Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression

PLoS Pathogens

Volumn 6, Issue 6, 2010, Pages

  Soucy Faulkner, Anton ^a,b   Mukawera, Espérance ^a   Fink, Karin ^a,b   Martel, Alexis ^a,b   Jouan, Loubna ^a,b   Nzengue, Yves ^a,b   Lamarre, Daniel ^a,b   vande Velde, Christine ^a,b   Grandvaux, Nathalie ^a,b  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; CARRIER PROTEIN; I KAPPA B KINASE EPSILON; INTERFERON REGULATORY FACTOR 3; PROTEIN IFIT1; PROTEIN MAVS; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; RETINOIC ACID INDUCIBLE PROTEIN I; TBK1 ENZYME; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ISG56; UNCLASSIFIED DRUG; CYBB PROTEIN, HUMAN; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; IFIT1 PROTEIN, HUMAN; INTERLEUKIN 6; LUCIFERASE; MEMBRANE PROTEIN; MESSENGER RNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VISA PROTEIN, HUMAN;

ARTICLE; DOWN REGULATION; ENZYME ACTIVATION; HOST CELL; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; BRONCHUS; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LUNG TUMOR; METABOLISM; PHYSIOLOGY; RESPIROVIRUS INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENDAI VIRUS; SIGNAL TRANSDUCTION; VIROLOGY; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BLOTTING, WESTERN; BRONCHI; CARRIER PROTEINS; CELLS, CULTURED; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERLEUKIN-6; LUCIFERASES; LUNG NEOPLASMS; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RESPIROVIRUS INFECTIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENDAI VIRUS; SIGNAL TRANSDUCTION;

EID: 77954680592     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000930     Document Type: Article

References (66)

1. Kawai T, Akira S (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143: 1-20.
2. Michallet MC, Meylan E, Ermolaeva MA, Vazquez J, Rebsamen M, et al. (2008) TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 28: 651-661.
3. Sen GC, Peters GA (2007) Viral stress-inducible genes. Adv Virus Res 70: 233-263.
4. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, et al. (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76: 5532-5539.
5. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, et al. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
6. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, et al. (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4: 491-496.
7. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95.
8. Nauseef WM (2008) Biological roles for the NOX family NADPH oxidases. J Biol Chem 283: 16961-16965.
9. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313.
10. Vignais PV (2002) The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci 59: 1428-1459.
11. Grandvaux N, Soucy-Faulkner A, Fink K (2007) Innate host defense: Nox and Duox on phox's tail. Biochimie 89: 1113-1122.
12. Rada B, Leto TL (2008) Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15: 164-187.
13. Ogier-Denis E, Mkaddem SB, Vandewalle A (2008) NOX enzymes and Tolllike receptor signaling. Semin Immunopathol 30: 291-300.
14. Yang CS, Shin DM, Kim KH, Lee ZW, Lee CH, et al. (2009) NADPH oxidase 2 interaction with TLR2 is required for efficient innate immune responses to mycobacteria via cathelicidin expression. J Immunol 182: 3696-3705.
15. Fink K, Duval A, Martel A, Soucy-Faulkner A, Grandvaux N (2008) Dual role of NOX2 in respiratory syncytial virus- and sendai virus-induced activation of NF-kappaB in airway epithelial cells. J Immunol 180: 6911-6922.
16. Servant MJ, ten Oever B, LePage C, Conti L, Gessani S, et al. (2001) Identification of Distinct Signaling Pathways Leading to the Phosphorylation of Interferon Regulatory Factor 3. J Biol Chem 276: 355-363.
17. Servant MJ, Grandvaux N, Hiscott J (2002) Multiple signaling pathways leading to the activation of interferon regulatory factor 3. Biochem Pharmacol 64: 985-992.
18. Mori M, Yoneyama M, Ito T, Takahashi K, Inagaki F, et al. (2004) Identification of Ser-386 of interferon regulatory factor 3 as critical target for inducible phosphorylation that determines activation. J Biol Chem 279: 9698-9702.
19. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19-28.
20. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
21. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, et al. (2008) Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82: 335-345.
22. Arimoto K, Takahashi H, Hishiki T, Konishi H, Fujita T, et al. (2007) Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc Natl Acad Sci U S A 104: 7500-7505.
23. Diao F, Li S, Tian Y, Zhang M, Xu LG, et al. (2007) Negative regulation of MDA5- but not RIG-I-mediated innate antiviral signaling by the dihydroxy-acetone kinase. Proc Natl Acad Sci U S A 104: 11706-11711.
24. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, et al. (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205: 1601-1610.
25. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, et al. (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5: 439-449.
26. Lin R, Lacoste J, Nakhaei P, Sun Q, Yang L, et al. (2006) Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mito-chondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 80: 6072-6083.
27. Nauseef WM (2007) How human neutrophils kill and degrade microbes: an integrated view. Immunol Rev 219: 88-102.
28. Wu RF, Ma Z, Myers DP, Terada LS (2007) HIV-1 Tat activates dual Nox pathways leading to independent activation of ERK and JNK MAP kinases. J Biol Chem 282: 37412-37419.
29. Snelgrove RJ, Edwards L, Rae AJ, Hussell T (2006) An absence of reactive oxygen species improves the resolution of lung influenza infection. Eur J Immunol 36: 1364-1373.
30. Indukuri H, Castro SM, Liao SM, Feeney LA, Dorsch M, et al. (2006) Ikkepsilon regulates viral-induced interferon regulatory factor-3 activation via a redox-sensitive pathway. Virology 353: 155-165.
31. Liu P, Jamaluddin M, Li K, Garofalo RP, Casola A, et al. (2007) 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 81: 1401-1411.
32. Koarai A, Sugiura H, Yanagisawa S, Ichikawa T, Minakata Y, et al. (2009) Oxidative Stress Enhances Toll-like Receptor 3 Response to Double-stranded RNA in Airway Epithelial Cells. Am J Respir Cell Mol Biol.
33. Ushio-Fukai M, Nakamura Y (2008) Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett 266: 37-52.
34. Chen K, Craige SE, Keaney J (2009) Downstream Targets and Intracellular Compartmentalization in Nox Signaling. Antioxid Redox Signal.
35. Chiang E, Dang O, Anderson K, Matsuzawa A, Ichijo H, et al. (2006) Cutting edge: apoptosis-regulating signal kinase 1 is required for reactive oxygen species-mediated activation of IFN regulatory factor 3 by lipopolysaccharide. J Immunol 176: 5720-5724.
36. Solis M, Romieu-Mourez R, Goubau D, Grandvaux N, Mesplede T, et al. (2007) Involvement of TBK1 and IKKepsilon in lipopolysaccharide-induced activation of the interferon response in primary human macrophages. Eur J Immunol 37: 528-539.
37. Tal MC, Sasai M, Lee HK, Yordy B, Shadel GS, et al. (2009) Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci U S A 106: 2770-2775.
38. Mukherjee TK, Mukhopadhyay S, Hoidal JR (2005) The role of reactive oxygen species in TNFalpha-dependent expression of the receptor for advanced glycation end products in human umbilical vein endothelial cells. Biochim Biophys Acta 1744: 213-223.
39. Tephly LA, Carter AB (2007) Constitutive NADPH oxidase and increased mitochondrial respiratory chain activity regulate chemokine gene expression. Am J Physiol Lung Cell Mol Physiol 293: L1143-1155.
40. Soulat D, Burckstummer T, Westermayer S, Goncalves A, Bauch A, et al. (2008) The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. Embo J 27: 2135-2146.
41. Clement JF, Bibeau-Poirier A, Gravel SP, Grandvaux N, Bonneil E, et al. (2008) Phosphorylation of IRF-3 on Ser 339 generates a hyperactive form of IRF-3 through regulation of dimerization and CBP association. J Virol 82: 3984-3996.
42. tenOever BR, Sharma S, Zhou W, Sun Q, Grandvaux N, et al. (2004) Activation of TBK1 and IKKe Kinases by Vesicular Stomatitis Virus Infection in Human Epithelial Cells. J Virol 78: 10636-10649.
43. Johnson J, Albarani V, Nguyen M, Goldman M, Willems F, et al. (2007) Protein kinase Calpha is involved in interferon regulatory factor 3 activation and type I interferon-beta synthesis. J Biol Chem 282: 15022-15032.
44. Sarkar SN, Peters KL, Elco CP, Sakamoto S, Pal S, et al. (2004) Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat Struct Mol Biol 11: 1060-1067.
45. Wang RP, Zhang M, Li Y, Diao FC, Chen D, et al. (2008) Differential regulation of IKK alpha-mediated activation of IRF3/7 by NIK. Mol Immunol 45: 1926-1934.
46. Zhang B, Li M, Chen L, Yang K, Shan Y, et al. (2009) The TAK1-JNK cascade is required for IRF3 function in the innate immune response. Cell Res 19: 412-428.
47. Ting JPY, Duncan JA, Lei Y (2010) How the noninflammasome NLRs function in the innate immune system. Science 327: 286-290.
48. Bubici C, Papa S, Dean K, Franzoso G (2006) Mutual cross-talk between reactive oxygen species and nuclear factor-kappa B: molecular basis and biological significance. Oncogene 25: 6731-6748.
49. Groeger G, Quiney C, Cotter TG (2009) Hydrogen peroxide as a cell-survival signaling molecule. Antioxid Redox Signal 11: 2655-2671.
50. Gorospe M, Kumar S, Baglioni C (1993) Tumor necrosis factor increases stability of interleukin-1 mRNA by activating protein kinase C. J Biol Chem 268: 6214-6220.
51. Zhao J, Chen J, Lu B, Dong L, Wang H, et al. (2008) TIP30 induces apoptosis under oxidative stress through stabilization of p53 messenger RNA in human hepatocellular carcinoma. Cancer Res 68: 4133-4141.
52. Li J-M, Fan LM, George VT, Brooks G (2007) Nox2 regulates endothelial cell cycle arrest and apoptosis via p21cip1 and p53. Free Radic Biol Med 43: 976-986.
53. Petry A, Djordjevic T, Weitnauer M, Kietzmann T, Hess J, et al. (2006) NOX2 and NOX4 mediate proliferative response in endothelial cells. Antioxid Redox Signal 8: 1473-1484.
54. Peshavariya H, Dusting GJ, Jiang F, Halmos LR, Sobey CG, et al. (2009) NADPH oxidase isoform selective regulation of endothelial cell proliferation and survival. Naunyn Schmiedebergs Arch Pharmacol 380: 193-204.
55. Chose O, Sansilvestri-Morel P, Badier-Commander C, Bernhardt F, Fabiani JN, et al. (2008) Distinct role of nox1, nox2, and p47phox in unstimulated versus angiotensin II-induced NADPH oxidase activity in human venous smooth muscle cells. J Cardiovasc Pharmacol 51: 131-139.
56. Takemura Y, Goodson P, Bao HF, Jain L, Helms MN Rac1-mediated NADPH Oxidase Release of O2- Regulates Epithelial Sodium Channel (ENaC) activity in the Alveolar Epithelium. Am J Physiol Lung Cell Mol Physiol.
57. You F, Sun H, Zhou X, Sun W, Liang S, et al. (2009) PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol. pp 1300-1308.
58. Brown DI, Griendling KK (2009) Nox proteins in signal transduction. Free Radic Biol Med 47: 1239-1253.
59. Ushio-Fukai M (2006) Localizing NADPH oxidase-derived ROS. Sci STKE 2006: re8.
60. Anilkumar N, Weber R, Zhang M, Brewer A, Shah AM (2008) Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 28: 1347-1354.
61. Baril M, Racine M-E, Penin F, Lamarre D (2009) MAVS dimer is a crucial signaling component of innate immunity and the target of hepatitis C virus NS3/4A protease. J Virol. pp 1299-1311.
62. Servant MJ, Grandvaux N, tenOever BR, Duguay D, Lin R, et al. (2003) Identification of the minimal phosphoacceptor site required for in vivo activation of interferon regulatory factor 3 in response to virus and double-stranded RNA. J Biol Chem 278: 9441-9447.
63. Iwamura T, Yoneyama M, Yamaguchi K, Suhara W, Mori W, et al. (2001) Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection: common and unique pathways. Genes Cells 6: 375-388.
64. Lin R, Genin P, Mamane Y, Hiscott J (2000) Selective DNA binding and association with the CREB binding protein coactivator contribute to differential activation of alpha/beta interferon genes by interferon regulatory factors 3 and 7. Mol Cell Biol 20: 6342-6353.
65. Dussault AA, Pouliot M (2006) Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol Proced Online 8: 1-10.
66. Lad SP, Yang G, Scott DA, Chao TH, Correia Jda S, et al. (2008) Identification of MAVS splicing variants that interfere with RIGI/MAVS pathway signaling. Mol Immunol 45: 2277-2287.