramatic loss of ciliated cells, Sci. Rep., 6, 39668, 10.1038/srep39668

Short, 2016, Influenza virus damages the alveolar barrier by disrupting epithelial cell tight junctions, Eur. Respir. J., 47, 954, 10.1183/13993003.01282-2015

Gotts, 2014, Influenza causes prolonged disruption of the alveolar-capillary barrier in mice unresponsive to mesenchymal stem cell therapy, Am. J. Physiol. Lung Cell. Mol. Physiol., 307, L395, 10.1152/ajplung.00110.2014

Sun, 2016, Nox2-derived oxidative stress results in inefficacy of antibiotics against post-influenza S. aureus pneumonia, J. Exp. Med., 213, 1851, 10.1084/jem.20150514

Harrison, 2013, Targeting the “cytokine storm” for therapeutic benefit, Clin. Vaccine Immunol., 20, 319, 10.1128/CVI.00636-12

Komaravelli, 2014, Respiratory Viral Infections and Subversion of Cellular Antioxidant Defenses, J. Pharmacogenomics Pharmacoproteomics, 5, 1000141

Uchide, 2011, Antioxidant therapy as a potential approach to severe influenza-associated complications, Molecules, 16, 2032, 10.3390/molecules16032032

Sgarbanti, 2014, Intracellular redox state as target for anti-influenza therapy: Are antioxidants always effective?, Curr. Top. Med. Chem., 14, 2529, 10.2174/1568026614666141203125211

Bonville, 2003, Replication of respiratory syncytial virus is inhibited in target cells generating nitric oxide in situ, Front. Biosci., 8, a48, 10.2741/986

Stark, 2005, Immune and functional role of nitric oxide in a mouse model of respiratory syncytial virus infection, J. Infect. Dis., 191, 387, 10.1086/427241

Bazhanov, 2017, Hydrogen Sulfide: A Novel Player in Airway Development, Pathophysiology of Respiratory Diseases, and Antiviral Defenses, Am. J. Respir. Cell. Mol. Biol., 57, 403, 10.1165/rcmb.2017-0114TR

Li, 2015, Role of hydrogen sulfide in paramyxovirus infections, J. Virol., 89, 5557, 10.1128/JVI.00264-15

Vlahos, 2014, NADPH oxidases as novel pharmacologic targets against influenza A virus infection, Mol. Pharmacol., 86, 747, 10.1124/mol.114.095216

Vlahos, 2012, Suppressing production of reactive oxygen species (ROS) for influenza A virus therapy, Trends Pharmacol. Sci., 33, 3, 10.1016/j.tips.2011.09.001

Geiler, 2010, N-acetyl-l-cysteine (NAC) inhibits virus replication and expression of pro-inflammatory molecules in A549 cells infected with highly pathogenic H5N1 influenza A virus, Biochem. Pharmacol., 79, 413, 10.1016/j.bcp.2009.08.025

Ghezzi, 2004, Synergistic combination of N-acetylcysteine and ribavirin to protect from lethal influenza viral infection in a mouse model, Int. J. Immunopathol. Pharmacol., 17, 99, 10.1177/039463200401700114

Garozzo, 2007, N-acetylcysteine synergizes with oseltamivir in protecting mice from lethal influenza infection, Int. J. Immunopathol. Pharmacol., 20, 349, 10.1177/039463200702000215

Grassi, 1997, Attenuation of influenza-like symptomatology and improvement of cell-mediated immunity with long-term N-acetylcysteine treatment, Eur. Respir. J., 10, 1535, 10.1183/09031936.97.10071535

Mata, M., Sarrion, I., Armengot, M., Carda, C., Martinez, I., Melero, J.A., and Cortijo, J. (2012). Respiratory syncytial virus inhibits ciliagenesis in differentiated normal human bronchial epithelial cells: Effectiveness of N-acetylcysteine. PLoS ONE, 7.

Wiesener, 2011, Therapy of experimental influenza virus infection with pyrrolidine dithiocarbamate, Med. Microbiol. Immunol., 200, 115, 10.1007/s00430-010-0182-x

Castro, 2006, Antioxidant treatment ameliorates respiratory syncytial virus-induced disease and lung inflammation, Am. J. Respir. Crit. Care Med., 174, 1361, 10.1164/rccm.200603-319OC

Serkedjieva, 2003, Combined protective effect of a fungal Cu/Zn-containing superoxide dismutase and rimantadine hydrochloride in experimental murine influenza a virus infection, Acta Virol., 47, 53

Wyde, 1996, Recombinant superoxide dismutase (SOD) administered by aerosol inhibits respiratory syncytial virus infection in cotton rats, Antivir. Res., 31, 173, 10.1016/0166-3542(95)06967-4

Sidwell, 1996, Inhibitory effects of recombinant manganese superoxide dismutase on influenza virus infections in mice, Antimicrob. Agents Chemother., 40, 2626, 10.1128/AAC.40.11.2626

Suliman, 2001, Prevention of influenza-induced lung injury in mice overexpressing extracellular superoxide dismutase, Am. J. Physiol. Lung Cell. Mol. Physiol., 280, L69, 10.1152/ajplung.2001.280.1.L69

Mata, M., Martinez, I., Melero, J.A., Tenor, H., and Cortijo, J. (2013). Roflumilast inhibits respiratory syncytial virus infection in human differentiated bronchial epithelial cells. PLoS ONE, 8.

Yamaya, 2010, Inhibitory effects of carbocisteine on type A seasonal influenza virus infection in human airway epithelial cells, Am. J. Physiol. Lung Cell. Mol. Physiol., 299, L160, 10.1152/ajplung.00376.2009

Asada, 2012, l-carbocisteine inhibits respiratory syncytial virus infection in human tracheal epithelial cells, Respir. Physiol. Neurobiol., 180, 112, 10.1016/j.resp.2011.10.017

Furuya, 2008, Antiviral effects of ascorbic and dehydroascorbic acids in vitro, Int. J. Mol. Med., 22, 541

Kim, 2013, Vitamin C Is an Essential Factor on the Anti-viral Immune Responses through the Production of Interferon-α/β at the Initial Stage of Influenza A Virus (H3N2) Infection, Immune Netw., 13, 70, 10.4110/in.2013.13.2.70

Cai, 2015, A new mechanism of vitamin C effects on A/FM/1/47(H1N1) virus-induced pneumonia in restraint-stressed mice, Biomed. Res. Int., 2015, 675149, 10.1155/2015/675149

Yang, 2002, Ambroxol suppresses influenza-virus proliferation in the mouse airway by increasing antiviral factor levels, Eur. Respir. J., 19, 952, 10.1183/09031936.02.00253302

Palamara, 2005, Inhibition of influenza A virus replication by resveratrol, J. Infect. Dis., 191, 1719, 10.1086/429694

Xie, 2012, Resveratrol Inhibits respiratory syncytial virus-induced IL-6 production, decreases viral replication, and downregulates TRIF expression in airway epithelial cells, Inflammation, 35, 1392, 10.1007/s10753-012-9452-7

Zang, 2011, Resveratrol-mediated gamma interferon reduction prevents airway inflammation and airway hyperresponsiveness in respiratory syncytial virus-infected immunocompromised mice, J. Virol., 85, 13061, 10.1128/JVI.05869-11

Uchide, 2002, Effect of antioxidants on apoptosis induced by influenza virus infection: Inhibition of viral gene replication and transcription with pyrrolidine dithiocarbamate, Antivir. Res., 56, 207, 10.1016/S0166-3542(02)00109-2

Mileva, 2002, Effect of vitamin E supplementation on lipid peroxidation in blood and lung of influenza virus infected mice, Comp. Immunol. Microbiol. Infect. Dis., 25, 1, 10.1016/S0147-9571(01)00010-8

Hayek, 1997, Vitamin E supplementation decreases lung virus titers in mice infected with influenza, J. Infect. Dis., 176, 273, 10.1086/517265

Shi, 2014, Ability of recombinant human catalase to suppress inflammation of the murine lung induced by influenza A, Inflammation, 37, 809, 10.1007/s10753-013-9800-2

Shi, 2010, Therapeutic effect of recombinant human catalase on H1N1 influenza-induced pneumonia in mice, Inflammation, 33, 166, 10.1007/s10753-009-9170-y

Gaudernak, 2002, Antiviral effects of pyrrolidine dithiocarbamate on human rhinoviruses, J. Virol., 76, 6004, 10.1128/JVI.76.12.6004-6015.2002

Krenn, 2005, Inhibition of polyprotein processing and RNA replication of human rhinovirus by pyrrolidine dithiocarbamate involves metal ions, J. Virol., 79, 13892, 10.1128/JVI.79.22.13892-13899.2005

Yasuda, 2006, Carbocisteine inhibits rhinovirus infection in human tracheal epithelial cells, Eur. Respir. J., 28, 51, 10.1183/09031936.06.00058505

Yamaya, 2014, Ambroxol inhibits rhinovirus infection in primary cultures of human tracheal epithelial cells, Arch. Pharm. Res., 37, 520, 10.1007/s12272-013-0210-7