Herpes simplex virus 1 ubiquitin-specific protease UL36 abrogates NF-κB activation in DNA sensing signal pathway

Journal of Virology

Volumn 91, Issue 5, 2017, Pages

  Ye, Ruijie ^a   Su, Chenhe ^a   Xu, Haiyan ^a   Zheng, Chunfu ^a,b  

^a SOOCHOW UNIVERSITY   (China)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

DNA sensor; HSV 1; I B ; NF B; UL36

Indexed keywords

BETA INTERFERON; CYCLIC GMP DEPENDENT PROTEIN KINASE; DEUBIQUITINASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN STING; SYNAPTOTAGMIN I; TANK BINDING KINASE 1; UBIQUITIN SPECIFIC PROTEASE UL36; UNCLASSIFIED DRUG; VIRAL PROTEIN; UL36 PROTEIN, HUMAN HERPESVIRUS 1;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVATION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; INNATE IMMUNITY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CHLOROCEBUS AETHIOPS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; UBIQUITINATION; VERO CELL LINE;

ANIMALS; CERCOPITHECUS AETHIOPS; HEK293 CELLS; HERPESVIRUS 1, HUMAN; HUMANS; INTERFERON-BETA; NF-KAPPA B; PROTEOLYSIS; SIGNAL TRANSDUCTION; UBIQUITINATION; VERO CELLS; VIRAL PROTEINS;

EID: 85013984217     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02417-16     Document Type: Article

References (59)

1. 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. https://doi.org/10.1126/science.1232458.
2. Wu JX, Sun LJ, Chen X, Du FH, Shi HP, Chen C, Chen ZJJ. 2013. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339:826-830. https://doi.org/10.1126/science.1229963.
3. Abe T, Barber GN. 2014. Cytosolic-DNA-mediated, STING-dependent proinflammatory gene induction necessitates canonical NF-κB activation through TBK1. J Virol 88:5328-5341. https://doi.org/10.1128/JVI.00037-14.
4. Ishikawa H, Barber GN. 2011. The STING pathway and regulation of innate immune signaling in response to DNA pathogens. Cell Mol Life Sci 68:1157-1165. https://doi.org/10.1007/s00018-010-0605-2.
5. Ikeda F, Crosetto N, Dikic I. 2010. What determines the specificity and outcomes of ubiquitin signaling? Cell 143:677-681. https://doi.org/10.1016/j.cell.2010.10.026.
6. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP. 2003. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21:921-926. https://doi.org/10.1038/nbt849.
7. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J 19:94-102. https://doi.org/10.1093/emboj/19.1.94.
8. Chen ZJ, Sun LJ. 2009. Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 33:275-286. https://doi.org/10.1016/j.molcel.2009.01.014.
9. Dev A, Iyer S, Razani B, Cheng G. 2011. NF-κB and innate immunity. Curr Top Microbiol Immunol 349:115-143.
10. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. 2006. Activation of IKK by TNF-α requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 22:245-257. https://doi.org/10.1016/j.molcel.2006.03.026.
11. Wu CJ, Conze DB, Li T, Srinivasula SM, Ashwell JD. 2006. Sensing of Lys 63-linked polyubiquitination by NEMO is a key event in NF-κB activation (corrected). Nat Cell Biol 8:398-406. https://doi.org/10.1038/ncb1384.
12. Kanayama A, Seth RB, Sun L, Ea CK, Hong M, Shaito A, Chiu YH, Deng L, Chen ZJ. 2004. TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol Cell 15:535-548. https://doi.org/10.1016/j.molcel.2004.08.008.
13. Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, Kato R, Kensche T, Uejima T, Bloor S, Komander D, Randow F, Wakatsuki S, Dikic I. 2009. Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation. Cell 136:1098-1109. https://doi.org/10.1016/j.cell.2009.03.007.
14. Karin M, Ben-Neriah Y. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol 18:621-663. https://doi.org/10.1146/annurev.immunol.18.1.621.
15. Hayden MS, Ghosh S. 2004. Signaling to NF-κB. Genes Dev 18: 2195-2224. https://doi.org/10.1101/gad.1228704.
16. Zhong B, Zhang L, Lei C, Li Y, Mao AP, Yang Y, Wang YY, Zhang XL, Shu HB. 2009. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 30: 397-407. https://doi.org/10.1016/j.immuni.2009.01.008.
17. Qin Y, Zhou MT, Hu MM, Hu YH, Zhang J, Guo L, Zhong B, Shu HB. 2014. RNF26 temporally regulates virus-triggered type I interferon induction by two distinct mechanisms. PLoS Pathog 10:e1004358. https://doi.org/10.1371/journal.ppat.1004358.
18. Tsuchida T, Zou J, Saitoh T, Kumar H, Abe T, Matsuura Y, Kawai T, Akira S. 2010. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33:765-776. https://doi.org/10.1016/j.immuni.2010.10.013.
19. Zhang J, Hu MM, Wang YY, Shu HB. 2012. TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J Biol Chem 287: 28646-28655. https://doi.org/10.1074/jbc. M112.362608.
20. Wang Q, Liu X, Cui Y, Tang Y, Chen W, Li S, Yu H, Pan Y, Wang C. 2014. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41:919-933. https://doi.org/10.1016/j.immuni.2014.11.011.
21. 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(Pt 7):1531-1574. https://doi.org/10.1099/0022-1317-69-7-1531.
22. McGeoch DJ, Cook S. 1994. Molecular phylogeny of the alphaherpesvirinae subfamily and a proposed evolutionary timescale. J Mol Biol 238: 9-22. https://doi.org/10.1006/jmbi.1994.1264.
23. 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.
24. 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. https://doi.org/10.1128/JVI.01211-13.
25. 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.
26. Ma Z, Jacobs SR, West JA, Stopford C, Zhang Z, Davis Z, Barber GN, Glaunsinger BA, Dittmer DP, Damania B. 2015. Modulation of the cGASSTING DNA sensing pathway by gammaherpesviruses. Proc Natl Acad Sci U S A 112:E4306-E4315. https://doi.org/10.1073/pnas.1503831112.
27. 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. https://doi.org/10.1038/ni.1932.
28. Ishikawa H, Barber GN. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signaling. Nature 455:674-678. https://doi.org/10.1038/nature07317.
29. Chen Z, Hagler J, Palombella VJ, Melandri F, Scherer D, Ballard D, Maniatis T. 1995. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev 9:1586-1597. https://doi.org/10.1101/gad.9.13.1586.
30. DiDonato J, Mercurio F, Rosette C, Wu-Li J, Suyang H, Ghosh S, Karin M. 1996. Mapping of the inducible IκB phosphorylation sites that signal its ubiquitination and degradation. Mol Cell Biol 16:1295-1304. https://doi.org/10.1128/MCB.16.4.1295.
31. Santoro MG, Rossi A, Amici C. 2003. NF-κB and virus infection: who controls whom. EMBO J 22:2552-2560. https://doi.org/10.1093/emboj/cdg267.
32. Goodkin ML, Ting AT, Blaho JA. 2003. NF-κB is required for apoptosis prevention during herpes simplex virus type 1 infection. J Virol 77: 7261-7280. https://doi.org/10.1128/JVI.77.13.7261-7280.2003.
33. Amici C, Rossi A, Costanzo A, Ciafre S, Marinari B, Balsamo M, Levrero M, Santoro MG. 2006. Herpes simplex virus disrupts NF-κB regulation by blocking its recruitment on the IκBα promoter and directing the factor on viral genes. J Biol Chem 281:7110-7117. https://doi.org/10.1074/jbc. M512366200.
34. 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.
35. Zhang J, Wang K, Wang S, Zheng C. 2013. Herpes simplex virus 1 E3 ubiquitin ligase ICP0 protein inhibits tumor necrosis factor alphainduced NF-κB activation by interacting with p65/RelA and p50/NF-κB1. J Virol 87:12935-12948. https://doi.org/10.1128/JVI.01952-13.
36. Wang K, Ni L, Wang S, Zheng C. 2014. Herpes simplex virus 1 protein kinase US3 hyperphosphorylates p65/RelA and dampens NF-κB activation. J Virol 88:7941-7951. https://doi.org/10.1128/JVI.03394-13.
37. Kim JC, Lee SY, Kim SY, Kim JK, Kim HJ, Lee HM, Choi MS, Min JS, Kim MJ, Choi HS, Ahn JK. 2008. HSV-1 ICP27 suppresses NF-κB activity by stabilizing IκBα. FEBS Lett 582:2371-2376. https://doi.org/10.1016/j.febslet.2008.05.044.
38. Zhang J, Wang S, Wang K, Zheng C. 2013. Herpes simplex virus 1 DNA polymerase processivity factor UL42 inhibits TNF-α-induced NF-κB activation by interacting with p65/RelA and p50/NF-κB1. Med Microbiol Immunol 202:313-325. https://doi.org/10.1007/s00430-013-0295-0.
39. 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-κB 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.
40. Zenner HL, Mauricio R, Banting G, Crump CM. 2013. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoffactivity. J Virol 87:13115-13123. https://doi.org/10.1128/JVI.02167-13.
41. Shen G, Wang K, Wang S, Cai M, Li ML, Zheng C. 2014. Herpes simplex virus 1 counteracts viperin via its virion host shutoffprotein UL41. J Virol 88:12163-12166. https://doi.org/10.1128/JVI.01380-14.
42. 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.
43. 134.5 protein of herpes simplex virus 1. J Biol Chem 284:1097-1105. https://doi.org/10.1074/jbc. M805905200.
44. 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.
45. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341:1390-1394. https://doi.org/10.1126/science.1244040.
46. 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 cGAS DNA sensing by a herpesvirus virion protein. Cell Host Microbe 18:333-344. https://doi.org/10.1016/j.chom.2015.07.015.
47. Zhang D, Su C, Zheng C. 2016. Herpes simplex virus 1 serine protease VP24 blocks the DNA-sensing signal pathway by abrogating activation of interferon regulatory factor 3. J Virol 90:5824-5829. https://doi.org/10.1128/JVI.00186-16.
48. Schlieker C, Korbel GA, Kattenhorn LM, Ploegh HL. 2005. A deubiquitinating activity is conserved in the large tegument protein of the herpesviridae. J Virol 79:15582-15585. https://doi.org/10.1128/JVI.79.24.15582-15585.2005.
49. Kim YE, Oh SE, Kwon KM, Lee CH, Ahn JH. 2016. Involvement of the N-terminal DUB domain of human cytomegalovirus UL48 tegument protein in auto-ubiquitination, virion stability, virus entry. J Virol 90: 3229-3242. https://doi.org/10.1128/JVI.02766-15.
50. Saito S, Murata T, Kanda T, Isomura H, Narita Y, Sugimoto A, Kawashima D, Tsurumi T. 2013. Epstein-Barr virus deubiquitinase downregulates TRAF6-mediated NF-κB signaling during productive replication. J Virol 87:4060-4070. https://doi.org/10.1128/JVI.02020-12.
51. Inn KS, Lee SH, Rathbun JY, Wong LY, Toth Z, Machida K, Ou JH, Jung JU. 2011. Inhibition of RIG-I-mediated signaling by Kaposi's sarcomaassociated herpesvirus-encoded deubiquitinase ORF64. J Virol 85: 10899-10904. https://doi.org/10.1128/JVI.00690-11.
52. 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. https://doi.org/10.1128/JVI.01730-10.
53. 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 IκB kinase epsilon to the MAVS interferon signaling adapter. Mol Cell Biol 29:3401-3412. https://doi.org/10.1128/MCB.00880-08.
54. Park KA, Byun HS, Won M, Yang KJ, Shin S, Piao L, Kim JM, Yoon WH, Junn E, Park J, Seok JH, Hur GM. 2007. Sustained activation of protein kinase C downregulates nuclear factor-κB signaling by dissociation of IKK-γ and Hsp90 complex in human colonic epithelial cells. Carcinogenesis 28:71-80. https://doi.org/10.1093/carcin/bgl094.
55. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J, Young DB, Barbosa M, Mann M, Manning A, Rao A. 1997. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science 278:860-866. https://doi.org/10.1126/science.278.5339.860.
56. Severa M, Coccia EM, Fitzgerald KA. 2006. Toll-like receptor-dependent and-independent viperin gene expression and counter-regulation by PRDI-binding factor-1/BLIMP1. J Biol Chem 281:26188-26195. https://doi.org/10.1074/jbc. M604516200.
57. 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-IKKε molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 80:6072-6083. https://doi.org/10.1128/JVI.02495-05.
58. 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.
59. 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.