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Mitochondrion: an emerging platform critical for host antiviral signaling

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Pages 647-665 | Published online: 26 Feb 2011

Bibliography

  • Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 2007;449:811-18
  • Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007;449:819-26
  • Medzhitov R, Janeway CA Jr. Decoding the patterns of self and nonself by the innate immune system. Science 2002;296:298-300
  • Bowie AG, Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 2008;8:911-22
  • Katze MG, He Y, Gale M Jr. Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2002;2:675-87
  • Unterholzner L, Keating SE, Baran M, IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010;11:997-1004
  • Takaoka A, Wang Z, Choi MK, DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007;448:501-5
  • Hornung V, Ablasser A, Charrel-Dennis M, AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009;458:514-18
  • Fernandes-Alnemri T, Yu JW, Datta P, AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009;458:509-13
  • Burckstummer T, Baumann C, Bluml S, An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 2009;10:266-72
  • Roberts TL, Idris A, Dunn JA, HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009;323:1057-60
  • Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010;11:373-84
  • Sun Q, Sun L, Liu HH, The specific and essential role of MAVS in antiviral innate immune responses. Immunity 2006;24:633-42
  • Moore CB, Ting JP. Regulation of mitochondrial antiviral signaling pathways. Immunity 2008;28:735-9
  • Ablasser A, Bauernfeind F, Hartmann G, RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 2009;10:1065-72
  • Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009;138:576-91
  • Takeuchi O, Akira S. MDA5/RIG-I and virus recognition. Curr Opin Immunol 2008;20:17-22
  • Yoneyama M, Fujita T. Structural mechanism of RNA recognition by the RIG-I-like receptors. Immunity 2008;29:178-81
  • Kawai T, Takahashi K, Sato S, IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005;6:981-8
  • Meylan E, Curran J, Hofmann K, Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005;437:1167-72
  • Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF3. Cell 2005;122:669-82
  • Xu LG, Wang YY, Han KJ, VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 2005;19:727-40
  • Saha SK, Pietras EM, He JQ, Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J 2006;25:3257-63
  • Liu XY, Wei B, Shi HX, Tom70 mediates activation of interferon regulatory factor 3 on mitochondria. Cell Res 2010;20:994-1011
  • Tang ED, Wang CY. TRAF5 is a downstream target of MAVS in antiviral innate immune signaling. PLoS One 2010;5:e9172
  • Zhao T, Yang L, Sun Q, The NEMO adaptor bridges the nuclear factor-κB and interferon regulatory factor signaling pathways. Nat Immunol 2007;8:592-600
  • Guo B, Cheng G. Modulation of the interferon antiviral response by the TBK1/IKKi adaptor protein TANK. J Biol Chem 2007;282:11817-26
  • Li XD, Sun L, Seth RB, Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc Natl Acad Sci USA 2005;102:17717-22
  • Gray MW, Burger G, Lang BF. Mitochondrial evolution. Science 1999;283:1476-81
  • McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol 2006;16:R551-60
  • Castanier C, Arnoult D. Mitochondrial localization of viral proteins as a means to subvert host defense. Biochim Biophys Acta 2010; published online 31 August 2010, doi:101016/jbbamcr201008009
  • Andrejeva J, Childs KS, Young DF, The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci USA 2004;101:17264-9
  • Yoneyama M, Kikuchi M, Natsukawa T, The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004;5:730-7
  • Yoneyama M, Kikuchi M, Matsumoto K, Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 2005;175:2851-8
  • Zeng W, Xu M, Liu S, Key role of Ubc5 and lysine-63 polyubiquitination in viral activation of IRF3. Mol Cell 2009;36:315-25
  • Lin R, Lacoste J, Nakhaei P, Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKϵ molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 2006;80:6072-83
  • Paz S, Vilasco M, Arguello M, Ubiquitin-regulated recruitment of IκB kinase ϵ to the MAVS interferon signaling adapter. Mol Cell Biol 2009;29:3401-12
  • Yang K, Shi H, Qi R, Hsp90 regulates activation of interferon regulatory factor 3 and TBK-1 stabilization in Sendai virus-infected cells. Mol Biol Cell 2006;17:1461-71
  • Neupert W, Herrmann JM. Translocation of proteins into mitochondria. Annu Rev Biochem 2007;76:723-49
  • Young JC, Hoogenraad NJ, Hartl FU. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003;112:41-50
  • Wu Y, Sha B. Crystal structure of yeast mitochondrial outer membrane translocon member Tom70p. Nat Struct Mol Biol 2006;13:589-93
  • Millar DG, Shore GC. Mitochondrial Mas70p signal anchor sequence. Mutations in the transmembrane domain that disrupt dimerization but not targeting or membrane insertion. J Biol Chem 1994;269:12229-32
  • Pearl LH, Prodromou C, Workman P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 2008;410:439-53
  • Tang ED, Wang CY. MAVS self-association mediates antiviral innate immune signaling. J Virol 2009;83:3420-8
  • Baril M, Racine ME, Penin F, Lamarre D. MAVS dimer is a crucial signaling component of innate immunity and the target of hepatitis C virus NS3/4A protease. J Virol 2009;83:1299-311
  • Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol 2008;8:559-68
  • Komuro A, Horvath CM. RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J Virol 2006;80:12332-42
  • Venkataraman T, Valdes M, Elsby R, Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J Immunol 2007;178:6444-55
  • Satoh T, Kato H, Kumagai Y, LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci USA 2010;107:1512-17
  • Oshiumi H, Sakai K, Matsumoto M, Seya T. DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta-inducing potential. Eur J Immunol 2010;40:940-8
  • Wang YY, Liu LJ, Zhong B, WDR5 is essential for assembly of the VISA-associated signaling complex and virus-triggered IRF3 and NF-κB activation. Proc Natl Acad Sci USA 2010;107:815-20
  • Moore CB, Bergstralh DT, Duncan JA, NLRX1 is a regulator of mitochondrial antiviral immunity. Nature 2008;451:573-7
  • Arnoult D, Soares F, Tattoli I, An N-terminal addressing sequence targets NLRX1 to the mitochondrial matrix. J Cell Sci 2009;122:3161-8
  • Cui J, Zhu L, Xia X, NLRC5 negatively regulates the NF-κB and type I interferon signaling pathways. Cell 2010;141:483-96
  • Kumar H, Pandey S, Zou J, NLRC5 deficiency does not influence cytokine induction by virus and bacteria infections. J Immunol 2011;186:994-1000
  • Yasukawa K, Oshiumi H, Takeda M, Mitofusin 2 inhibits mitochondrial antiviral signaling. Sci Signal 2009;2:ra47
  • Onoguchi K, Onomoto K, Takamatsu S, Virus-infection or 5′ppp-RNA activates antiviral signal through redistribution of IPS-1 mediated by MFN1. PLoS Pathog 2010;6:e1001012
  • Castanier C, Garcin D, Vazquez A, Arnoult D. Mitochondrial dynamics regulate the RIG-I-like receptor antiviral pathway. EMBO Rep 2010;11:133-8
  • You F, Sun H, Zhou X, PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat Immunol 2009;10:1300-8
  • de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008;456:605-10
  • Sun W, Li Y, Chen L, ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci USA 2009;106:8653-8
  • Zhong B, Yang Y, Li S, The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 2008;29:538-50
  • Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008;455:674-8
  • Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009;461:788-92
  • Saitoh T, Fujita N, Hayashi T, Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci USA 2009;106:20842-6
  • Zhong B, Zhang L, Lei C, The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 2009;30:397-407
  • Tsuchida T, Zou J, Saitoh T, The Ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 2010;33:765-76
  • Li Y, Li C, Xue P, ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proc Natl Acad Sci USA 2009;106:7945-50
  • Jounai N, Takeshita F, Kobiyama K, The Atg5–Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci USA 2007;104:14050-5
  • Dixit E, Boulant S, Zhang Y, Peroxisomes are signaling platforms for antiviral innate immunity. Cell 2010;141:668-81
  • Song T, Wei C, Zheng Z, c-Abl tyrosine kinase interacts with MAVS and regulates innate immune response. FEBS Lett 2010;584:33-8
  • Johnsen IB, Nguyen TT, Bergstroem B, The tyrosine kinase c-Src enhances RIG-I (retinoic acid-inducible gene I)-elicited antiviral signaling. J Biol Chem 2009;284:19122-31
  • Vitour D, Dabo S, Ahmadi Pour M, Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS. J Biol Chem 2009;284:21797-809
  • Gack MU, Shin YC, Joo CH, TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007;446:916-20
  • Gack MU, Kirchhofer A, Shin YC, Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc Natl Acad Sci USA 2008;105:16743-8
  • Shigemoto T, Kageyama M, Hirai R, Identification of loss of function mutations in human genes encoding RIG-I and MDA5: implications for resistance to type I diabetes. J Biol Chem 2009;284:13348-54
  • Oshiumi H, Matsumoto M, Hatakeyama S, Seya T. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J Biol Chem 2009;284:807-17
  • Gao D, Yang YK, Wang RP, REUL is a novel E3 ubiquitin ligase and stimulator of retinoic-acid-inducible gene-I. PLoS One 2009;4:e5760
  • Arimoto K, Takahashi H, Hishiki T, Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc Natl Acad Sci USA 2007;104:7500-5
  • Arimoto K, Konishi H, Shimotohno K. UbcH8 regulates ubiquitin and ISG15 conjugation to RIG-I. Mol Immunol 2008;45:1078-84
  • Friedman CS, O'Donnell MA, Legarda-Addison D, The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep 2008;9:930-6
  • Zhang M, Wu X, Lee AJ, Regulation of IκB kinase-related kinases and antiviral responses by tumor suppressor CYLD. J Biol Chem 2008;283:18621-6
  • Kayagaki N, Phung Q, Chan S, DUBA: a deubiquitinase that regulates type I interferon production. Science 2007;318:1628-32
  • Boone DL, Turer EE, Lee EG, The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004;5:1052-60
  • Wertz IE, O'Rourke KM, Zhou H, De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature 2004;430:694-9
  • Lin R, Yang L, Nakhaei P, Negative regulation of the retinoic acid-inducible gene I-induced antiviral state by the ubiquitin-editing protein A20. J Biol Chem 2006;281:2095-103
  • Saitoh T, Yamamoto M, Miyagishi M, A20 is a negative regulator of IFN regulatory factor 3 signaling. J Immunol 2005;174:1507-12
  • Parvatiyar K, Barber GN, Harhaj EW. TAX1BP1 and A20 inhibit antiviral signaling by targeting TBK1-IKKi kinases. J Biol Chem 2010;285:14999-5009
  • Nakhaei P, Mesplede T, Solis M, The E3 ubiquitin ligase Triad3A negatively regulates the RIG-I/MAVS signaling pathway by targeting TRAF3 for degradation. PLoS Pathog 2009;5:e1000650
  • Jia Y, Song T, Wei C, Negative regulation of MAVS-mediated innate immune response by PSMA7. J Immunol 2009;183:4241-8
  • Yang K, Shi HX, Liu XY, TRIM21 is essential to sustain IFN regulatory factor 3 activation during antiviral response. J Immunol 2009;182:3782-92
  • Mao AP, Li S, Zhong B, Virus-triggered ubiquitination of TRAF3/6 by cIAP1/2 is essential for induction of interferon-beta (IFN-beta) and cellular antiviral response. J Biol Chem 2010;285:9470-6
  • Li S, Zheng H, Mao AP, Regulation of virus-triggered signaling by OTUB1- and OTUB2-mediated deubiquitination of TRAF3 and TRAF6. J Biol Chem 2010;285:4291-7
  • Chen R, Zhang L, Zhong B, The ubiquitin-specific protease 17 is involved in virus-triggered type I IFN signaling. Cell Res 2010;20:802-11
  • Kim MJ, Hwang SY, Imaizumi T, Yoo JY. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J Virol 2008;82:1474-83
  • Zhao C, Denison C, Huibregtse JM, Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc Natl Acad Sci USA 2005;102:10200-5
  • Shi HX, Yang K, Liu X, Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol Cell Biol 2010;30:2424-36
  • Skaug B, Chen ZJ. Emerging role of ISG15 in antiviral immunity. Cell 2010;143:187-90
  • Mi Z, Fu J, Xiong Y, Tang H. SUMOylation of RIG-I positively regulates the type I interferon signaling. Protein Cell 2010;1:275-83
  • Kubota T, Matsuoka M, Chang TH, Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. J Biol Chem 2008;283:25660-70
  • Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003;552:335-44
  • Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004;4:181-9
  • Fang FC. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2004;2:820-32
  • Tattoli I, Carneiro LA, Jehanno M, NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-κB and JNK pathways by inducing reactive oxygen species production. EMBO Rep 2008;9:293-300
  • Gack MU, Nistal-Villan E, Inn KS, Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J Virol 2010;84:3220-9
  • Nistal-Villan E, Gack MU, Martinez-Delgado G, Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-beta production. J Biol Chem 2010;285:20252-61
  • Li K, Foy E, Ferreon JC, Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci USA 2005;102:2992-7
  • Chen Z, Benureau Y, Rijnbrand R, GB virus B disrupts RIG-I signaling by NS3/4A-mediated cleavage of the adaptor protein MAVS. J Virol 2007;81:964-76
  • Rebsamen M, Meylan E, Curran J, Tschopp J. The antiviral adaptor proteins Cardif and Trif are processed and inactivated by caspases. Cell Death Differ 2008;15:1804-11
  • Yang Y, Liang Y, Qu L, Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc Natl Acad Sci USA 2007;104:7253-8
  • Lei X, Liu X, Ma Y, The 3C protein of enterovirus 71 inhibits retinoid acid-inducible gene I-mediated interferon regulatory factor 3 activation and type I interferon responses. J Virol 2010;84:8051-61
  • Mibayashi M, Martinez-Sobrido L, Loo YM, Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 2007;81:514-24
  • Dauber B, Schneider J, Wolff T. Double-stranded RNA binding of influenza B virus nonstructural NS1 protein inhibits protein kinase R but is not essential to antagonize production of alpha/beta interferon. J Virol 2006;80:11667-77
  • Ling Z, Tran KC, Teng MN. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J Virol 2009;83:3734-42
  • Iwai A, Shiozaki T, Kawai T, Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J Biol Chem 2010;285:32064-74
  • Wei C, Ni C, Song T, The hepatitis B virus X protein disrupts innate immunity by downregulating mitochondrial antiviral signaling protein. J Immunol 2010;185:1158-68
  • Wang X, Li Y, Mao A, Hepatitis B virus X protein suppresses virus-triggered IRF3 activation and IFN-beta induction by disrupting the VISA-associated complex. Cell Mol Immunol 2010;7:341-8
  • Wang H, Ryu WS. Hepatitis B virus polymerase blocks pattern recognition receptor signaling via interaction with DDX3: implications for immune evasion. PLoS Pathog 2010;6:e1000986
  • Yu S, Chen J, Wu M, Hepatitis B virus polymerase inhibits RIG-I- and Toll-like receptor 3-mediated beta interferon induction in human hepatocytes through interference with interferon regulatory factor 3 activation and dampening of the interaction between TBK1/IKKϵ and DDX3. J Gen Virol 2010;91:2080-90
  • Dong X, Feng H, Sun Q, Murine gamma-herpesvirus 68 hijacks MAVS and IKKbeta to initiate lytic replication. PLoS Pathog 2010;6:e1001001
  • Chattopadhyay S, Marques JT, Yamashita M, Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J 2010;29:1762-73
  • Lei Y, Moore CB, Liesman RM, MAVS-mediated apoptosis and its inhibition by viral proteins. PLoS One 2009;4:e5466
  • Lin R, Paz S, Hiscott J. Tom70 imports antiviral immunity to the mitochondria. Cell Res 2010;20:971-3
  • Cheng G, Zhong J, Chung J, Chisari FV. Double-stranded DNA and double-stranded RNA induce a common antiviral signaling pathway in human cells. Proc Natl Acad Sci USA 2007;104:9035-40
  • Matzinger P. The danger model: a renewed sense of self. Science 2002;296:301-5
  • Tveita AA. The danger model in deciphering autoimmunity. Rheumatology (Oxford) 2010;49:632-9
  • Okabe Y, Kawane K, Akira S, Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med 2005;202:1333-9
  • Stetson DB, Ko JS, Heidmann T, Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008;134:587-98
  • Yasutomo K, Horiuchi T, Kagami S, Mutation of DNASE1 in people with systemic lupus erythematosus. Nat Genet 2001;28:313-14
  • Lamarre D, Anderson PC, Bailey M, An NS3 protease inhibitor with antiviral effects in humans infected with hepatitis C virus. Nature 2003;426:186-9
  • Foy E, Li K, Wang C, Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 2003;300:1145-8

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