Multi-Step Regulation of Interferon Induction by Hepatitis C Virus

Akazawa T, Ebihara T, Okuno M et al (2007) Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells. Proc Natl Acad Sci USA 104:252–257 Andersson A, Yang SC, Huang M et al (2009) IL-7 promotes CXCR3 ligand-dependent T cell antitumor reactivity in lung cancer. J Immunol 182:6951–6958 Angus AGN, Dalrymple D, Boulant S et al (2010) Requirement of cellular DDX3 for hepatitis C virus replication is unrelated to its interaction with the viral core protein. J Gen Virol 91:122–132 Antonelli A, Ferri C, Ferrari SM et al (2008) Immunopathogenesis of HCV-related endocrine manifestations in chronic hepatitis and mixed cryoglobulinemia. Autoimmun Rev 8:18–23 Antonelli A, Ferri C, Ferrari SM et al (2009) Endocrine manifestations of hepatitis C virus infection. Nat Clin Pract Endocrinol Metab 5:26–34 Apolinario A, Majano PL, Lorente R et al (2005) Gene expression profile of T-cell-specific chemokines in human hepatocyte-derived cells: evidence for a synergistic inducer effect of cytokines and hepatitis C virus proteins. J Viral Hepat 12:27–37 Ariumi Y, Kuroki M, Abe K et al (2007) DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol 81:13922–13926 Azuma M, Ebihara T, Oshiumi H et al (2012) Cross-priming for antitumor CTL induced by soluble Ag + polyI:C depends on the TICAM-1 pathway in mouse CD11c+/CD8a+ dendritic cells. Oncoimmunology 1:581–592 Bantel H, Schulze-Osthoff K (2003) Apoptosis in hepatitis C virus infection. Cell Death Differ 10(Suppl 1):S48–S58 Binder M, Kochs G, Bartenschlager R et al (2007) Hepatitis C virus escape from the interferon regulatory factor 3 pathway by a passive and active evasion strategy. Hepatology 46:1365–1374 Bortoluci KR, Medzhitov R (2010) Control of infection by pyroptosis and autophagy: role of TLR and NLR. Cell Mol Life Sci 67:1643–1651 Caskey M, Lefebvre F, Filali-Mouhim A et al (2011) Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J Exp Med 208:2357–2366 Chang PC, Chi CW, Chau GY et al (2006) DDX3, a DEAD box RNA helicase, is deregulated in hepatitis virus-associated hepatocellular carcinoma and is involved in cell growth control. Oncogene 25:1991–2003 Cheng G, Zhong J, Chisari FV (2006) Inhibition of dsRNA-induced signaling in hepatitis C virus-infected cells by NS3 protease-dependent and -independent mechanisms. Proc Natl Acad Sci USA 103:8499–8504 Cho YS, Challa S, Moquin D et al (2009) Phosphorylation-driven assembly of the RIP1–RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:1112–1123 Ding Q, Huang B, Lu J et al (2012) Hepatitis C virus NS3/4A blocks IL-28 production. Eur J Immunol 42:2374–2382 Dixit E, Boulant S, Zhang Y et al (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141:668–681 Ebihara T, Masuda H, Akazawa T et al (2007) Induction of NKG2D ligands on human dendritic cells by TLR ligand stimulation and RNA virus infection. Int Immunol 19:1145–1155 Ebihara T, Shingai M, Matsumoto M et al (2008) Hepatitis C virus-infected hepatocytes extrinsically modulate dendritic cell maturation to activate T cells and natural killer cells. Hepatology 48:48–58 Ebihara T, Azuma M, Oshiumi H et al (2010) Identification of a polyI:C-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation. J Exp Med 207:2675–2687 Eksioglu EA, Zhu H, Bayouth L et al (2011) Characterization of HCV interactions with Toll-like receptors and RIG-I in liver cells. PLoS One 6:e21186 Estornes Y, Toscano F, Virard F et al (2012) dsRNA induces apoptosis through an atypical death complex associating TLR3 to caspase-8. Cell Death Differ 19:1482–1494 Ferreon JC, Ferreon AC, Li K et al (2005) Molecular determinants of TRIF proteolysis mediated by the hepatitis C virus NS3/4A protease. J Biol Chem 280:20483–20492 Florentin J, Aouar B, Dental C et al (2012) HCV glycoprotein E2 is a novel BDCA2 ligand and acts as an inhibitor of IFN production by plasmacytoid dendritic cells. Blood 120:4544–4551 Gack MU, Shin YC, Joo CH et al (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446:916–920 Harada K, Sato Y, Itatsu K et al (2007) Innate immune response to double-stranded RNA in biliary epithelial cells is ssociated with the pathogenesis of biliary atresia. Hepatology 46:1146–1154 He S, Wang L, Miao L et al (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137:1100–1111 He S, Liang Y, Shao F et al (2011) Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc Natl Acad Sci USA 108:20054–20059 Hogbom M, Collins R, van den Berg S et al (2007) Crystal structure of conserved domains 1 and 2 of the human DEAD-box helicase DDX3X in complex with the mononucleotide AMP. J Mol Biol 372:150–159 Horner SM, Liu HM, Park HS et al (2011) Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus. Proc Natl Acad Sci USA 108:14590–14595 Jelinek I, Leonard JN, Price GE et al (2011) TLR3-specific double-stranded RNA oligonucleotide adjuvants induce dendritic cell cross-presentation, CTL responses and antiviral protection. J Immunol 186:2422–2429 Jin B, Wang RY, Qiu Q et al (2007) Induction of potent cellular immune response in mice by hepatitis C virus NS3 protein with double-stranded RNA. Immunology 122:15–27 Kanda T, Steele R, Ray R et al (2009) Inhibition of intrahepatic gamma interferon production by hepatitis C virus nonstructural protein 5A in transgenic mice. J Virol 83:8463–8469 Kawai T, Akira S (2009) The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 21:317–337 Khvalevsky E, Rivkin L, Rachmilewitz J et al (2007) TLR3 signaling in a hepatoma cell line is skewed towards apoptosis. J Cell Biochem 100:1301–1312 Kim YS, Lee SG, Park SH et al (2001) Gene structure of the human DDX3 and chromosome mapping of its related sequences. Mol Cells 12:209–214 Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8:279–289 Larrubia JR, Benito-Martinez S, Calvino M et al (2008) Role of chemokines and their receptors in viral persistence and liver damage during chronic hepatitis C virus infection. World J Gastroenterol 14:7149–7159 Li K, Foy E, Ferreon JC et al (2005a) 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 102:2992–2997 Li XD, Sun L, Seth RB et al (2005b) Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc Natl Acad Sci USA 102:17717–17722 Li K, Li NL, Wei D et al (2012) Activation of chemokine and inflammatory cytokine response in hepatitis C virus-infected hepatocytes depends on Toll-like receptor 3 sensing of hepatitis C virus double-stranded RNA intermediates. Hepatology 55:666–675 Lim EJ, Chin R, Angus PW et al (2012) Enhanced apoptosis in post-liver transplant hepatitis C: effects of virus and immunosuppressants. World J Gastroenterol 18:2172–2179 Lindenbach BD, Thiel HJ, Rice CM (2007) Flaviviridae: the viruses and their replication. In: Knipe DM, Howley PM (eds) Fields virology. Lippincott Williams & Wilkins, Philadelphia, pp 1117–1118 Liu HM, Loo YM, Horner SM et al (2012) The mitochondrial targeting chaperone 14–3-3ε regulates a RIG-I translocon that mediates membrane association and innate antiviral immunity. Cell Host Microbe 11:528–537 Longhi MP, Trumpfheller C, Idoyaga J et al (2009) Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med 206:1589–1602 Loo YM, Owen DM, Li K et al (2006) Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc Natl Acad Sci USA 103:6001–6006 Lucas M, Schachterle W, Oberle K et al (2007) Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26:503–517 Matsumoto M, Seya T (2008) TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv Drug Deliv Rev 60:805–812 Matsumoto M, Oshiumi H, Seya T (2011) Antiviral responses induced by the TLR3 pathway. Rev Med Virol. doi:10.1002/rmv.680 McCartney S, Vermi W, Gilfillan S et al (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J Exp Med 206:2967–2976 McLauchlan J, Lemberg MK, Hope G et al (2002) Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J 21:3980–3988 Meylan E, Burns K, Hofmann K et al (2004) RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat Immunol 5:503–507 Morosky SA, Zhu J, Mukherjee A et al (2011) Retinoic acid-induced gene-I (RIG-I) associates with nucleotide-binding oligomerization domain-2 (NOD2) to negatively regulate inflammatory signaling. J Biol Chem 286:28574–28583 Mulhern O, Bowie AG (2010) Unexpected roles for DEAD-box protein 3 in viral RNA sensing pathways. Eur J Immunol 40:933–935 Nace G, Evankovich J, Eid R et al (2012) Dendritic cells and damage-associated molecular patterns: endogenous danger signals linking innate and adaptive immunity. J Innate Immun 4:6–15 Nakamura M, Funami K, Komori A et al (2008) Increased expression of Toll-like receptor 3 in intrahepatic biliary epithelial cells at sites of ductular reaction in diseased livers. Hepatol Int 2:222–230 Nitta S, Sakamoto N, Nakagawa M et al (2012) Hepatitis C virus NS4B protein targets STING and abrogates RIG-I-mediated type-I interferon-dependent innate immunity. Hepatology. doi:10.1002/hep.26017 Oda S, Schroder M, Khan AR (2009) Structural basis for targeting of human RNA helicase DDX3 by poxvirus protein K7. Structure 17:1528–1537 Okamoto K, Moriishi K, Miyamura T et al (2004) Intramembrane proteolysis and endoplasmic reticulum retention of hepatitis C virus core protein. J Virol 78:6370–6380 Oshiumi H, Sasai M, Shida K et al (2003) TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-beta. J Biol Chem 278:49751–49762 Oshiumi H, Matsumoto M, Hatakeyama S et al (2009) Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J Biol Chem 284:807–817 Oshiumi H, Ikeda M, Matsumoto M et al (2010a) Hepatitis C virus core protein abrogates the DDX3 function that enhances IPS-1-mediated IFN-beta induction. PLoS One 5:e14258 Oshiumi H, Sakai K, Matsumoto M et al (2010b) DEAD/H BOX 3 (DDX3) helicase binds the RIG-I adaptor IPS-1 to up-regulate IFN-beta-inducing potential. Eur J Immunol 40:940–948 Oshiumi H, Miyashita M, Inoue N et al (2010c) The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8:496–509 Owsianka AM, Patel AH (1999) Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257:330–340 Rathinam VA, Fitzgerald KA (2011) Cytosolic surveillance and antiviral immunity. Curr Opin Virol 1:455–462 Saeed M, Shiina M, Date T et al (2011) In vivo adaptation of hepatitis C virus in chimpanzees for efficient virus production and evasion of apoptosis. Hepatology 54:425–433 Saito T, Owen DM, Jiang F et al (2008) Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523–527 Sawa Y, Arima Y, Ogura H et al (2009) Hepatic interleukin-7 expression regulates T cell responses. Immunity 30:447–457 Schoggins JW, Wilson SJ, Panis M et al (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481–485 Schroder M (2009) Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochem Pharmacol 79:297–306 Schroder M, Baran M, Bowie AG et al (2008) Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J 27:2147–2157 Schulz O, Diebold SS, Chen M et al (2005) Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 433:887–892 Seth RB, Sun L, Ea CK et al (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122:669–682 Seya T, Matsumoto M (2009) The extrinsic RNA-sensing pathway for adjuvant immunotherapy of cancer. Cancer Immunol Immunother 58:1175–1184 Seya T, Shime H, Takaki H et al (2012) TLR3/TICAM-1 signaling in RIP3 tumor necroptosis. Oncoimmunology 1:917–923 Shimoda S, Harada K, Niiro H et al (2008) Biliary epithelial cells and primary biliary cirrhosis: the role of liver-infiltrating mononuclear cells. Hepatology 47:958–965 Shimoda S, Harada K, Niiro H et al (2011) Interaction between Toll-like receptors and natural killer cells in the destruction of bile ducts in primary biliary cirrhosis. Hepatology 53:1270–1281 Sillanpaa M, Kaukinen P, Melen K et al (2008) Hepatitis C virus proteins interfere with the activation of chemokine gene promoters and downregulate chemokine gene expression. J Gen Virol 89:432–443 Soulat D, Burckstummer T, Westermayer S 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 Takaoka A, Taniguchi T (2008) Cytosolic DNA recognition for triggering innate immune responses. Adv Drug Deliv Rev 60:847–857 Takaoka A, Yanai H, Kondo S et al (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434:243–249 Tanabe M, Kurita-Taniguchi M, Takeuchi K et al (2003) Mechanism of up-regulation of human Toll-like receptor 3 secondary to infection of measles virus-attenuated strains. Biochem Biophys Res Commun 311:39–48 Thomas E, Gonzalez VD, Li Q et al (2012) HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons. Gastroenterology 142:978–988 Uematsu S, Akira S (2007) Toll-like receptors and type I interferons. J Biol Chem 282:15319–15323 Wang N, Liang Y, Devaraj S et al (2009) Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells. J Virol 83:9824–9934 Wen C, He X, Ma H et al (2008) Hepatitis C virus infection downregulates the ligands of the activating receptor NKG2D. Cell Mol Immunol 5:475–478 Yeretssian G (2012) Effector functions of NLRs in the intestine: innate sensing, cell death, and disease. Immunol Res 54:25–36 Yoneyama M, Kikuchi M, Natsukawa T et al (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5:730–737 Yoneyama M, Onomoto K, Fujita T (2008) Cytoplasmic recognition of RNA. Adv Drug Deliv Rev 60:841–846 Zeremski M, Petrovic LM, Talal AH (2007) The role of chemokines as inflammatory mediators in chronic hepatitis C virus infection. J Viral Hepat 14:675–687 Zhang Z, Kim T, Bao M et al (2011) DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells. Immunity 34:866–878 Zhu H, Dong H, Eksioglu E et al (2007) Hepatitis C virus triggers apoptosis of a newly developed hepatoma cell line through antiviral defense system. Gastroenterology 133:1649–1659