Requirement of NOX2 and Reactive Oxygen Species for Efficient RIG-I-Mediated Antiviral Response through Regulation of MAVS Expression
The innate immune response is essential to the host defense against viruses, through restriction of virus replication and coordination of the adaptive immune response. Induction of antiviral genes is a tightly regulated process initiated mainly through sensing of invading virus nucleic acids in the cytoplasm by RIG-I like helicases, RIG-I or Mda5, which transmit the signal through a common mitochondria-associated adaptor, MAVS. Although major breakthroughs have recently been made, much remains unknown about the mechanisms that translate virus recognition into antiviral genes expression. Beside the reputed detrimental role, reactive oxygen species (ROS) act as modulators of cellular signaling and gene regulation. NADPH oxidase (NOX) enzymes are a main source of deliberate cellular ROS production. Here, we found that NOX2 and ROS are required for the host cell to trigger an efficient RIG-I-mediated IRF-3 activation and downstream antiviral IFNβ and IFIT1 gene expression. Additionally, we provide evidence that NOX2 is critical for the expression of the central mitochondria-associated adaptor MAVS. Taken together these data reveal a new facet to the regulation of the innate host defense against viruses through the identification of an unrecognized role of NOX2 and ROS.
Vyšlo v časopise:
Requirement of NOX2 and Reactive Oxygen Species for Efficient RIG-I-Mediated Antiviral Response through Regulation of MAVS Expression. PLoS Pathog 6(6): e32767. doi:10.1371/journal.ppat.1000930
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000930
Souhrn
The innate immune response is essential to the host defense against viruses, through restriction of virus replication and coordination of the adaptive immune response. Induction of antiviral genes is a tightly regulated process initiated mainly through sensing of invading virus nucleic acids in the cytoplasm by RIG-I like helicases, RIG-I or Mda5, which transmit the signal through a common mitochondria-associated adaptor, MAVS. Although major breakthroughs have recently been made, much remains unknown about the mechanisms that translate virus recognition into antiviral genes expression. Beside the reputed detrimental role, reactive oxygen species (ROS) act as modulators of cellular signaling and gene regulation. NADPH oxidase (NOX) enzymes are a main source of deliberate cellular ROS production. Here, we found that NOX2 and ROS are required for the host cell to trigger an efficient RIG-I-mediated IRF-3 activation and downstream antiviral IFNβ and IFIT1 gene expression. Additionally, we provide evidence that NOX2 is critical for the expression of the central mitochondria-associated adaptor MAVS. Taken together these data reveal a new facet to the regulation of the innate host defense against viruses through the identification of an unrecognized role of NOX2 and ROS.
Zdroje
1. KawaiT
AkiraS
2008 Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143 1 20
2. MichalletMC
MeylanE
ErmolaevaMA
VazquezJ
RebsamenM
2008 TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 28 651 661
3. SenGC
PetersGA
2007 Viral stress-inducible genes. Adv Virus Res 70 233 263
4. GrandvauxN
ServantMJ
tenOeverB
SenGC
BalachandranS
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. SharmaS
tenOeverBR
GrandvauxN
ZhouGP
LinR
2003 Triggering the interferon antiviral response through an IKK-related pathway. Science 300 1148 1151
6. FitzgeraldKA
McWhirterSM
FaiaKL
RoweDC
LatzE
2003 IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4 491 496
7. DrogeW
2002 Free radicals in the physiological control of cell function. Physiol Rev 82 47 95
8. NauseefWM
2008 Biological roles for the NOX family NADPH oxidases. J Biol Chem 283 16961 16965
9. BedardK
KrauseKH
2007 The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87 245 313
10. VignaisPV
2002 The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci 59 1428 1459
11. GrandvauxN
Soucy-FaulknerA
FinkK
2007 Innate host defense: Nox and Duox on phox's tail. Biochimie 89 1113 1122
12. RadaB
LetoTL
2008 Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15 164 187
13. Ogier-DenisE
MkaddemSB
VandewalleA
2008 NOX enzymes and Toll-like receptor signaling. Semin Immunopathol 30 291 300
14. YangCS
ShinDM
KimKH
LeeZW
LeeCH
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. FinkK
DuvalA
MartelA
Soucy-FaulknerA
GrandvauxN
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. ServantMJ
ten OeverB
LePageC
ContiL
GessaniS
2001 Identification of Distinct Signaling Pathways Leading to the Phosphorylation of Interferon Regulatory Factor 3. J Biol Chem 276 355 363
17. ServantMJ
GrandvauxN
HiscottJ
2002 Multiple signaling pathways leading to the activation of interferon regulatory factor 3. Biochem Pharmacol 64 985 992
18. MoriM
YoneyamaM
ItoT
TakahashiK
InagakiF
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. KatoH
SatoS
YoneyamaM
YamamotoM
UematsuS
2005 Cell type-specific involvement of RIG-I in antiviral response. Immunity 23 19 28
20. KatoH
TakeuchiO
SatoS
YoneyamaM
YamamotoM
2006 Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 101 105
21. LooYM
FornekJ
CrochetN
BajwaG
PerwitasariO
2008 Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82 335 345
22. ArimotoK
TakahashiH
HishikiT
KonishiH
FujitaT
2007 Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc Natl Acad Sci U S A 104 7500 7505
23. DiaoF
LiS
TianY
ZhangM
XuLG
2007 Negative regulation of MDA5- but not RIG-I-mediated innate antiviral signaling by the dihydroxyacetone kinase. Proc Natl Acad Sci U S A 104 11706 11711
24. KatoH
TakeuchiO
Mikamo-SatohE
HiraiR
KawaiT
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. GackMU
AlbrechtRA
UranoT
InnKS
HuangIC
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. LinR
LacosteJ
NakhaeiP
SunQ
YangL
2006 Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 80 6072 6083
27. NauseefWM
2007 How human neutrophils kill and degrade microbes: an integrated view. Immunol Rev 219 88 102
28. WuRF
MaZ
MyersDP
TeradaLS
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. SnelgroveRJ
EdwardsL
RaeAJ
HussellT
2006 An absence of reactive oxygen species improves the resolution of lung influenza infection. Eur J Immunol 36 1364 1373
30. IndukuriH
CastroSM
LiaoSM
FeeneyLA
DorschM
2006 Ikkepsilon regulates viral-induced interferon regulatory factor-3 activation via a redox-sensitive pathway. Virology 353 155 165
31. LiuP
JamaluddinM
LiK
GarofaloRP
CasolaA
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. KoaraiA
SugiuraH
YanagisawaS
IchikawaT
MinakataY
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-FukaiM
NakamuraY
2008 Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett 266 37 52
34. ChenK
CraigeSE
KeaneyJ
2009 Downstream Targets and Intracellular Compartmentalization in Nox Signaling. Antioxid Redox Signal
35. ChiangE
DangO
AndersonK
MatsuzawaA
IchijoH
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. SolisM
Romieu-MourezR
GoubauD
GrandvauxN
MespledeT
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. TalMC
SasaiM
LeeHK
YordyB
ShadelGS
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. MukherjeeTK
MukhopadhyayS
HoidalJR
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. TephlyLA
CarterAB
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. SoulatD
BurckstummerT
WestermayerS
GoncalvesA
BauchA
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. ClementJF
Bibeau-PoirierA
GravelSP
GrandvauxN
BonneilE
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. tenOeverBR
SharmaS
ZhouW
SunQ
GrandvauxN
2004 Activation of TBK1 and IKKe Kinases by Vesicular Stomatitis Virus Infection in Human Epithelial Cells. J Virol 78 10636 10649
43. JohnsonJ
AlbaraniV
NguyenM
GoldmanM
WillemsF
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. SarkarSN
PetersKL
ElcoCP
SakamotoS
PalS
2004 Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat Struct Mol Biol 11 1060 1067
45. WangRP
ZhangM
LiY
DiaoFC
ChenD
2008 Differential regulation of IKK alpha-mediated activation of IRF3/7 by NIK. Mol Immunol 45 1926 1934
46. ZhangB
LiM
ChenL
YangK
ShanY
2009 The TAK1-JNK cascade is required for IRF3 function in the innate immune response. Cell Res 19 412 428
47. TingJPY
DuncanJA
LeiY
2010 How the noninflammasome NLRs function in the innate immune system. Science 327 286 290
48. BubiciC
PapaS
DeanK
FranzosoG
2006 Mutual cross-talk between reactive oxygen species and nuclear factor-kappa B: molecular basis and biological significance. Oncogene 25 6731 6748
49. GroegerG
QuineyC
CotterTG
2009 Hydrogen peroxide as a cell-survival signaling molecule. Antioxid Redox Signal 11 2655 2671
50. GorospeM
KumarS
BaglioniC
1993 Tumor necrosis factor increases stability of interleukin-1 mRNA by activating protein kinase C. J Biol Chem 268 6214 6220
51. ZhaoJ
ChenJ
LuB
DongL
WangH
2008 TIP30 induces apoptosis under oxidative stress through stabilization of p53 messenger RNA in human hepatocellular carcinoma. Cancer Res 68 4133 4141
52. LiJ-M
FanLM
GeorgeVT
BrooksG
2007 Nox2 regulates endothelial cell cycle arrest and apoptosis via p21cip1 and p53. Free Radic Biol Med 43 976 986
53. PetryA
DjordjevicT
WeitnauerM
KietzmannT
HessJ
2006 NOX2 and NOX4 mediate proliferative response in endothelial cells. Antioxid Redox Signal 8 1473 1484
54. PeshavariyaH
DustingGJ
JiangF
HalmosLR
SobeyCG
2009 NADPH oxidase isoform selective regulation of endothelial cell proliferation and survival. Naunyn Schmiedebergs Arch Pharmacol 380 193 204
55. ChoseO
Sansilvestri-MorelP
Badier-CommanderC
BernhardtF
FabianiJN
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. TakemuraY
GoodsonP
BaoHF
JainL
HelmsMN
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. YouF
SunH
ZhouX
SunW
LiangS
2009 PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol 1300 1308
58. BrownDI
GriendlingKK
2009 Nox proteins in signal transduction. Free Radic Biol Med 47 1239 1253
59. Ushio-FukaiM
2006 Localizing NADPH oxidase-derived ROS. Sci STKE 2006 re8
60. AnilkumarN
WeberR
ZhangM
BrewerA
ShahAM
2008 Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 28 1347 1354
61. BarilM
RacineM-E
PeninF
LamarreD
2009 MAVS dimer is a crucial signaling component of innate immunity and the target of hepatitis C virus NS3/4A protease. J Virol 1299 1311
62. ServantMJ
GrandvauxN
tenOeverBR
DuguayD
LinR
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. IwamuraT
YoneyamaM
YamaguchiK
SuharaW
MoriW
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. LinR
GeninP
MamaneY
HiscottJ
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. DussaultAA
PouliotM
2006 Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol Proced Online 8 1 10
66. LadSP
YangG
ScottDA
ChaoTH
Correia JdaS
2008 Identification of MAVS splicing variants that interfere with RIGI/MAVS pathway signaling. Mol Immunol 45 2277 2287
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