Herpes simplex virus 1 UL36USP antagonizes type I interferon-mediated antiviral innate immunity

Journal of Virology

Volumn 92, Issue 19, 2018, Pages

  Yuan, Hui ^a,b   You, Jia ^a   You, Hongjuan ^c   Zheng, Chunfu ^a,d  

^a FUJIAN MEDICAL UNIVERSITY   (China)

^b JIANGNAN UNIVERSITY   (China)

^c XUZHOU MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

HSV 1; IFNAR2; Type I IFN mediated signaling; UL36USP

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; ALPHA INTERFERON; BETA INTERFERON; IFNAR1 PROTEIN, HUMAN; IFNAR2 PROTEIN, HUMAN; INTERFERON REGULATORY FACTOR 9; JAK1 PROTEIN, HUMAN; JANUS KINASE 1; SMALL INTERFERING RNA; STAT PROTEIN; UL36 PROTEIN, HUMAN HERPESVIRUS 1; VIRAL PROTEIN;

ANIMAL; CHLOROCEBUS AETHIOPS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; HUMAN ALPHAHERPESVIRUS 1; IMMUNE EVASION; IMMUNOLOGY; INNATE IMMUNITY; SIGNAL TRANSDUCTION; VERO CELL LINE;

ANIMALS; CERCOPITHECUS AETHIOPS; GENE EXPRESSION REGULATION; HEK293 CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; INTERFERON-ALPHA; INTERFERON-BETA; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; JANUS KINASE 1; RECEPTOR, INTERFERON ALPHA-BETA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; VERO CELLS; VIRAL PROTEINS;

EID: 85053421210     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01161-18     Document Type: Article

References (52)

1. Honda K, Takaoka A, Taniguchi T. 2006. Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25:349–360. https://doi.org/10.1016/j.immuni.2006.08.009.
2. Takaoka A, Yanai H. 2006. Interferon signalling network in innate defence. Cell Microbiol 8:907–922. https://doi.org/10.1111/j.1462-5822.2006.00716.x.
3. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR, Stark GR. 2007. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 6:975–990. https://doi.org/10.1038/nrd2422.
4. de Weerd NA, Nguyen T. 2012. The interferons and their receptors–distribution and regulation. Immunol Cell Biol 90:483–491. https://doi.org/10.1038/icb.2012.9.
5. Gonzalez-Navajas JM, Lee J, David M, Raz E. 2012. Immunomodulatory functions of type I interferons. Nat Rev Immunol 12:125–135. https://doi.org/10.1038/nri3133.
6. Platanias LC. 2005. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5:375–386. https://doi.org/10.1038/nri1604.
7. Majoros A, Platanitis E, Kernbauer-Holzl E, Rosebrock F, Muller M, Decker T. 2017. Canonical and non-canonical aspects of JAK-STAT signaling: lessons from interferons for cytokine responses. Front Immunol 8:29. https://doi.org/10.3389/fimmu.2017.00029.
8. Yan N, Chen ZJ. 2012. Intrinsic antiviral immunity. Nat Immunol 13: 214–222. https://doi.org/10.1038/ni.2229.
9. Nan Y, Wu C, Zhang YJ. 2017. Interplay between Janus kinase/signal transducer and activator of transcription signaling activated by type I interferons and viral antagonism. Front Immunol 8:1758. https://doi.org/10.3389/fimmu.2017.01758.
10. McGeoch DJ, Dalrymple MA, Davison AJ, Dolan A, Frame MC, McNab D, Perry LJ, Scott JE, Taylor P. 1988. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol 69(Part 7):1531–1574.
11. McGeoch DJ, Cook S. 1994. Molecular phylogeny of the alphaherpesviri-nae subfamily and a proposed evolutionary timescale. J Mol Biol 238: 9–22. https://doi.org/10.1006/jmbi.1994.1264.
12. Johnson KE, Knipe DM. 2010. Herpes simplex virus-1 infection causes the secretion of a type I interferon-antagonizing protein and inhibits signaling at or before Jak-1 activation. Virology 396:21–29. https://doi.org/10.1016/j.virol.2009.09.021.
13. Chee AV, Roizman B. 2004. Herpes simplex virus 1 gene products occlude the interferon signaling pathway at multiple sites. J Virol 78: 4185–4196. https://doi.org/10.1128/JVI.78.8.4185-4196.2004.
14. Frey KG, Ahmed CM, Dabelic R, Jager LD, Noon-Song EN, Haider SM, Johnson HM, Bigley NJ. 2009. HSV-1-induced SOCS-1 expression in keratinocytes: use of a SOCS-1 antagonist to block a novel mechanism of viral immune evasion. J Immunol 183:1253–1262. https://doi.org/10.4049/jimmunol.0900570.
15. Kattenhorn LM, Korbel GA, Kessler BM, Spooner E, Ploegh HL. 2005. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol Cell 19:547–557. https://doi.org/10.1016/j.molcel.2005.07.003.
16. Bolstad M, Abaitua F, Crump CM, O’Hare P. 2011. Autocatalytic activity of the ubiquitin-specific protease domain of herpes simplex virus 1 VP1-2. J Virol 85:8738 – 8751. https://doi.org/10.1128/JVI.00798-11.
17. Wang S, Wang K, Li J, Zheng C. 2013. Herpes simplex virus 1 ubiquitin-specific protease UL36 inhibits beta interferon production by deubiquitinating TRAF3. J Virol 87:11851–11860. https://doi.org/10.1128/JVI.01211-13.
18. Fensterl V, Chattopadhyay S, Sen GC. 2015. No love lost between viruses and interferons. Annu Rev Virol 2:549–572. https://doi.org/10.1146/annurev-virology-100114-055249.
19. Su C, Zhan G, Zheng C. 2016. Evasion of host antiviral innate immunity by HSV-1, an update. Virol J 13:38. https://doi.org/10.1186/s12985-016-0495-5.
20. Peri P, Mattila RK, Kantola H, Broberg E, Karttunen HS, Waris M, Vuorinen T, Hukkanen V. 2008. Herpes simplex virus type 1 Us3 gene deletion influences toll-like receptor responses in cultured monocytic cells. Virol J 5:140. https://doi.org/10.1186/1743-422X-5-140.
21. Wang S, Wang K, Lin R, Zheng C. 2013. Herpes simplex virus 1 serine/ threonine kinase US3 hyperphosphorylates IRF3 and inhibits beta interferon production. J Virol 87:12814–12827. https://doi.org/10.1128/JVI.02355-13.
22. Melroe GT, DeLuca NA, Knipe DM. 2004. Herpes simplex virus 1 has multiple mechanisms for blocking virus-induced interferon production. J Virol 78:8411–8420. https://doi.org/10.1128/JVI.78.16.8411-8420.2004.
23. Melroe GT, Silva L, Schaffer PA, Knipe DM. 2007. Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-beta induction. Virology 360:305–321. https://doi.org/10.1016/j.virol.2006.10.028.
24. 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.
25. Su C, Zheng C. 2017. Herpes simplex virus 1 abrogates the cGAS/STING-mediated cytosolic DNA-sensing pathway via its virion host shutoff protein, UL41. J Virol 91:e02414-16. https://doi.org/10.1128/JVI.02414-16.
26. Xing J, Ni L, Wang S, Wang K, Lin R, Zheng C. 2013. Herpes simplex virus 1-encoded tegument protein VP16 abrogates the production of beta interferon (IFN) by inhibiting NF-kappaB activation and blocking IFN regulatory factor 3 to recruit its coactivator CBP. J Virol 87:9788–9801. https://doi.org/10.1128/JVI.01440-13.
27. Shen G, Wang K, Wang S, Cai M, Li ML, Zheng C. 2014. Herpes simplex virus 1 counteracts viperin via its virion host shutoff protein UL41. J Virol 88:12163–12166. https://doi.org/10.1128/JVI.01380-14.
28. Su C, Zhang J, Zheng C. 2015. Herpes simplex virus 1 UL41 protein abrogates the antiviral activity of hZAP by degrading its mRNA. Virol J 12:203. https://doi.org/10.1186/s12985-015-0433-y.
29. Zenner HL, Mauricio R, Banting G, Crump CM. 2013. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity. J Virol 87:13115–13123. https://doi.org/10.1128/JVI.02167-13.
30. Jiang Z, Su C, Zheng C. 2016. Herpes simplex virus 1 tegument protein UL41 counteracts IFIT3 antiviral innate immunity. J Virol 90: 11056–11061. https://doi.org/10.1128/JVI.01672-16.
31. You H, Yuan H, Fu W, Su C, Wang W, Cheng T, Zheng C. 2017. Herpes simplex virus type 1 abrogates the antiviral activity of Ch25h via its virion host shutoff protein. Antiviral Res 143:69–73. https://doi.org/10.1016/j.antiviral.2017.04.004.
32. Johnson KE, Song B, Knipe DM. 2008. Role for herpes simplex virus 1 ICP27 in the inhibition of type I interferon signaling. Virology 374: 487–494. https://doi.org/10.1016/j.virol.2008.01.001.
33. Luxton GW, Lee JI, Haverlock-Moyns S, Schober JM, Smith GA. 2006. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J Virol 80:201–209. https://doi.org/10.1128/JVI.80.1.201-209.2006.
34. Sandbaumhuter M, Dohner K, Schipke J, Binz A, Pohlmann A, Sodeik B, Bauerfeind R. 2013. Cytosolic herpes simplex virus capsids not only require binding inner tegument protein pUL36 but also pUL37 for active transport prior to secondary envelopment. Cell Microbiol 15:248–269. https://doi.org/10.1111/cmi.12075.
35. Abaitua F, Hollinshead M, Bolstad M, Crump CM, O’Hare P. 2012. A Nuclear localization signal in herpesvirus protein VP1-2 is essential for infection via capsid routing to the nuclear pore. J Virol 86:8998–9014. https://doi.org/10.1128/JVI.01209-12.
36. Roberts AP, Abaitua F, O’Hare P, McNab D, Rixon FJ, Pasdeloup D. 2009. Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J Virol 83:105–116. https://doi.org/10.1128/JVI.01032-08.
37. Desai PJ. 2000. A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J Virol 74:11608–11618. https://doi.org/10 .1128/JVI.74.24.11608-11618.2000.
38. Kim ET, Oh SE, Lee YO, Gibson W, Ahn JH. 2009. Cleavage specificity of the UL48 deubiquitinating protease activity of human cytomegalovirus and the growth of an active-site mutant virus in cultured cells. J Virol 83:12046–12056. https://doi.org/10.1128/JVI.00411-09.
39. Ye R, Su C, Xu H, Zheng C. 2017. Herpes simplex virus 1 ubiquitin-specific protease UL36 abrogates NF-kappaB activation in DNA sensing signal pathway. J Virol 91:e02417-16. https://doi.org/10.1128/JVI.02417-16.
40. Symons JA, Alcami A, Smith GL. 1995. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81:551–560. https://doi.org/10.1016/0092-8674(95)90076-4.
41. Alcami A, Symons JA, Smith GL. 2000. The vaccinia virus soluble alpha/ beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J Virol 74:11230–11239. https://doi.org/10.1128/JVI.74.23.11230-11239.2000.
42. Yokota S, Saito H, Kubota T, Yokosawa N, Amano K, Fujii N. 2003. Measles virus suppresses interferon-alpha signaling pathway: suppression of Jak1 phosphorylation and association of viral accessory proteins, C and V, with interferon-alpha receptor complex. Virology 306:135–146. https://doi.org/10.1016/S0042-6822(02)00026-0.
43. Bisson SA, Page AL, Ganem D. 2009. A Kaposi’s sarcoma-associated herpesvirus protein that forms inhibitory complexes with type I interferon receptor subunits, Jak and STAT proteins, and blocks interferon-mediated signal transduction. J Virol 83:5056–5066. https://doi.org/10.1128/JVI.02516-08.
44. Shah KM, Stewart SE, Wei W, Woodman CB, O’Neil JD, Dawson CW, Young LS. 2009. The EBV-encoded latent membrane proteins, LMP2A and LMP2B, limit the actions of interferon by targeting interferon receptors for degradation. Oncogene 28:3903–3914. https://doi.org/10.1038/onc.2009.249.
45. Xia C, Vijayan M, Pritzl CJ, Fuchs SY, McDermott AB, Hahm B. 2015. Hemagglutinin of influenza A virus antagonizes type I interferon (IFN) responses by inducing degradation of type I IFN receptor 1. J Virol 90:2403–2417. https://doi.org/10.1128/JVI.02749-15.
46. Zhang R, Xu A, Qin C, Zhang Q, Chen S, Lang Y, Wang M, Li C, Feng W, Zhang R, Jiang Z, Tang J. 2017. Pseudorabies virus dUTPase UL50 induces lysosomal degradation of type I interferon receptor 1 and antagonizes the alpha interferon response. J Virol 91:e01148-17. https://doi.org/10.1128/JVI.01148-17.
47. Xing J, Wang S, Lin F, Pan W, Hu CD, Zheng C. 2011. Comprehensive characterization of interaction complexes of herpes simplex virus type 1 ICP22, UL3, UL4, and UL205. J Virol 85:1881–1886.
48. Saleh AZ, Fang AT, Arch AE, Neupane D, El Fiky A, Krolewski JJ. 2004. Regulated proteolysis of the IFNaR2 subunit of the interferon-alpha receptor. Oncogene 23:7076–7086. https://doi.org/10.1038/sj.onc.1207955.
49. Jia H, Song L, Cong Q, Wang J, Xu H, Chu Y, Li Q, Zhang Y, Zou X, Zhang C, Chin YE, Zhang X, Li Z, Zhu K, Wang B, Peng H, Hou Z. 2017. The LIM protein AJUBA promotes colorectal cancer cell survival through suppression of JAK1/STAT1/IFIT2 network. Oncogene 36:2655–2666. https://doi.org/10.1038/onc.2016.418.
50. Lin R, Yang L, Nakhaei P, Sun Q, Sharif-Askari E, Julkunen I, Hiscott J. 2006. Negative regulation of the retinoic acid-inducible gene I-induced antiviral state by the ubiquitin-editing protein A20. J Biol Chem 281: 2095–2103. https://doi.org/10.1074/jbc.M510326200.
51. 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.
52. Jordan M, Schallhorn A, Wurm FM. 1996. Transfecting mammalian cells: optimization of critical parameters affecting calcium-phosphate precipitate formation. Nucleic Acids Res 24:596–601. https://doi.org/10.1093/nar/24.4.596.