West Nile virus NS1 antagonizes interferon beta production by targeting RIG-I and MDA5

Journal of Virology

Volumn 91, Issue 18, 2017, Pages

  Zhang, Hong Lei ^a,b   Ye, Han Qing ^a   Liu, Si Qing ^a   Deng, Cheng Lin ^a   Li, Xiao Dan ^a,b   Shi, Pei Yong ^c   Zhang, Bo ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Flavivirus; IFN ; MDA5; NS1; RIG I; West Nile virus

Indexed keywords

BETA INTERFERON; DDX58 PROTEIN, HUMAN; IFIH1 PROTEIN, HUMAN; INTERFERON INDUCED HELICASE C DOMAIN CONTAINING PROTEIN 1; NONSTRUCTURAL PROTEIN 1, WEST NILE VIRUS; PROTEASOME; RETINOIC ACID INDUCIBLE PROTEIN I; VIRAL PROTEIN;

ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PATHOGENICITY; PROTEIN DEGRADATION; WEST NILE VIRUS;

ANIMALS; CELL LINE; DEAD BOX PROTEIN 58; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERFERON-BETA; INTERFERON-INDUCED HELICASE, IFIH1; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; VIRAL NONSTRUCTURAL PROTEINS; WEST NILE VIRUS;

EID: 85028339545     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02396-16     Document Type: Article

References (61)

1. Suthar MS, Aguirre S, Fernandez-Sesma A. 2013. Innate immune sensing of flaviviruses. PLoS Pathog 9:e1003541. https://doi.org/10.1371/journal.ppat.1003541
2. Shi PY, Tilgner M, Lo MK, Kent KA, Bernard KA. 2002. Infectious cDNA clone of the epidemic West Nile virus from New York City. J Virol 76:5847-5856. https://doi.org/10.1128/JVI.76.12.5847-5856.2002
3. Suthar MS, Diamond MS, Gale M, Jr. 2013. West Nile virus infection and immunity. Nat Rev Microbiol 11:115-128. https://doi.org/10.1038/ nrmicro2950
4. Lazear HM, Diamond MS. 2014. New insights into innate immune restriction of West Nile virus infection. Curr Opin Virol 11C:1-6
5. Zhang B, Dong H, Zhou Y, Shi PY. 2008. Genetic interactions among the West Nile virus methyltransferase, the RNA-dependent RNA polymerase, and the 5= stem-loop of genomic RNA. J Virol 82:7047-7058. https://doi.org/10.1128/JVI.00654-08
6. Zhang B, Dong H, Ye H, Tilgner M, Shi PY. 2010. Genetic analysis of West Nile virus containing a complete 3=CSI RNA deletion. Virology 408: 138-145. https://doi.org/10.1016/j.virol.2010.09.033
7. Shi PY. 2014. Flavivirus NS5 prevents the inSTATement of IFN. Cell Host Microbe 16:269-271. https://doi.org/10.1016/j.chom.2014.08.011
8. Munoz-Jordan JL, Sanchez-Burgos GG, Laurent-Rolle M, Garcia-Sastre A. 2003. Inhibition of interferon signaling by dengue virus. Proc Natl Acad Sci U S A 100:14333-14338. https://doi.org/10.1073/pnas.2335168100
9. Liu WJ, Chen HB, Wang XJ, Huang H, Khromykh AA. 2004. Analysis of adaptive mutations in Kunjin virus replicon RNA reveals a novel role for the flavivirus nonstructural protein NS2A in inhibition of beta interferon promoter-driven transcription. J Virol 78:12225-12235. https://doi.org/ 10.1128/JVI.78.22.12225-12235.2004
10. Munoz-Jordan JL, Laurent-Rolle M, Ashour J, Martinez-Sobrido L, Ashok M, Lipkin WI, Garcia-Sastre A. 2005. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J Virol 79:8004-8013. https://doi.org/10.1128/JVI.79.13.8004-8013.2005
11. Lin RJ, Chang BL, Yu HP, Liao CL, Lin YL. 2006. Blocking of interferoninduced Jak-Stat signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J Virol 80: 5908-5918. https://doi.org/10.1128/JVI.02714-05
12. Ashour J, Laurent-Rolle M, Shi PY, Garcia-Sastre A. 2009. NS5 of dengue virus mediates STAT2 binding and degradation. J Virol 83:5408-5418. https://doi.org/10.1128/JVI.02188-08
13. Laurent-Rolle M, Boer EF, Lubick KJ, Wolfinbarger JB, Carmody AB, Rockx B, Liu W, Ashour J, Shupert WL, Holbrook MR, Barrett AD, Mason PW, Bloom ME, Garcia-Sastre A, Khromykh AA, Best SM. 2010. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J Virol 84:3503-3515. https://doi.org/10.1128/JVI.01161-09
14. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol Rev 227:75-86. https://doi.org/10.1111/j.1600-065X.2008.00737.x
15. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820. https://doi.org/10.1016/j.cell.2010.01.022
16. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa C, Matsuura Y, Fujita T, Akira S. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105. https://doi.org/10.1038/nature04734
17. Zhong B, Yang Y, Li S, Wang YY, Li Y, Diao F, Lei C, He X, Zhang L, Tien P, Shu HB. 2008. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29:538-550. https://doi.org/10.1016/j.immuni.2008.09.003
18. Loo YM, Gale M, Jr. 2011. Immune signaling by RIG-I-like receptors. Immunity 34:680-692. https://doi.org/10.1016/j.immuni.2011.05.003
19. Cui J, Li Y, Zhu L, Liu D, Songyang Z, Wang HY, Wang RF. 2012. NLRP4 negatively regulates type I interferon signaling by targeting the kinase TBK1 for degradation via the ubiquitin ligase DTX4. Nat Immunol 13: 387-395. https://doi.org/10.1038/ni.2239
20. Luo H, Zhang Z, Zheng Z, Ke X, Zhang X, Li Q, Liu Y, Bai B, Mao P, Hu Q, Wang H. 2013. Human bocavirus VP2 upregulates IFN-beta pathway by inhibiting ring finger protein 125-mediated ubiquitination of retinoic acid-inducible gene-I. J Immunol 191:660-669. https://doi.org/10.4049/ jimmunol.1202933
21. Ding Z, Fang L, Jing H, Zeng S, Wang D, Liu L, Zhang H, Luo R, Chen H, Xiao S. 2014. Porcine epidemic diarrhea virus nucleocapsid protein antagonizes beta interferon production by sequestering the interaction between IRF3 and TBK1. J Virol 88:8936-8945. https://doi.org/10.1128/ JVI.00700-14
22. Kochs G, Garcia-Sastre A, Martinez-Sobrido L. 2007. Multiple antiinterferon actions of the influenza A virus NS1 protein. J Virol 81: 7011-7021. https://doi.org/10.1128/JVI.02581-06
23. Lefort S, Soucy-Faulkner A, Grandvaux N, Flamand L. 2007. Binding of Kaposi's sarcoma-associated herpesvirus K-bZIP to interferon-responsive factor 3 elements modulates antiviral gene expression. J Virol 81: 10950-10960. https://doi.org/10.1128/JVI.00183-07
24. Cloutier N, Flamand L. 2010. Kaposi sarcoma-associated herpesvirus latency-associated nuclear antigen inhibits interferon (IFN) beta expression by competing with IFN regulatory factor-3 for binding to IFNB promoter. J Biol Chem 285:7208-7221. https://doi.org/10.1074/jbc.M109.018838
25. Zhang Z, Zheng Z, Luo H, Meng J, Li H, Li Q, Zhang X, Ke X, Bai B, Mao P, Hu Q, Wang H. 2012. Human bocavirus NP1 inhibits IFN-beta production by blocking association of IFN regulatory factor 3 with IFNB promoter. J Immunol 189:1144-1153. https://doi.org/10.4049/jimmunol.1200096
26. Saira K, Zhou Y, Jones C. 2007. The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits beta interferon promoter activity. J Virol 81:3077-3086. https://doi.org/10.1128/JVI.02064-06
27. Zhu H, Zheng C, Xing J, Wang S, Li S, Lin R, Mossman KL. 2011. Varicella-zoster virus immediate-early protein ORF61 abrogates the IRF3-mediated innate immune response through degradation of activated IRF3. J Virol 85:11079-11089. https://doi.org/10.1128/JVI.05098-11
28. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, Goodbourn S, Randall RE. 2004. The V proteins of paramyxoviruses bind the IFNinducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A 101:17264-17269. https://doi.org/ 10.1073/pnas.0407639101
29. Xing J, Wang S, Lin R, Mossman KL, Zheng C. 2012. Herpes simplex virus 1 tegument protein US11 downmodulates the RLR signaling pathway via direct interaction with RIG-I and MDA-5. J Virol 86:3528-3540. https://doi.org/10.1128/JVI.06713-11
30. Chung KM, Liszewski MK, Nybakken G, Davis AE, Townsend RR, Fremont DH, Atkinson JP, Diamond MS. 2006. West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proc Natl Acad Sci U S A 103:19111-19116. https://doi.org/10.1073/pnas.0605668103
31. Wilson JR, de Sessions PF, Leon MA, Scholle F. 2008. West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J Virol 82: 8262-8271. https://doi.org/10.1128/JVI.00226-08
32. Youn S, Cho H, Fremont DH, Diamond MS. 2010. A short N-terminal peptide motif on flavivirus nonstructural protein NS1 modulates cellular targeting and immune recognition. J Virol 84:9516-9532. https://doi.org/10.1128/JVI.00775-10
33. Morrison CR, Scholle F. 2014. Abrogation of TLR3 inhibition by discrete amino acid changes in the C-terminal half of the West Nile virus NS1 protein. Virology 456-457:96-107
34. Baronti C, Sire J, de Lamballerie X, Querat G. 2010. Nonstructural NS1 proteins of several mosquito-borne flavivirus do not inhibit TLR3 signaling. Virology 404:319-330. https://doi.org/10.1016/j.virol.2010.05.020
35. Akey DL, Brown WC, Dutta S, Konwerski J, Jose J, Jurkiw TJ, DelProposto J, Ogata CM, Skiniotis G, Kuhn RJ, Smith JL. 2014. Flavivirus NS1 structures reveal surfaces for associations with membranes and the immune system. Science 343:881-885. https://doi.org/10.1126/science.1247749
36. Hale BG, Randall RE, Ortin J, Jackson D. 2008. The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89:2359-2376. https://doi.org/ 10.1099/vir.0.2008/004606-0
37. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4:491-496. https://doi.org/10.1038/ni921
38. Ramos HJ, Gale M, Jr. 2011. RIG-I like receptors and their signaling crosstalk in the regulation of antiviral immunity. Curr Opin Virol 1:167-176. https://doi.org/10.1016/j.coviro.2011.04.004
39. Shyu J, Liu H, Deng X, Hu C-D. 2006. Identification of new fluorescent protein fragments for bimolecular fluorescence complementation analysis under physiological conditions. Biotechniques 40:61-66. https://doi.org/10.2144/000112036
40. Lilyestrom W, Klein MG, Zhang R, Joachimiak A, Chen XS. 2006. Crystal structure of SV40 large T-antigen bound to p53: interplay between a viral oncoprotein and a cellular tumor suppressor. Genes Dev 20: 2373-2382. https://doi.org/10.1101/gad.1456306
41. Yu CY, Chang TH, Liang JJ, Chiang RL, Lee YL, Liao CL, Lin YL. 2012. Dengue virus targets the adaptor protein MITA to subvert host innate immunity. PLoS Pathog 8:e1002780. https://doi.org/10.1371/journal.ppat.1002780
42. Ding Q, Cao X, Lu J, Huang B, Liu YJ, Kato N, Shu HB, Zhong J. 2013. Hepatitis C virus NS4B blocks the interaction of STING and TBK1 to evade host innate immunity. J Hepatol 59:52-58. https://doi.org/10.1016/j.jhep.2013.03.019
43. Nitta S, Sakamoto N, Nakagawa M, Kakinuma S, Mishima K, Kusano-Kitazume A, Kiyohashi K, Murakawa M, Nishimura-Sakurai Y, Azuma S, Tasaka-Fujita M, Asahina Y, Yoneyama M, Fujita T, Watanabe M. 2013. Hepatitis C virus NS4B protein targets STING and abrogates RIG-Imediated type I interferon-dependent innate immunity. Hepatology 57:46-58. https://doi.org/10.1002/hep.26017
44. Dalrymple NA, Cimica V, Mackow ER. 2015. Dengue virus NS proteins inhibit RIG-I/MAVS signaling by blocking TBK1/IRF3 phosphorylation: dengue virus serotype 1 NS4A is a unique interferon-regulating virulence determinant. mBio 6:e00553-15. https://doi.org/10.1128/mBio.00553-15
45. Chang TH, Liao CL, Lin YL. 2006. Flavivirus induces interferon-beta gene expression through a pathway involving RIG-I-dependent IRF-3 and PI3K-dependent NF-kappaB activation. Microbes Infect 8:157-171. https://doi.org/10.1016/j.micinf.2005.06.014
46. Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M, Jr. 2008. Establishment and maintenance of the innate antiviral response to West Nile virus involves both RIG-I and MDA5 signaling through IPS-1. J Virol 82:609-616. https://doi.org/10.1128/JVI.01305-07
47. 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. https://doi.org/10.1128/JVI.01265-06
48. Lei X, Liu X, Ma Y, Sun Z, Yang Y, Jin Q, He B, Wang J. 2010. 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 84:8051-8061. https://doi.org/10.1128/JVI.02491-09
49. Ling Z, Tran KC, Teng MN. 2009. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J Virol 83:3734-3742. https://doi.org/10.1128/JVI.02434-08
50. Fan L, Briese T, Lipkin WI. 2010. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J Virol 84: 1785-1791. https://doi.org/10.1128/JVI.01362-09
51. Bhoj VG, Chen ZJ. 2009. Ubiquitylation in innate and adaptive immunity. Nature 458:430-437. https://doi.org/10.1038/nature07959
52. Oshiumi H, Miyashita M, Inoue N, Okabe M, Matsumoto M, Seya T. 2010. The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8:496-509. https://doi.org/10.1016/j.chom.2010.11.008
53. Jiang X, Kinch LN, Brautigam CA, Chen X, Du F, Grishin NV, Chen ZJ. 2012. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36: 959-973. https://doi.org/10.1016/j.immuni.2012.03.022
54. Oshiumi H, Miyashita M, Matsumoto M, Seya T. 2013. A distinct role of Riplet-mediated K63-linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog 9:e1003533. https://doi.org/10.1371/journal.ppat.1003533
55. Crook KR, Miller-Kittrell M, Morrison CR, Scholle F. 2014. Modulation of innate immune signaling by the secreted form of the West Nile virus NS1 glycoprotein. Virology 458-459:172-182
56. Xie X, Gayen S, Kang C, Yuan Z, Shi PY. 2013. Membrane topology and function of dengue virus NS2A protein. J Virol 87:4609-4622. https:// doi.org/10.1128/JVI.02424-12
57. Li XD, Li XF, Ye HQ, Deng CL, Ye Q, Shan C, Shang BD, Xu LL, Li SH, Cao SB, Yuan ZM, Shi PY, Qin CF, Zhang B. 2014. Recovery of a chemically synthesized Japanese encephalitis virus reveals two critical adaptive mutations in NS2B and NS4A. J Gen Virol 95:806-815. https://doi.org/ 10.1099/vir.0.061838-0
58. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90. https://doi.org/ 10.1038/nbt0102-87
59. Fan JY, Cui ZQ, Wei HP, Zhang ZP, Zhou YF, Wang YP, Zhang XE. 2008. Split mCherry as a new red bimolecular fluorescence complementation system for visualizing protein-protein interactions in living cells. Biochem Biophys Res Commun 367:47-53. https://doi.org/10.1016/j.bbrc.2007.12.101
60. Ehrhardt C, Kardinal C, Wurzer WJ, Wolff T, von Eichel-Streiber C, Pleschka S, Planz O, Ludwig S. 2004. Rac1 and PAK1 are upstream of IKK-epsilon and TBK-1 in the viral activation of interferon regulatory factor-3. FEBS Lett 567:230-238. https://doi.org/10.1016/j.febslet.2004.04.069
61. 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. https://doi.org/10.1038/ni1087