Pathogen-associated molecular pattern recognition of hepatitis C virus transmitted/founder variants by RIG-I is dependent on U-Core length

Journal of Virology

Volumn 89, Issue 21, 2015, Pages 11056-11068

  Kell, Alison ^a   Stoddard, Mark ^b   Li, Hui ^b   Marcotrigiano, Joe ^c   Shaw, George M ^b   Gale, Michael ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; POLYURIDYLIC ACID; RETINOIC ACID INDUCIBLE PROTEIN I; VIRUS RNA; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE SEQUENCE; GENETIC VARIABILITY; HEPATITIS C VIRUS; IMMUNOREGULATION; INNATE IMMUNITY; LIVER CELL; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; VIRUS GENOME; VIRUS TRANSMISSION; CELL LINE; GEL MOBILITY SHIFT ASSAY; GENETIC VARIATION; GENETICS; HEPACIVIRUS; HEPATITIS C; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOBLOTTING; IMMUNOLOGY; METABOLISM; PLASMID; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; VIROLOGY;

CELL LINE; DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENETIC VARIATION; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; IMMUNOBLOTTING; PLASMIDS; POLY U; POLYMERASE CHAIN REACTION; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84945207994     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01964-15     Document Type: Article

References (63)

1. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M, Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454:523-527. http://dx.doi.org/10.1038 /nature07106.
2. Schnell G, Loo YM, Marcotrigiano J, Gale M, Jr. 2012. Uridine composition of the poly-U/UC tract ofHCVRNAdefines non-self recognition by RIG-I. PLoS Pathog 8:e1002839. http://dx.doi.org/10.1371/journal.ppat .1002839.
3. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G. 2006. 5=-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997. http: //dx.doi.org/10.1126/science.1132505.
4. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez- Sobrido L, Akira S, Gill MA, Garcia-Sastre A, Katze MG, Gale M, Jr. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82:335-345. http://dx.doi.org/10.1128/JVI.01080-07.
5. Kell AM, Gale M, Jr. 5 March 2015, posting date. RIG-I in RNA virus recognition. Virology http://dx.doi.org/10.1016/j.virol.2015.02.017.
6. Loo YM, Gale M, Jr. 2011. Immune signaling by RIG-I-like receptors. Immunity 34:680-692. http://dx.doi.org/10.1016/j.immuni.2011.05.003.
7. Jiang F, Ramanathan A, Miller MT, Tang GQ, Gale M, Jr, Patel SS, Marcotrigiano J. 2011. Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 479:423-427. http://dx.doi.org /10.1038/nature10537.
8. Kowalinski E, Lunardi T, McCarthy AA, Louber J, Brunel J, Grigorov B, Gerlier D, Cusack S. 2011. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 147:423- 435. http://dx.doi.org/10.1016/j.cell.2011.09.039.
9. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6:981-988. http://dx.doi.org/10.1038/ni1243.
10. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167- 1172. http://dx.doi.org/10.1038/nature04193.
11. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. 2005. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19:727-740. http://dx.doi.org/10.1016/j.molcel.2005.08.014.
12. Preiss S, Thompson A, Chen X, Rodgers S, Markovska V, Desmond P, Visvanathan K, Li K, Locarnini S, Revill P. 2008. Characterization of the innate immune signalling pathways in hepatocyte cell lines. J Viral Hepat 15:888-900. http://dx.doi.org/10.1111/j.1365-2893.2008.01001.x.
13. Errett JS, Suthar MS, McMillan A, Diamond MS, Gale M, Jr. 2013. The essential, nonredundant roles of RIG-I and MDA5 in detecting and controlling West Nile virus infection. J Virol 87:11416-11425. http://dx.doi .org/10.1128/JVI.01488-13.
14. Feng Q, Langereis MA, Olagnier D, Chiang C, van de Winkel R, van Essen P, Zoll J, Hiscott J, van Kuppeveld FJ. 2014. Coxsackievirus cloverleaf RNA containing a 5= triphosphate triggers an antiviral response via RIG-I activation. PLoS One 9:e95927. http://dx.doi.org/10.1371 /journal.pone.0095927.
15. Huang C, Kolokoltsova OA, Yun NE, Seregin AV, Poussard AL, Walker AG, Brasier AR, Zhao Y, Tian B, de la Torre JC, Paessler S. 2012. Junin virus infection activates the type I interferon pathway in a RIG-Idependent manner. PLoS Negl Trop Dis 6:e1659. http://dx.doi.org/10 .1371/journal.pntd.0001659.
16. Ikegame S, Takeda M, Ohno S, Nakatsu Y, Nakanishi Y, Yanagi Y. 2010. Both RIG-I and MDA5 RNA helicases contribute to the induction of alpha/ beta interferon in measles virus-infected human cells. J Virol 84:372- 379. http://dx.doi.org/10.1128/JVI.01690-09.
17. Lee MH, Lalwani P, Raftery MJ, Matthaei M, Lutteke N, Kirsanovs S, Binder M, Ulrich RG, Giese T, Wolff T, Kruger DH, Schonrich G. 2011. RNA helicase retinoic acid-inducible gene I as a sensor of Hantaan virus replication. J Gen Virol 92:2191-2200. http://dx.doi.org/10.1099/vir.0 .032367-0.
18. Spiropoulou CF, Ranjan P, Pearce MB, Sealy TK, Albarino CG, Gangappa S, Fujita T, Rollin PE, Nichol ST, Ksiazek TG, Sambhara S. 2009. RIG-I activation inhibits ebolavirus replication. Virology 392:11-15. http: //dx.doi.org/10.1016/j.virol.2009.06.032.
19. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5:730-737. http://dx.doi.org/10.1038/ni1087.
20. Alff PJ, Gavrilovskaya IN, Gorbunova E, Endriss K, Chong Y, Geimonen E, Sen N, Reich NC, Mackow ER. 2006. The pathogenic NY-1 hantavirus G1 cytoplasmic tail inhibits RIG-I- and TBK-1-directed interferon responses. J Virol 80:9676-9686. http://dx.doi.org/10.1128/JVI .00508-06.
21. Basler CF, Mikulasova A, Martinez-Sobrido L, Paragas J, Muhlberger E, Bray M, Klenk HD, Palese P, Garcia-Sastre A. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J Virol 77:7945-7956. http://dx.doi.org/10.1128/JVI.77.14.7945-7956.2003.
22. Chen X, Yang X, Zheng Y, Yang Y, Xing Y, Chen Z. 2014. SARS coronavirus papain-like protease inhibits the type I interferon signaling pathway through interaction with the STING-TRAF3-TBK1 complex. Protein Cell 5:369-381. http://dx.doi.org/10.1007/s13238-014-0026-3.
23. Chiang JJ, Davis ME, Gack MU. 21 June 2014, posting date.Regulation of RIG-I-like receptor signaling by host and viral proteins.Cytokine Growth Factor Rev http://dx.doi.org/10.1016/j.cytogfr.2014.06.005.
24. Childs K, Randall R, Goodbourn S. 2012. Paramyxovirus V proteins interact with the RNA helicase LGP2 to inhibit RIG-I-dependent interferon induction. J Virol 86:3411-3421. http://dx.doi.org/10.1128/JVI .06405-11.
25. Cimica V, Dalrymple NA, Roth E, Nasonov A, Mackow ER. 2014. An innate immunity-regulating virulence determinant is uniquely encoded by the Andes virus nucleocapsid protein. mBio 5:e01088 -13. http://dx.doi .org/10.1128/mBio.01088-13.
26. Deng L, Dai P, Parikh T, Cao H, Bhoj V, Sun Q, Chen Z, Merghoub T, Houghton A, Shuman S. 2008. Vaccinia virus subverts a mitochondrial antiviral signaling protein-dependent innate immune response in keratinocytes through its double-stranded RNA binding protein, E3. J Virol 82:10735-10746. http://dx.doi.org/10.1128/JVI.01305-08.
27. Fensterl V, Grotheer D, Berk I, Schlemminger S, Vallbracht A, Dotzauer A. 2005. Hepatitis A virus suppresses RIG-I-mediated IRF-3 activation to block induction of beta interferon. J Virol 79:10968-10977. http: //dx.doi.org/10.1128/JVI.79.17.10968-10977.2005.
28. Frolova EI, Fayzulin RZ, Cook SH, Griffin DE, Rice CM, Frolov I. 2002. Roles of nonstructural protein nsP2 and alpha/beta interferons in determining the outcome of Sindbis virus infection. J Virol 76:11254-11264. http://dx.doi.org/10.1128/JVI.76.22.11254-11264.2002.
29. Li J, Liu Y, Zhang X. 2010. Murine coronavirus induces type I interferon in oligodendrocytes through recognition by RIG-I and MDA5. J Virol 84:6472-6482. http://dx.doi.org/10.1128/JVI.00016-10.
30. Luo R, Xiao S, Jiang Y, Jin H, Wang D, Liu M, Chen H, Fang L. 2008. Porcine reproductive and respiratory syndrome virus (PRRSV) suppresses interferon-beta production by interfering with the RIG-I signaling pathway. Mol Immunol 45:2839 -2846. http://dx.doi.org/10 .1016/j.molimm.2008.01.028.
31. Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M, Jr, Garcia-Sastre A. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 81:514-524. http://dx.doi.org/10.1128/JVI.01265-06.
32. McGivern DR, Lemon SM. 2011. Virus-specific mechanisms of carcinogenesis in hepatitis C virus associated liver cancer. Oncogene 30:1969- 1983. http://dx.doi.org/10.1038/onc.2010.594.
33. Pawlotsky JM. 2004. Pathophysiology of hepatitis C virus infection and related liver disease. Trends Microbiol 12:96-102. http://dx.doi.org/10 .1016/j.tim.2003.12.005.
34. Horner SM, Gale M, Jr. 2013. Regulation of hepatic innate immunity by hepatitis C virus. Nat Med 19:879-888. http://dx.doi.org/10.1038/nm .3253.
35. Horner SM, Park HS, Gale M, Jr. 2012. Control of innate immune signaling and membrane targeting by the hepatitis C virus NS3/4A pro-tease are governed by the NS3 helix alpha0. J Virol 86:3112-3120. http: //dx.doi.org/10.1128/JVI.06727-11.
36. Loo YM, Owen DM, Li K, Erickson AK, Johnson CL, Fish PM, Carney DS, Wang T, Ishida H, Yoneyama M, Fujita T, Saito T, Lee WM, Hagedorn CH, Lau DT, Weinman SA, Lemon SM, Gale M, Jr. 2006. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc Natl Acad Sci U S A 103:6001-6006. http: //dx.doi.org/10.1073/pnas.0601523103.
37. You S, Rice CM. 2008. 3= RNA elements in hepatitis C virus replication: kissing partners and long poly(U). J Virol 82:184-195. http://dx.doi.org /10.1128/JVI.01796-07.
38. Friebe P, Bartenschlager R. 2002. Genetic analysis of sequences in the 3= nontranslated region of hepatitis C virus that are important for RNA replication. J Virol 76:5326-5338. http://dx.doi.org/10.1128/JVI.76.11.5326 -5338.2002.
39. Yi M, Lemon SM. 2003. 3= Nontranslated RNA signals required for replication of hepatitis C virus RNA. J Virol 77:3557-3568. http://dx.doi .org/10.1128/JVI.77.6.3557-3568.2003.
40. Foy E, Li K, Sumpter R, Jr, Loo YM, Johnson CL, Wang C, Fish PM, Yoneyama M, Fujita T, Lemon SM, Gale M, Jr. 2005. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci U S A 102:2986-2991. http://dx.doi .org/10.1073/pnas.0408707102.
41. Yang Y, Liang Y, Qu L, Chen Z, Yi M, Li K, Lemon SM. 2007. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc Natl Acad Sci U S A 104:7253-7258. http: //dx.doi.org/10.1073/pnas.0611506104.
42. Cainelli F. 2013. Hepatitis C virus and human immunodeficiency virus transmission routes: Differences and similarities. World J Hepatol 5:234- 236. http://dx.doi.org/10.4254/wjh.v5.i5.234.
43. Li H, Stoddard MB, Wang S, Blair LM, Giorgi EE, Parrish EH, Learn GH, Hraber P, Goepfert PA, Saag MS, Denny TN, Haynes BF, Hahn BH, Ribeiro RM, Perelson AS, Korber BT, Bhattacharya T, Shaw GM. 2012. Elucidation of hepatitis C virus transmission and early diversification by single genome sequencing. PLoS Pathog 8:e1002880. http://dx.doi .org/10.1371/journal.ppat.1002880.
44. Stoddard MB, Li H, Wang S, Saeed M, Andrus L, Ding W, Jiang X, Learn GH, von Schaewen M, Wen J, Goepfert PA, Hahn BH, Ploss A, Rice CM, Shaw GM. 2015. Identification, molecular cloning, and analysis of full-length hepatitis C virus transmitted/founder genotypes 1, 3, and 4. mBio 6:e02518. http://dx.doi.org/10.1128/mBio.02518-14.
45. Sumpter R, Jr, Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79:2689-2699. http://dx.doi.org/10.1128/JVI.79.5 .2689-2699.2005.
46. Blight KJ, McKeating JA, Rice CM. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76: 13001-13014. http://dx.doi.org/10.1128/JVI.76.24.13001-13014.2002.
47. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. 2005. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102:9294-9299. http: //dx.doi.org/10.1073/pnas.0503596102.
48. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, Bartenschlager R, Liang TJ. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791-796. http://dx.doi .org/10.1038/nm1268.
49. Reed KE, Rice CM. 1998. Molecular characterization of hepatitis C virus. Curr Stud Hematol Blood Transfus 1998:1-37.
50. Saito T, Hirai R, Loo YM, Owen D, Johnson CL, Sinha SC, Akira S, Fujita T, Gale M, Jr. 2007. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci U S A 104:582-587. http://dx.doi.org/10.1073/pnas.0606699104.
51. Luo D, Ding SC, Vela A, Kohlway A, Lindenbach BD, Pyle AM. 2011. Structural insights into RNA recognition by RIG-I. Cell 147:409-422. http://dx.doi.org/10.1016/j.cell.2011.09.023.
52. Cui S, Eisenacher K, Kirchhofer A, Brzozka K, Lammens A, Lammens K, Fujita T, Conzelmann KK, Krug A, Hopfner KP. 2008. The C-terminal regulatory domain is the RNA 5=-triphosphate sensor of RIG-I. Mol Cell 29:169-179. http://dx.doi.org/10.1016/j.molcel.2007.10.032.
53. Lu C, Ranjith-Kumar CT, Hao L, Kao CC, Li P. 2011. Crystal structure of RIG-I C-terminal domain bound to blunt-ended double-strand RNA without 5= triphosphate. Nucleic Acids Res 39:1565-1575. http://dx.doi .org/10.1093/nar/gkq974.
54. Wang Y, Ludwig J, Schuberth C, Goldeck M, Schlee M, Li H, Juranek S, Sheng G, Micura R, Tuschl T, Hartmann G, Patel DJ. 2010. Structural and functional insights into 5=-pppRNApattern recognition by the innate immune receptor RIG-I. Nat Struct Mol Biol 17:781-787. http://dx.doi .org/10.1038/nsmb.1863.
55. Wang N, Liang Y, Devaraj S, Wang J, Lemon SM, Li K. 2009. Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells. J Virol 83:9824-9834. http://dx.doi.org/10.1128 /JVI.01125-09.
56. Zhang YL, Guo YJ, Bin L, Sun SH. 2009. Hepatitis C virus singlestranded RNA induces innate immunity via Toll-like receptor 7. J Hepatol 51:29-38. http://dx.doi.org/10.1016/j.jhep.2009.03.012.
57. Negash AA, Ramos HJ, Crochet N, Lau DT, Doehle B, Papic N, Delker DA, Jo J, Bertoletti A, Hagedorn CH, Gale M, Jr. 2013. IL-1beta production through the NLRP3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog 9:e1003330. http://dx.doi.org/10.1371/journal.ppat.1003330.
58. Israelow B, Narbus CM, Sourisseau M, Evans MJ. 2014. HepG2 cells mount an effective antiviral interferon-lambda based innate immune response to hepatitis C virus infection. Hepatology 60:1170-1179. http://dx .doi.org/10.1002/hep.27227.
59. Li K, Chen Z, Kato N, Gale M, Jr, Lemon SM. 2005. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J Biol Chem 280:16739-16747. http://dx.doi.org/10 .1074/jbc.M414139200.
60. Li XD, Sun L, Seth RB, Pineda G, Chen ZJ. 2005. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc Natl Acad Sci U S A 102: 17717-17722. http://dx.doi.org/10.1073/pnas.0508531102.
61. Uzri D, Gehrke L. 2009. Nucleotide sequences and modifications that determine RIG-I/RNA binding and signaling activities. J Virol 83:4174- 4184. http://dx.doi.org/10.1128/JVI.02449-08.
62. Giugliano S, Kriss M, Golden-Mason L, Dobrinskikh E, Stone AE, Soto-Gutierrez A, Mitchell A, Khetani SR, Yamane D, Stoddard M, Li H, Shaw GM, Edwards MG, Lemon SM, Gale M, Jr, Shah VH, Rosen HR. 2015. Hepatitis C virus infection induces autocrine interferon signaling by human liver endothelial cells and release of exosomes, which inhibits viral replication. Gastroenterology 148:392-402. http://dx.doi.org/10 .1053/j.gastro.2014.10.040.
63. Mitchell AM, Stone AE, Cheng L, Ballinger K, Edwards MG, Stoddard M, Li H, Golden-Mason L, Shaw GM, Khetani S, Rosen HR. 2015. Transmitted/founder hepatitis C viruses induce cell-type- and genotypespecific differences in innate signaling within the liver. mBio 6:e02510.