Herpes simplex virus 1 serine protease VP24 blocks the DNA-sensing signal pathway by abrogating activation of interferon regulatory factor 3

Journal of Virology

Volumn 90, Issue 12, 2016, Pages 5824-5829

  Zhang, Dandan ^a   Su, Chenhe ^a   Zheng, Chunfu ^a,b  

^a SOOCHOW UNIVERSITY   (China)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; BINDING PROTEIN; CYCLIC GMP AMP SYNTHASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; PROTEIN VP24; SYNTHETASE; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; VIRUS PROTEIN; DNA; IRF3 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; SCAFFOLD PROTEIN, HERPES SIMPLEX VIRUS-1; SMALL INTERFERING RNA; TBK1 PROTEIN, HUMAN; VIRAL PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIMERIZATION; DOWN REGULATION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; VIRUS REPLICATION; CELL LINE; CYTOLOGY; FIBROBLAST; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; IMMUNE EVASION; MALE; METABOLISM; PREPUCE; PROMOTER REGION; VIROLOGY;

CELL LINE; DNA; FIBROBLASTS; FORESKIN; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; MALE; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84971373915     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00186-16     Document Type: Article

References (52)

1. Pichlmair A, Reise Sousa C. 2007. Innate recognition of viruses. Immunity 27:370-383. http://dx.doi.org/10.1016/j.immuni.2007.08.012.
2. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol Rev 227:75-86. http://dx.doi.org/10.1111/j.1600-065X.2008.00737.x.
3. Vandevenne P, Sadzot-Delvaux C, Piette J. 2010. Innate immune response and viral interference strategies developed by human herpesviruses. Biochem Pharmacol 80:1955-1972. http://dx.doi.org/10.1016/j.bcp.2010.07.001.
4. Sun L, Wu J, Du F, Chen X, Chen ZJ. 2013. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339:786-791. http://dx.doi.org/10.1126/science.1232458.
5. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, Bowie AG. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997-1004. http://dx.doi.org/10.1038/ni.1932.
6. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. 2011. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12:959-965. http://dx.doi.org/10.1038/ni.2091.
7. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, Lu Y, Miyagishi M, Kodama T, Honda K, Ohba Y, Taniguchi T. 2007. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448:501-505. http://dx.doi.org/10.1038/nature06013.
8. Wu J, Chen ZJ. 2014. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 32:461-488. http://dx.doi.org/10.1146/annurev-immunol-032713-120156.
9. Abe T, Barber GN. 2014. Cytosolic-DNA-mediated, STING-dependent proinflammatory gene induction necessitates canonical NF-kappaB activation through TBK1. J Virol 88:5328-5341. http://dx.doi.org/10.1128/JVI.00037-14.
10. Dempsey A, Bowie AG. 2015. Innate immune recognition of DNA: a recent history. Virology 479-480:146-152. http://dx.doi.org/10.1016/j.virol.2015.03.013.
11. Ma Z, Jacobs SR, West JA, Stopford C, Zhang Z, Davis Z, Barber GN, Glaunsinger BA, Dittmer DP, Damania B. 2015. Modulation of the cGAS-STING DNA sensing pathway by gammaherpesviruses. Proc Natl Acad Sci U S A 112:E4306-E4315. http://dx.doi.org/10.1073/pnas.1503831112.
12. Diner EJ, Vance RE. 2014. Taking the STING out of cytosolic DNA sensing. Trends Immunol 35:1-2. http://dx.doi.org/10.1016/j.it.2013.10.011.
13. Bhat N, Fitzgerald KA. 2014. Recognition of cytosolic DNA by cGAS and other STING-dependent sensors. Eur J Immunol 44:634-640. http://dx.doi.org/10.1002/eji.201344127.
14. Wu J, Sun L, Chen X, Du F, Shi H, Chen C, Chen ZJ. 2013. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339:826-830. http://dx.doi.org/10.1126/science.1229963.
15. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47.
16. Sarkar SN, Sen GC. 2004. Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol Ther 103:245-259. http://dx.doi.org/10.1016/j.pharmthera.2004.07.007.
17. Leib DA. 2002. Counteraction of interferon-induced antiviral responses by herpes simplex viruses. Curr Top Microbiol Immunol 269:171-185.
18. Mossman KL, Ashkar AA. 2005. Herpesviruses and the innate immune response. Viral Immunol 18:267-281. http://dx.doi.org/10.1089/vim.2005.18.267.
19. Paladino P, Mossman KL. 2009. Mechanisms employed by herpes simplex virus 1 to inhibit the interferon response. J Interferon Cytokine Res 29:599-607. http://dx.doi.org/10.1089/jir.2009.0074.
20. Mossman KL, Macgregor PF, Rozmus JJ, Goryachev AB, Edwards AM, Smiley JR. 2001. Herpes simplex virus triggers and then disarms a host antiviral response. J Virol 75:750-758. http://dx.doi.org/10.1128/JVI.75.2.750-758.2001.
21. Nicholl MJ, Robinson LH, Preston CM. 2000. Activation of cellular interferon-responsive genes after infection of human cells with herpes simplex virus type 1. J Gen Virol 81:2215-2218. http://dx.doi.org/10.1099/0022-1317-81-9-2215.
22. Lin R, Noyce RS, Collins SE, Everett RD, Mossman KL. 2004. The herpes simplex virus ICP0 RING finger domain inhibits IRF3-and IRF7-mediated activation of interferon-stimulated genes. J Virol 78:1675-1684. http://dx.doi.org/10.1128/JVI.78.4.1675-1684.2004.
23. 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. http://dx.doi.org/10.1128/JVI.78.16.8411-8420.2004.
24. Mossman K. 2005. Analysis of anti-interferon properties of the herpes simplex virus type I ICP0 protein. Methods Mol Med 116:195-205.
25. Paz S, Vilasco M, Arguello M, Sun Q, Lacoste J, Nguyen TL, Zhao T, Shestakova EA, Zaari S, Bibeau-Poirier A, Servant MJ, Lin R, Meurs EF, Hiscott J. 2009. Ubiquitin-regulated recruitment of IkappaB kinase epsilon to the MAVS interferon signaling adapter. Mol Cell Biol 29:3401-3412. http://dx.doi.org/10.1128/MCB.00880-08.
26. Zhang J, Wang K, Wang S, Zheng C. 2013. Herpes simplex virus 1 E3 ubiquitin ligase ICP0 protein inhibits tumor necrosis factor alphainduced NF-kappaB activation by interacting with p65/RelA and p50/NF-kappaB1. J Virol 87:12935-12948. http://dx.doi.org/10.1128/JVI.01952-13.
27. 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. http://dx.doi.org/10.1016/j.virol.2008.01.001.
28. Liang L, Roizman B. 2008. Expression of gamma interferon-dependent genes is blocked independently by virion host shutoff RNase and by US3 protein kinase. J Virol 82:4688-4696. http://dx.doi.org/10.1128/JVI.02763-07.
29. Wang K, Ni L, Wang S, Zheng C. 2014. Herpes simplex virus 1 protein kinase US3 hyperphosphorylates p65/RelA and dampens NF-kappaB activation. J Virol 88:7941-7951. http://dx.doi.org/10.1128/JVI.03394-13.
30. 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. http://dx.doi.org/10.1128/JVI.02355-13.
31. 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. http://dx.doi.org/10.1128/JVI.06713-11.
32. Wang S, Wang K, Li J, Zheng C. 2013. Herpes simplex virus 1 ubiquitinspecific protease UL36 inhibits beta interferon production by deubiquitinating TRAF3. J Virol 87:11851-11860. http://dx.doi.org/10.1128/JVI.01211-13.
33. Zhang J, Wang S, Wang K, Zheng C. 2013. Herpes simplex virus 1 DNA polymerase processivity factor UL42 inhibits TNF-alpha-induced NFkappaB activation by interacting with p65/RelA and p50/NF-kappaB1. Med Microbiol Immunol 202:313-325. http://dx.doi.org/10.1007/s00430-013-0295-0.
34. 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. http://dx.doi.org/10.1128/JVI.01440-13.
35. Elgadi MM, Hayes CE, Smiley JR. 1999. The herpes simplex virus vhs protein induces endoribonucleolytic cleavage of target RNAs in cell extracts. J Virol 73:7153-7164.
36. Kwong AD, Frenkel N. 1987. Herpes simplex virus-infected cells contain a function(s) that destabilizes both host and viral mRNAs. Proc Natl Acad Sci U S A 84:1926-1930. http://dx.doi.org/10.1073/pnas.84.7.1926.
37. Smiley JR. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J Virol 78:1063-1068. http://dx.doi.org/10.1128/JVI.78.3.1063-1068.2004.
38. 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. http://dx.doi.org/10.1128/JVI.01380-14.
39. 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. http://dx.doi.org/10.1186/s12985-015-0433-y.
40. Liu F, Roizman B. 1992. Differentiation of multiple domains in the herpes simplex virus 1 protease encoded by the UL26 gene. Proc Natl Acad Sci U S A 89:2076-2080. http://dx.doi.org/10.1073/pnas.89.6.2076.
41. Person S, Laquerre S, Desai P, Hempel J. 1993. Herpes simplex virus type 1 capsid protein, VP21, originates within the UL26 open reading frame. J Gen Virol 74:2269-2273. http://dx.doi.org/10.1099/0022-1317-74-10-2269.
42. 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 UL20.5. J Virol 85:1881-1886. http://dx.doi.org/10.1128/JVI.01730-10.
43. Xing J, Wu F, Pan W, Zheng C. 2010. Molecular anatomy of subcellular localization of HSV-1 tegument protein US11 in living cells. Virus Res 153:71-81. http://dx.doi.org/10.1016/j.virusres.2010.07.009.
44. 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. http://dx.doi.org/10.1016/j.febslet.2004.04.069.
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. http://dx.doi.org/10.1016/j.micinf.2005.06.014.
46. Lin R, Lacoste J, Nakhaei P, Sun Q, Yang L, Paz S, Wilkinson P, Julkunen I, Vitour D, Meurs E, Hiscott J. 2006. Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 80:6072-6083. http://dx.doi.org/10.1128/JVI.02495-05.
47. 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. http://dx.doi.org/10.1093/nar/24.4.596.
48. 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. http://dx.doi.org/10.1016/j.immuni.2008.09.003.
49. 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. http://dx.doi.org/10.1128/JVI.05098-11.
50. Ishikawa H, Barber GN. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674-678. http://dx.doi.org/10.1038/nature07317.
51. Keating SE, Baran M, Bowie AG. 2011. Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol 32:574-581. http://dx.doi.org/10.1016/j.it.2011.08.004.
52. Wu JJ, Li W, Shao Y, Avey D, Fu B, Gillen J, Hand T, Ma S, Liu X, Miley W, Konrad A, Neipel F, Sturzl M, Whitby D, Li H, Zhu F. 2015. Inhibition of cGASDNAsensing by a herpesvirus virion protein. Cell Host Microbe 18:333-344. http://dx.doi.org/10.1016/j.chom.2015.07.015.