Respiratory syncytial virus and cellular stress responses: Impact on replication and physiopathology

Viruses

Volumn 8, Issue 5, 2016, Pages

  Cervantes Ortiz, Sandra L ^a   Cuervo, Natalia Zamorano ^a   Grandvaux, Nathalie ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Endoplasmic reticulum; ER stress; Inclusion bodies; Oxidative stress; Reactive oxygen species; Respiratory syncytial virus; RSV; Stress granule; Stress response; Virus

Indexed keywords

4 HYDROXYNONENAL; GLUTATHIONE TRANSFERASE; HN PROTEIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; X BOX BINDING PROTEIN 1; ANTIOXIDANT;

CELL STRESS; CELLULAR STRESS RESPONSE; ENDOPLASMIC RETICULUM; GENE EXPRESSION; HUMAN; HUMAN RESPIRATORY SYNCYTIAL VIRUS; OXIDATIVE STRESS; PARAMYXOVIRIDAE; PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; RNA TRANSLATION; SARS CORONAVIRUS; SENDAI VIRUS; UNFOLDED PROTEIN RESPONSE; VIRUS REPLICATION; ANIMAL; CELL GRANULE; ENDOPLASMIC RETICULUM STRESS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; ANTIOXIDANTS; CYTOPLASMIC GRANULES; ENDOPLASMIC RETICULUM STRESS; HOST-PATHOGEN INTERACTIONS; HUMANS; REACTIVE OXYGEN SPECIES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE; VIRUS REPLICATION;

EID: 84969524031     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8050124     Document Type: Review

References (95)

1. Russell, C.J.; Hurwitz, J.L. Sendai virus as a backbone for vaccines against rsv and other human paramyxoviruses. Expert Rev. Vaccines 2016, 15, 189-200
2. Palgen, J.L.; Jurgens, E.M.; Moscona, A.; Porotto, M.; Palermo, L.M. Unity in diversity: Shared mechanism of entry among paramyxoviruses. Prog. Mol. Biol. Transl. Sci. 2015, 129, 1-32
3. Collins, P.L.; Melero, J.A. Progress in understanding and controlling respiratory syncytial virus: Still crazy after all these years. Virus Res. 2011, 162, 80-99
4. Pickles, R.J.; DeVincenzo, J.P. Respiratory syncytial virus (rsv) and its propensity for causing bronchiolitis. J. Pathol. 2015, 235, 266-276
5. Krilov, L.R. Respiratory syncytial virus disease: Update on treatment and prevention. Expert Rev. Anti Infect. Ther. 2011, 9, 27-32
6. Lay, M.K.; Gonzalez, P.A.; Leon, M.A.; Cespedes, P.F.; Bueno, S.M.; Riedel, C.A.; Kalergis, A.M. Advances in understanding respiratory syncytial virus infection in airway epithelial cells and consequential effects on the immune response. Microbes Infect. 2013, 15, 230-242
7. De Graaff, P.M.; de Jong, E.C.; van Capel, T.M.; van Dijk, M.E.; Roholl, P.J.; Boes, J.; Luytjes, W.; Kimpen, J.L.; van Bleek, G.M. Respiratory syncytial virus infection of monocyte-derived dendritic cells decreases their capacity to activate cd4 t cells. J. Immunol. 2005, 175, 5904-5911
8. Dakhama, A.; Kaan, P.M.; Hegele, R.G. Permissiveness of guinea pig alveolar macrophage subpopulations to acute respiratory syncytial virus infection in vitro. Chest 1998, 114, 1681-1688
9. Guerrero-Plata, A.; Casola, A.; Suarez, G.; Yu, X.; Spetch, L.; Peeples, M.E.; Garofalo, R.P. Differential response of dendritic cells to human metapneumovirus and respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 2006, 34, 320-329
10. Johnson, T.R.; Johnson, C.N.; Corbett, K.S.; Edwards, G.C.; Graham, B.S. Primary human mdc1, mdc2, and pdc dendritic cells are differentially infected and activated by respiratory syncytial virus. PLoS ONE 2011, 6, e16458
11. Noton, S.L.; Fearns, R. Initiation and regulation of paramyxovirus transcription and replication. Virology 2015, 479-480, 545-554
12. Lamb, R.A.; Parks, G.D. Paramyxoviridae: The Viruses and Their Replication, 5th ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; pp. 1449-1496.
13. Tayyari, F.; Marchant, D.; Moraes, T.J.; Duan, W.; Mastrangelo, P.; Hegele, R.G. Identification of nucleolin as a cellular receptor for human respiratory syncytial virus. Nat. Med. 2011, 17, 1132-1135
14. Krzyzaniak, M.A.; Zumstein, M.T.; Gerez, J.A.; Picotti, P.; Helenius, A. Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the f protein. PLoS Pathog. 2013, 9, e1003309
15. Marr, N.; Turvey, S.E.; Grandvaux, N. Pathogen recognition receptor crosstalk in respiratory syncytial virus sensing: A host and cell type perspective. Trends Microbiol. 2013, 21, 568-574
16. Walsh, D.; Mathews, M.B.; Mohr, I. Tinkering with translation: Protein synthesis in virus-infected cells. Cold Spring Harb. Perspect. Biol. 2013, 5, a012351
17. Levine, S.; Peeples, M.; Hamilton, R. Effect of respiratory syncytial virus infection of hela-cell macromolecular synthesis. J. Gen. Virol. 1977, 37, 53-63
18. Barik, S. Respiratory syncytial virus mechanisms to interfere with type 1 interferons. Curr. Top. Microbiol. Immunol. 2013, 372, 173-191
19. Ellgaard, L.; Helenius, A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 2003, 4, 181-191
20. Walter, P.; Ron, D. The unfolded protein response: From stress pathway to homeostatic regulation. Science 2011, 334, 1081-1086
21. Byun, H.; Gou, Y.; Zook, A.; Lozano, M.M.; Dudley, J.P. Erad and how viruses exploit it. Front. Microbiol. 2014, 5, 330
22. Jheng, J.R.; Ho, J.Y.; Horng, J.T. Er stress, autophagy, and rna viruses. Front. Microbiol. 2014, 5, 388
23. Zhang, L.; Wang, A. Virus-induced er stress and the unfolded protein response. Front. Plant Sci. 2012, 3, 293
24. Bitko, V.; Barik, S. An endoplasmic reticulum-specific stress-activated caspase (caspase-12) is implicated in the apoptosis of a549 epithelial cells by respiratory syncytial virus. J. Cell. Biochem. 2001, 80, 441-454
25. Hassan, I.; Gaines, K.S.; Hottel, W.J.; Wishy, R.M.; Miller, S.E.; Powers, L.S.; Rutkowski, D.T.; Monick, M.M. Inositol-requiring enzyme 1 inhibits respiratory syncytial virus replication. J. Biol. Chem. 2014, 289, 7537-7546
26. Chatel-Chaix, L.; Bartenschlager, R. Dengue virus- and hepatitis c virus-induced replication and assembly compartments: The enemy inside-Caught in the web. J. Virol. 2014, 88, 5907-5911
27. Vasallo, C.; Gastaminza, P. Cellular stress responses in hepatitis c virus infection: Mastering a two-edged sword. Virus Res. 2015, 209, 100-117
28. Garcia, J.; Garcia-Barreno, B.; Vivo, A.; Melero, J.A. Cytoplasmic inclusions of respiratory syncytial virus-infected cells: Formation of inclusion bodies in transfected cells that coexpress the nucleoprotein, the phosphoprotein, and the 22k protein. Virology 1993, 195, 243-247
29. Collins, P.L.; Graham, B.S. Viral and host factors in human respiratory syncytial virus pathogenesis. J. Virol. 2008, 82, 2040-2055
30. Panda, S.; Mohakud, N.K.; Pena, L.; Kumar, S. Human metapneumovirus: Review of an important respiratory pathogen. Int. J. Infect. Dis. 2014, 25, 45-52
31. Lindquist, M.E.; Lifland, A.W.; Utley, T.J.; Santangelo, P.J.; Crowe, J.E., Jr. Respiratory syncytial virus induces host rna stress granules to facilitate viral replication. J. Virol. 2010, 84, 12274-12284
32. He, B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Diff. 2006, 13, 393-403
33. Collins, P.L. Oglycosylation of glycoprotein g of human respiratory syncytial virus is specified within the divergent ectodomain. J. Virol. 1990, 64, 4007-4012
34. Rixon, H.W.; Brown, G.; Aitken, J.; McDonald, T.; Graham, S.; Sugrue, R.J. The small hydrophobic (sh) protein accumulates within lipid-raft structures of the golgi complex during respiratory syncytial virus infection. J. Gen. Virol. 2004, 85, 1153-1165
35. Batonick, M.; Wertz, G.W. Requirements for human respiratory syncytial virus glycoproteins in assembly and egress from infected cells. Adv. Virol. 2011, 2011
36. Kwilas, S.; Liesman, R.M.; Zhang, L.; Walsh, E.; Pickles, R.J.; Peeples, M.E. Respiratory syncytial virus grown in vero cells contains a truncated attachment protein that alters its infectivity and dependence on glycosaminoglycans. J. Virol. 2009, 83, 10710-10718
37. Brock, S.C.; Goldenring, J.R.; Crowe, J.E., Jr. Apical recycling systems regulate directional budding of respiratory syncytial virus from polarized epithelial cells. Proc. Natl. Acad. Sci. USA 2003, 100, 15143-15148
38. Anderson, K.; Stott, E.J.; Wertz, G.W. Intracellular processing of the human respiratory syncytial virus fusion glycoprotein: Amino acid substitutions affecting folding, transport and cleavage. J. Gen. Virol. 1992, 73 Pt 5, 1177-1188
39. Ng, D.T.; Randall, R.E.; Lamb, R.A. Intracellular maturation and transport of the sv5 type ii glycoprotein hemagglutinin-neuraminidase: Specific and transient association with grp78-bip in the endoplasmic reticulum and extensive internalization from the cell surface. J. Cell Biol. 1989, 109, 3273-3289
40. Fung, T.S.; Torres, J.; Liu, D.X. The emerging roles of viroporins in er stress response and autophagy induction during virus infection. Viruses 2015, 7, 2834-2857
41. Minakshi, R.; Padhan, K.; Rani, M.; Khan, N.; Ahmad, F.; Jameel, S. The sars coronavirus 3a protein causes endoplasmic reticulum stress and induces ligand-independent downregulation of the type 1 interferon receptor. PLoS ONE 2009, 4, e8342
42. DeDiego, M.L.; Nieto-Torres, J.L.; Jiménez-Guardeño, J.M.; Regla-Nava, J.A.; Álvarez, E.; Oliveros, J.C.; Zhao, J.; Fett, C.; Perlman, S.; Enjuanes, L. Severe acute respiratory syndrome coronavirus envelope protein regulates cell stress response and apoptosis. PLoS Pathog. 2011, 7, e1002315
43. Carter, S.D.; Dent, K.C.; Atkins, E.; Foster, T.L.; Verow, M.; Gorny, P.; Harris, M.; Hiscox, J.A.; Ranson, N.A.; Griffin, S.; et al. Direct visualization of the small hydrophobic protein of human respiratory syncytial virus reveals the structural basis for membrane permeability. FEBS Lett. 2010, 584, 2786-2790
44. Triantafilou, K.; Kar, S.; Vakakis, E.; Kotecha, S.; Triantafilou, M. Human respiratory syncytial virus viroporin sh: A viral recognition pathway used by the host to signal inflammasome activation. Thorax 2013, 68, 66-75
45. Fuentes, S.; Tran, K.C.; Luthra, P.; Teng, M.N.; He, B. Function of the respiratory syncytial virus small hydrophobic protein. J. Virol. 2007, 81, 8361-8366
46. Yu, C.; Achazi, K.; Niedrig, M. Tick-borne encephalitis virus triggers inositol-requiring enzyme 1 (ire1) and transcription factor 6 (atf6) pathways of unfolded protein response. Virus Res. 2013, 178, 471-477
47. Hassan, I.H.; Zhang, M.S.; Powers, L.S.; Shao, J.Q.; Baltrusaitis, J.; Rutkowski, D.T.; Legge, K.; Monick, M.M. Influenza a viral replication is blocked by inhibition of the inositol-requiring enzyme 1 (ire1) stress pathway. J. Biol. Chem. 2012, 287, 4679-4689
48. Hollien, J.; Lin, J.H.; Li, H.; Stevens, N.; Walter, P.; Weissman, J.S. Regulated ire1-dependent decay of messenger rnas in mammalian cells. J. Cell Biol. 2009, 186, 323-331
49. Darling, N.J.; Cook, S.J. The role of mapk signalling pathways in the response to endoplasmic reticulum stress. Biochim. Biophys. Acta 2014, 1843, 2150-2163
50. Reed, M.; Morris, S.H.; Owczarczyk, A.B.; Lukacs, N.W. Deficiency of autophagy protein map1-lc3b mediates il-17-dependent lung pathology during respiratory viral infection via er stress-associated il-1. Mucosal Immunol. 2015, 8, 1118-1130
51. Kedersha, N.; Ivanov, P.; Anderson, P. Stress granules and cell signaling: More than just a passing phase? Trends Biochem. Sci. 2013, 38
52. White, J.P.; Lloyd, R.E. Regulation of stress granules in virus systems. Trends Microbiol. 2012, 20, 175-183
53. Onomoto, K.; Yoneyama, M.; Fung, G.; Kato, H.; Fujita, T. Antiviral innate immunity and stress granule responses. Trends Immunol. 2014, 35, 420-428
54. Iseni, F.; Garcin, D.; Nishio, M.; Kedersha, N.; Anderson, P.; Kolakofsky, D. Sendai virus trailer rna binds tiar, a cellular protein involved in virus-induced apoptosis. Embo J. 2002, 21, 5141-5150
55. Okonski, K.M.; Samuel, C.E. Stress granule formation induced by measles virus is protein kinase pkr dependent and impaired by rna adenosine deaminase adar1. J. Virol. 2013, 87, 756-766
56. Lindquist, M.E.; Mainou, B.A.; Dermody, T.S.; Crowe, J.E., Jr. Activation of protein kinase r is required for induction of stress granules by respiratory syncytial virus but dispensable for viral replication. Virology 2011, 413, 103-110
57. Hanley, L.L.; McGivern, D.R.; Teng, M.N.; Djang, R.; Collins, P.L.; Fearns, R. Roles of the respiratory syncytial virus trailer region: Effects of mutations on genome production and stress granule formation. Virology 2010, 406, 241-252
58. Fricke, J.; Koo, L.Y.; Brown, C.R.; Collins, P.L. P38 and ogt sequestration into viral inclusion bodies in cells infected with human respiratory syncytial virus suppresses mk2 activities and stress granule assembly. J. Virol. 2013, 87, 1333-1347
59. Groskreutz, D.J.; Babor, E.C.; Monick, M.M.; Varga, S.M.; Hunninghake, G.W. Respiratory syncytial virus limits alpha subunit of eukaryotic translation initiation factor 2 (eif2alpha) phosphorylation to maintain translation and viral replication. J. Biol. Chem. 2010, 285, 24023-24031
60. Emara, M.M.; Brinton, M.A. Interaction of tia-1/tiar with west nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc. Natl. Acad. Sci. USA 2007, 104, 9041-9046
61. Takeuchi, K.; Komatsu, T.; Kitagawa, Y.; Sada, K.; Gotoh, B. Sendai virus c protein plays a role in restricting pkr activation by limiting the generation of intracellular double-stranded rna. J. Virol. 2008, 82, 10102-10110
62. Chambers, R.; Takimoto, T. Antagonism of innate immunity by paramyxovirus accessory proteins. Viruses 2009, 1, 574-593
63. Yoshida, A.; Kawabata, R.; Honda, T.; Tomonaga, K.; Sakaguchi, T.; Irie, T. Ifn-beta-inducing, unusual viral rna species produced by paramyxovirus infection accumulated into distinct cytoplasmic structures in an rna-type-dependent manner. Front. Microbiol. 2015, 6, 804
64. Santangelo, P.J.; Lifland, A.W.; Curt, P.; Sasaki, Y.; Bassell, G.J.; Lindquist, M.E.; Crowe, J.E., Jr. Single molecule-sensitive probes for imaging rna in live cells. Nat. Methods 2009, 6, 347-349
65. Carromeu, C.; Simabuco, F.M.; Tamura, R.E.; Farinha Arcieri, L.E.; Ventura, A.M. Intracellular localization of human respiratory syncytial virus l protein. Arch. Virol. 2007, 152, 2259-2263
66. Ohn, T.; Kedersha, N.; Hickman, T.; Tisdale, S.; Anderson, P. A functional rnai screen links o-glcnac modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 2008, 10, 1224-1231
67. Lifland, A.W.; Jung, J.; Alonas, E.; Zurla, C.; Crowe, J.E., Jr.; Santangelo, P.J. Human respiratory syncytial virus nucleoprotein and inclusion bodies antagonize the innate immune response mediated by mda5 and mavs. J. Virol. 2012, 86, 8245-8258
68. Grandvaux, N.; Mariani, M.; Fink, K. Lung epithelial nox/duox and respiratory virus infections. Clin. Sci. 2015, 128, 337-347
69. MacNee, W. Oxidative stress and lung inflammation in airways disease. Eur. J. Pharmacol. 2001, 429, 195-207
70. Chow, C.W.; Herrera Abreu, M.T.; Suzuki, T.; Downey, G.P. Oxidative stress and acute lung injury. Am. J. Respir. Cell Mol. Biol. 2003, 29, 427-431
71. Reshi, M.L.; Su, Y.C.; Hong, J.R. Rna viruses: Ros-mediated cell death. Int. J. Cell Biol. 2014, 2014, 467452
72. Castro, S.M.; Guerrero-Plata, A.; Suarez-Real, G.; Adegboyega, P.A.; Colasurdo, G.N.; Khan, A.M.; Garofalo, R.P.; Casola, A. Antioxidant treatment ameliorates respiratory syncytial virus-induced disease and lung inflammation. Am. J. Respir. Crit. Care Med. 2006, 174, 1361-1369
73. Hosakote, Y.M.; Jantzi, P.D.; Esham, D.L.; Spratt, H.; Kurosky, A.; Casola, A.; Garofalo, R.P. Viral-mediated inhibition of antioxidant enzymes contributes to the pathogenesis of severe respiratory syncytial virus bronchiolitis. Am. J. Respir. Crit. Care Med. 2011, 183, 1550-1560
74. Moreno-Solis, G.; de la Torre-Aguilar, M.J.; Torres-Borrego, J.; Llorente-Cantarero, F.J.; Gil-Campos, M.; Fernandez-Gutierrez, F.; Tunez-Finana, I.; Perez-Navero, J.L. Oxidative stress and inflamatory plasma biomarkers in respiratory syncytial virus bronchiolitis. Clin. Respir. J. 2015
75. Reddy, S.P.; Hassoun, P.M.; Brower, R. Redox imbalance and ventilator-induced lung injury. Antioxid. Redox Signal. 2007, 9, 2003-2012
76. Hosakote, Y.M.; Komaravelli, N.; Mautemps, N.; Liu, T.; Garofalo, R.P.; Casola, A. Antioxidant mimetics modulate oxidative stress and cellular signaling in airway epithelial cells infected with respiratory syncytial virus. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 303, L991-L1000
77. Hosakote, Y.M.; Liu, T.; Castro, S.M.; Garofalo, R.P.; Casola, A. Respiratory syncytial virus induces oxidative stress by modulating antioxidant enzymes. Am. J. Respir. Cell Mol. Biol. 2009, 41, 348-357
78. Komaravelli, N.; Tian, B.; Ivanciuc, T.; Mautemps, N.; Brasier, A.R.; Garofalo, R.P.; Casola, A. Respiratory syncytial virus infection down-regulates antioxidant enzyme expression by triggering deacetylation-proteasomal degradation of nrf2. Free Radic. Biol. Med. 2015, 88, 391-403
79. Filomeni, G.; de Zio, D.; Cecconi, F. Oxidative stress and autophagy: The clash between damage and metabolic needs. Cell Death Diff. 2015, 22, 377-388
80. Cho, H.Y.; Imani, F.; Miller-DeGraff, L.; Walters, D.; Melendi, G.A.; Yamamoto, M.; Polack, F.P.; Kleeberger, S.R. Antiviral activity of nrf2 in a murine model of respiratory syncytial virus disease. Am. J. Respir. Crit. Care Med. 2009, 179, 138-150
81. Ma, Q.; He, X. Molecular basis of electrophilic and oxidative defense: Promises and perils of nrf2. Pharmacol. Rev. 2012, 64, 1055-1081
82. Yoboua, F.; Martel, A.; Duval, A.; Mukawera, E.; Grandvaux, N. Respiratory syncytial virus-mediated nf-kappa b p65 phosphorylation at serine 536 is dependent on rig-i, traf6, and ikk beta. J. Virol. 2010, 84, 7267-7277
83. Grandvaux, N.; Guan, X.; Yoboua, F.; Zucchini, N.; Fink, K.; Doyon, P.; Martin, L.; Servant, M.J.; Chartier, S. Sustained activation of interferon regulatory factor 3 during infection by paramyxoviruses requires mda5. J. Innate Immun. 2014, 6, 650-662
84. Loo, Y.M.; Fornek, J.; Crochet, N.; Bajwa, G.; Perwitasari, O.; Martinez-Sobrido, L.; Akira, S.; Gill, M.A.; Garcia-Sastre, A.; Katze, M.G.; et al. Distinct rig-i and mda5 signaling by rna viruses in innate immunity. J. Virol. 2008, 82, 335-345
85. Liu, P.; Jamaluddin, M.; Li, K.; Garofalo, R.P.; Casola, A.; Brasier, A.R. Retinoic acid-inducible gene i mediates early antiviral response and toll-like receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J. Virol. 2007, 81, 1401-1411
86. Roebuck, K.A. Oxidant stress regulation of il-8 and icam-1 gene expression: Differential activation and binding of the transcription factors ap-1 and nf-kappab (review). Int. J. Mol. Med. 1999, 4, 223-230
87. Mastronarde, J.G.; Monick, M.M.; Hunninghake, G.W. Oxidant tone regulates il-8 production in epithelium infected with respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 1995, 13, 237-244
88. Casola, A.; Burger, N.; Liu, T.; Jamaluddin, M.; Brasier, A.R.; Garofalo, R.P. 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. 2001, 276, 19715-19722
89. Fan, J.; Frey, R.S.; Rahman, A.; Malik, A.B. Role of neutrophil nadph oxidase in the mechanism of tumor necrosis factor-alpha -induced nf-kappa b activation and intercellular adhesion molecule-1 expression in endothelial cells. J. Biol. Chem. 2002, 277, 3404-3411
90. Liu, T.; Castro, S.; Brasier, A.R.; Jamaluddin, M.; Garofalo, R.P.; Casola, A. Reactive oxygen species mediate virus-induced stat activation: Role of tyrosine phosphatases. J. Biol. Chem. 2004, 279, 2461-2469
91. Indukuri, H.; Castro, S.M.; Liao, S.M.; Feeney, L.A.; Dorsch, M.; Coyle, A.J.; Garofalo, R.P.; Brasier, A.R.; Casola, A. Ikkepsilon regulates viral-induced interferon regulatory factor-3 activation via a redox-sensitive pathway. Virology 2006, 353, 155-165
92. Fink, K.; Duval, A.; Martel, A.; Soucy-Faulkner, A.; Grandvaux, N. Dual role of nox2 in respiratory syncytial virus-and sendai virus-induced activation of nf-kappab in airway epithelial cells. J. Immunol. 2008, 180, 6911-6922
93. 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
94. Fink, K.; Martin, L.; Mukawera, E.; Chartier, S.; de Deken, X.; Brochiero, E.; Miot, F.; Grandvaux, N. Ifnbeta/tnfalpha synergism induces a non-canonical stat2/irf9-dependent pathway triggering a novel duox2 nadph oxidase-mediated airway antiviral response. Cell Res. 2013, 23, 673-690
95. Kim, H.J.; Kim, C.H.; Ryu, J.H.; Kim, M.J.; Park, C.Y.; Lee, J.M.; Holtzman, M.J.; Yoon, J.H. Reactive oxygen species induce antiviral innate immune response through ifn-lambda regulation in human nasal epithelial cells. Am. J. Respir. Cell Mol. Biol. 2013, 49, 855-865