Interferon-inducible protein IFI35 negatively regulates RIG-I antiviral signaling and supports vesicular stomatitis virus replication

Journal of Virology

Volumn 88, Issue 6, 2014, Pages 3103-3113

  Das, Anshuman ^a   Dinh, Phat X ^a   Panda, Debasis ^a,b   Pattnaik, Asit K ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON INDUCIBLE PROTEIN 35; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERFERON STIMULATED GENE 56 PROTEIN; M PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIVIRAL SIGNALING; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; GENE EXPRESSION; GENETIC SCREENING; GENOME ANALYSIS; IMMUNE RESPONSE; INNATE IMMUNITY; INTERFERON PRODUCTION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PSORIASIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; UBIQUITINATION; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS INHIBITION; VIRUS REPLICATION;

DEAD-BOX RNA HELICASES; DOWN-REGULATION; HUMANS; INTERFERON-BETA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN BINDING; VESICULAR STOMATITIS; VESICULAR STOMATITIS INDIANA VIRUS; VIRUS REPLICATION;

EID: 84894545130     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03202-13     Document Type: Article

References (58)

1. Gerlier D, Lyles DS. 2011. Interplay between innate immunity and negative-strand RNA viruses: towards a rational model. Microbiol. Mol. Biol. Rev. 75:468-490. http://dx.doi.org/10.1128/MMBR.00007-11.
2. Rieder M, Conzelmann KK. 2009. Rhabdovirus evasion of the interferon system. J. Interferon Cytokine Res. 29:499-509. http://dx.doi.org/10.1089/jir.2009.0068.
3. von Kobbe C, van Deursen JM, Rodrigues JP, Sitterlin D, Bachi A, Wu X, Wilm M, Carmo-Fonseca M, Izaurralde E. 2000. Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol. Cell 6:1243-1252. http://dx.doi.org/10.1016/S1097-2765(00)00120-9.
4. Faria PA, Chakraborty P, Levay A, Barber GN, Ezelle HJ, Enninga J, Arana C, van Deursen J, Fontoura BM. 2005. VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol. Cell 17:93-102. http://dx.doi.org/10.1016/j.molcel.2004.11.023.
5. Her LS, Lund E, Dahlberg JE. 1997. Inhibition of Ran guanosine triphosphatase-dependent nuclear transport by the matrix protein of vesicular stomatitis virus. Science 276:1845-1848. http://dx.doi.org/10.1126/sci ence.276.5320.1845.
6. Lyles DS. 2000. Cytopathogenesis and inhibition of host gene expression by RNA viruses. Microbiol. Mol. Biol. Rev. 64:709-724. http://dx.doi.org/10.1128/MMBR.64.4.709-724.2000.
7. Panda D, Das A, Dinh PX, Subramaniam S, Nayak D, Barrows NJ, Pearson JL, Thompson J, Kelly DL, Ladunga I, Pattnaik AK. 2011. RNAi screening reveals requirement for host cell secretory pathway in infection by diverse families of negative-strand RNA viruses. Proc. Natl. Acad. Sci. U.S.A. 108:19036-19041. http://dx.doi.org/10.1073/pnas.1113643108.
8. Bange FC, Vogel U, Flohr T, Kiekenbeck M, Denecke B, Bottger EC. 1994. IFP 35 is an interferon-induced leucine zipper protein that undergoes interferon-regulated cellular redistribution. J. Biol. Chem. 269:1091-1098.
9. Wang X, Johansen LM, Tae HJ, Taparowsky EJ. 1996. IFP 35 forms complexes with B-ATF, a member of the AP1 family of transcription factors. Biochem. Biophys. Res. Commun. 229:316-322. http://dx.doi.org/10.1006/bbrc.1996.1799.
10. Zhou X, Liao J, Meyerdierks A, Feng L, Naumovski L, Bottger EC, Omary MB. 2000. Interferon-alpha induces nmi-IFP35 heterodimeric complex formation that is affected by the phosphorylation of IFP35. J. Biol. Chem. 275: 21364-21371. http://dx.doi.org/10.1074/jbc.M003177200.
11. Chen J, Shpall RL, Meyerdierks A, Hagemeier M, Bottger EC, Naumovski L. 2000. Interferon-inducible Myc/STAT-interacting protein Nmi associates with IFP 35 into a high molecular mass complex and inhibits proteasome-mediated degradation of IFP 35. J. Biol. Chem. 275: 36278-36284. http://dx.doi.org/10.1074/jbc.M006975200.
12. Li Y, Li C, Xue P, Zhong B, Mao AP, Ran Y, Chen H, Wang YY, Yang F, Shu HB. 2009. ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proc. Natl. Acad. Sci. U.S.A. 106:7945-7950. http://dx.doi.org/10.1073/pnas.0900818106.
13. Mankouri J, Fragkoudis R, Richards KH, Wetherill LF, Harris M, Kohl A, Elliott RM, Macdonald A. 2010. Optineurin negatively regulates the induction of IFNbeta in response to RNA virus infection. PLoS Pathog. 6:e1000778. http://dx.doi.org/10.1371/journal.ppat.1000778.
14. Rothenfusser S, Goutagny N, DiPerna G, Gong M, Monks BG, Schoenemeyer A, Yamamoto M, Akira S, Fitzgerald KA. 2005. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175:5260-5268.
15. Xu L, Xiao N, Liu F, Ren H, Gu J. 2009. Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria. Proc. Natl. Acad. Sci. U.S.A. 106:1530-1535. http://dx.doi.org/10.1073/pnas.0811029106.
16. Carty M, Goodbody R, Schroder M, Stack J, Moynagh PN, Bowie AG. 2006. The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat. Immunol. 7:1074-1081. http://dx.doi.org/10.1038/ni1382.
17. Kim MJ, Hwang SY, Imaizumi T, Yoo JY. 2008. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J. Virol. 82:1474-1483. http://dx.doi.org/10.1128/JVI.01650-07.
18. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Koonin EV, Dixit VM. 2004. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430:694-699. http://dx.doi.org/10.1038/nature02794.
19. Arimoto K, Takahashi H, Hishiki T, Konishi H, Fujita T, Shimotohno K. 2007. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. U.S.A. 104:7500-7505. http://dx.doi.org/10.1073/pnas.0611551104.
20. You F, Sun H, Zhou X, Sun W, Liang S, Zhai Z, Jiang Z. 2009. PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4. Nat. Immunol. 10:1300-1308. http://dx.doi.org/10.1038/ni.1815.
21. Higgs R, Ni Gabhann J, Ben Larbi N, Breen EP, Fitzgerald KA, Jefferies CA. 2008. The E3 ubiquitin ligase Ro52 negatively regulates IFN-beta production post-pathogen recognition by polyubiquitin-mediated degradation of IRF3. J. Immunol. 181:1780-1786.
22. Nakhaei P, Mesplede T, Solis M, Sun Q, Zhao T, Yang L, Chuang TH, Ware CF, Lin R, Hiscott J. 2009. The E3 ubiquitin ligase Triad3A negatively regulates the RIG-I/MAVS signaling pathway by targeting TRAF3 for degradation. PLoS Pathog. 5:e1000650. http://dx.doi.org/10.1371/jou rnal.ppat.1000650.
23. Richards KH, Macdonald A. 2011. Putting the brakes on the anti-viral response: negative regulators of type I interferon (IFN) production. Microbes Infect. 13:291-302. http://dx.doi.org/10.1016/j.micinf.2010.12.007.
24. Wilkins C, Gale M, Jr. 2010. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 22:41-47. http://dx.doi.org/10.1016/j.coi.2009.12.003.
25. 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.
26. Maelfait J, Beyaert R. 2012. Emerging role of ubiquitination in antiviral RIG-I signaling. Microbiol. Mol. Biol. Rev. 76:33-45. http://dx.doi.org/10.1128/MMBR.05012-11.
27. Dixit E, Kagan JC. 2013. Intracellular pathogen detection by RIG-I-like receptors. Adv. Immunol. 117:99-125. http://dx.doi.org/10.1016/B978-0-12-410524-9.00004-9.
28. Wies E, Wang MK, Maharaj NP, Chen K, Zhou S, Finberg RW, Gack MU. 2013. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 38:437-449. http://dx.doi.org/10.1016/j.immuni.2012.11.018.
29. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446:916-920. http://dx.doi.org/10.1038/nature05732.
30. Nistal-Villan E, Gack MU, Martinez-Delgado G, Maharaj NP, Inn KS, Yang H, Wang R, Aggarwal AK, Jung JU, Garcia-Sastre A. 2010. Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-beta production. J. Biol. Chem. 285:20252-20261. http://dx.doi.org/10.1074/jbc.M109.089912.
31. Gack MU, Nistal-Villan E, Inn KS, Garcia-Sastre A, Jung JU. 2010. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J. Virol. 84:3220-3229. http://dx.doi.org/10.1128/JVI.02241-09.
32. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acidinducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205:1601-1610. http://dx.doi.org/10.1084/jem.20080091.
33. Das SC, Nayak D, Zhou Y, Pattnaik AK. 2006. Visualization of intracellular transport of vesicular stomatitis virus nucleocapsids in living cells. J. Virol. 80:6368-6377. http://dx.doi.org/10.1128/JVI.00211-06.
34. Das SC, Pattnaik AK. 2005. Role of the hypervariable hinge region of phosphoprotein P of vesicular stomatitis virus in viral RNA synthesis and assembly of infectious virus particles. J. Virol. 79:8101-8112. http://dx.doi.org/10.1128/JVI.79.13.8101-8112.2005.
35. Dinh PX, Beura LK, Panda D, Das A, Pattnaik AK. 2011. Antagonistic effects of cellular poly(C) binding proteins on vesicular stomatitis virus gene expression. J. Virol. 85:9459-9471. http://dx.doi.org/10.1128/JVI.05179-11.
36. Guo J, Peters KL, Sen GC. 2000. Induction of the human protein P56 by interferon, double-stranded RNA, or virus infection. Virology 267:209-219. http://dx.doi.org/10.1006/viro.1999.0135.
37. 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.
38. Beura LK, Sarkar SN, Kwon B, Subramaniam S, Jones C, Pattnaik AK, Osorio FA. 2010. Porcine reproductive and respiratory syndrome virus nonstructural protein 1beta modulates host innate immune response by antagonizing IRF3 activation. J. Virol. 84:1574-1584. http://dx.doi.org/10.1128/JVI.01326-09.
39. Sato S, Sugiyama M, Yamamoto M, Watanabe Y, Kawai T, Takeda K, Akira S. 2003. Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171:4304-4310.
40. Lim KL, Chew KC, Tan JM, Wang C, Chung KK, Zhang Y, Tanaka Y, Smith W, Engelender S, Ross CA, Dawson VL, Dawson TM. 2005. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25:2002-2009. http://dx.doi.org/10.1523/JNEUROSCI.4474-04.2005.
41. Panda D, Dinh PX, Beura LK, Pattnaik AK. 2010. Induction of interferon and interferon signaling pathways by replication of defective interfering particle RNA in cells constitutively expressing vesicular stomatitis virus replication proteins. J. Virol. 84:4826-4831. http://dx.doi.org/10.1128/JVI.02701-09.
42. Eisenacher K, Krug A. 2012. Regulation of RLR-mediated innate immune signaling-it is all about keeping the balance. Eur. J. Cell Biol. 91:36-47. http://dx.doi.org/10.1016/j.ejcb.2011.01.011.
43. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47. http://dx.doi.org/10.1099/vir.0.83391-0.
44. Lin R, Heylbroeck C, Pitha PM, Hiscott J. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18:2986-2996.
45. Dragan AI, Hargreaves VV, Makeyeva EN, Privalov PL. 2007. Mechanisms of activation of interferon regulator factor 3: the role of C-terminal domain phosphorylation in IRF-3 dimerization and DNA binding. Nucleic Acids Res. 35:3525-3534. http://dx.doi.org/10.1093/nar/gkm142.
46. Marie I, Durbin JE, Levy DE. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17:6660-6669. http://dx.doi.org/10.1093/emboj/17.22.6660.
47. Chen W, Han C, Xie B, Hu X, Yu Q, Shi L, Wang Q, Li D, Wang J, Zheng P, Liu Y, Cao X. 2013. Induction of Siglec-G by RNA viruses inhibits the innate immune response by promoting RIG-I degradation. Cell 152:467-478. http://dx.doi.org/10.1016/j.cell.2013.01.011.
48. Bibeau-Poirier A, Servant MJ. 2008. Roles of ubiquitination in patternrecognition receptors and type I interferon receptor signaling. Cytokine 43:359-367. http://dx.doi.org/10.1016/j.cyto.2008.07.012.
49. Tan J, Qiao W, Wang J, Xu F, Li Y, Zhou J, Chen Q, Geng Y. 2008. IFP35 is involved in the antiviral function of interferon by association with the viral tas transactivator of bovine foamy virus. J. Virol. 82:4275-4283. http://dx.doi.org/10.1128/JVI.02249-07.
50. Sabile A, Rhodes-Feuillette A, Jaoui FZ, Tobaly-Tapiero J, Giron ML, Lasneret J, Peries J, Canivet M. 1996. In vitro studies on interferoninducing capacity and sensitivity to IFN of human foamy virus. Res. Virol. 147:29-37. http://dx.doi.org/10.1016/0923-2516(96)80237-8.
51. Rua R, Lepelley A, Gessain A, Schwartz O. 2012. Innate sensing of foamy viruses by human hematopoietic cells. J. Virol. 86:909-918. http://dx.doi.org/10.1128/JVI.06235-11.
52. Parvatiyar K, Barber GN, Harhaj EW. 2010. TAX1BP1 and A20 inhibit antiviral signaling by targeting TBK1-IKKi kinases. J. Biol. Chem. 285: 14999-15009. http://dx.doi.org/10.1074/jbc.M110.109819.
53. Friedman CS, O'Donnell MA, Legarda-Addison D, Ng A, Cardenas WB, Yount JS, Moran TM, Basler CF, Komuro A, Horvath CM, Xavier R, Ting AT. 2008. The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep. 9:930-936. http://dx.doi.org/10.1038/embor.2008.136.
54. Metzger MB, Hristova VA, Weissman AM. 2012. HECT and RING finger families of E3 ubiquitin ligases at a glance. J. Cell Sci. 125:531-537. http://dx.doi.org/10.1242/jcs.091777.
55. Maharaj NP, Wies E, Stoll A, Gack MU. 2012. Conventional protein kinase C-alpha (PKC-alpha) and PKC-beta negatively regulate RIG-I antiviral signal transduction. J. Virol. 86:1358-1371. http://dx.doi.org/10.1128/JVI.06543-11.
56. Wang J, Yang B, Hu Y, Zheng Y, Zhou H, Wang Y, Ma Y, Mao K, Yang L, Lin G, Ji Y, Wu X, Sun B. 2013. Negative regulation of Nmi on virus-triggered type I IFN production by targeting IRF7. J. Immunol. 191: 3393-3399. http://dx.doi.org/10.4049/jimmunol.1300740.
57. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. 1990. The protein Id: a negative regulator of helix-loop-helixDNAbinding proteins. Cell 61:49-59. http://dx.doi.org/10.1016/0092-8674(90)90214-Y.
58. Pagliuca A, Bartoli PC, Saccone S, Della Valle G, Lania L. 1995. Molecular cloning of ID4, a novel dominant negative helix-loop-helix human gene on chromosome 6p21.3-p22. Genomics 27:200-203. http://dx.doi.org/10.1006/geno.1995.1026.