Herpes simplex virus 1 ubiquitin-specific protease UL36 inhibits beta interferon production by deubiquitinating TRAF3

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11851-11860

  Wang, Shuai ^a,b   Wang, Kezhen ^a,b   Li, Jie ^a   Zhenga, Chunfu ^a,b  

^a SOOCHOW UNIVERSITY   (China)

^b WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; I KAPPA B KINASE EPSILON; INTERFERON REGULATORY FACTOR 3; MAVS PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN KINASE; PROTEINASE; RETINOIC ACID INDUCIBLE PROTEIN I; TBK1 KINASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UL36 UBIQUITIN SPECIFIC PROTEASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEUBIQUITINATION; DIMERIZATION; DOWN REGULATION; FEMALE; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNE EVASION; INTERFERON PRODUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MODIFICATION; SENDAI VIRUS; VIRUS MUTANT;

ANIMALS; CELL LINE; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-BETA; SENDAI VIRUS; TNF RECEPTOR-ASSOCIATED FACTOR 3; UBIQUITIN; UBIQUITIN-SPECIFIC PROTEASES; VIRAL PROTEINS;

EID: 84886877704     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01211-13     Document Type: Article

References (79)

1. Kadowaki N, Antonenko S, Lau JY, Liu YJ. 2000. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J. Exp. Med. 192:219-226.
2. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
3. Sarkar SN, Sen GC. 2004. Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol. Ther. 103:245-259.
4. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86.
5. Bhoj VG, Chen ZJ. 2009. Ubiquitylation in innate and adaptive immunity. Nature 458:430-437.
6. Jiang X, Chen ZJ. 2012. The role of ubiquitylation in immune defence and pathogen evasion. Nat. Rev. Immunol. 12:35-48.
7. 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.
8. Oshiumi H, Matsumoto M, Hatakeyama S, Seya T. 2009. Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J. Biol. Chem. 284:807-817.
9. Hacker H, Redecke V, Blagoev B, Kratchmarova I, Hsu LC, Wang GG, Kamps MP, Raz E, Wagner H, Hacker G, Mann M, Karin M. 2006. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 439:204-207.
10. Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C, O'Rourke KM, Eby M, Pietras E, Cheng G, Bazan JF, Zhang Z, Arnott D, Dixit VM. 2007. DUBA: a deubiquitinase that regulates type I interferon production. Science 318:1628-1632.
11. Oganesyan G, Saha SK, Guo B, He JQ, Shahangian A, Zarnegar B, Perry A, Cheng G. 2006. Critical role of TRAF3 in the Toll-like receptordependent and -independent antiviral response. Nature 439:208-211.
12. Saha SK, Pietras EM, He JQ, Kang JR, Liu SY, Oganesyan G, Shahangian A, Zarnegar B, Shiba TL, Wang Y, Cheng G. 2006. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J. 25:3257-3263.
13. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122:669-682.
14. Barber GN. 2011. Innate immune DNA sensing pathways: STING, AIMII and the regulation of interferon production and inflammatory responses. Curr. Opin. Immunol. 23:10-20.
15. 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.
16. 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.
17. Wang C, Chen T, Zhang J, Yang M, Li N, Xu X, Cao X. 2009. The E3 ubiquitin ligase Nrdp1 'preferentially' promotes TLR-mediated production of type I interferon. Nat. Immunol. 10:744-752.
18. Arimoto K, Funami K, Saeki Y, Tanaka K, Okawa K, Takeuchi O, Akira S, Murakami Y, Shimotohno K. 2010. Polyubiquitin conjugation to NEMO by triparite motif protein 23 (TRIM23) is critical in antiviral defense. Proc. Natl. Acad. Sci. U. S. A. 107:15856-15861.
19. 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.
20. 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.
21. Mossman K. 2005. Analysis of anti-interferon properties of the herpes simplex virus type I ICP0 protein. Methods Mol. Med. 116:195-205.
22. Paladino P, Collins SE, Mossman KL. 2010. Cellular localization of the herpes simplex virus ICP0 protein dictates its ability to block IRF3-mediated innate immune responses. PLoS One 5:e10428. doi:10.1371/journal.pone.0010428.
23. 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.
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.
25. Mossman KL, Smiley JR. 2002. Herpes simplex virus ICP0 and ICP34.5 counteract distinct interferon-induced barriers to virus replication. J. Virol. 76:1995-1998.
26. Verpooten D, Ma Y, Hou S, Yan Z, He B. 2009. Control of TANKbinding kinase 1-mediated signaling by the gamma(1)34.5 protein of herpes simplex virus 1. J. Biol. Chem. 284:1097-1105.
27. 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.
28. Yao XD, Rosenthal KL. 2011. Herpes simplex virus type 2 virion host shutoffprotein suppresses innate dsRNA antiviral pathways in human vaginal epithelial cells. J. Gen. Virol. 92:1981-1993.
29. Melchjorsen J, Siren J, Julkunen I, Paludan SR, Matikainen S. 2006. Induction of cytokine expression by herpes simplex virus in human monocyte-derived macrophages and dendritic cells is dependent on virus replication and is counteracted by ICP27 targeting NF-kappaB and IRF-3. J. Gen. Virol. 87:1099-1108.
30. 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. doi:10.1186/1743-422X-5-140.
31. Abaitua F, O'Hare P. 2008. Identification of a highly conserved, functional nuclear localization signal within the N-terminal region of herpes simplex virus type 1 VP1-2 tegument protein. J. Virol. 82:5234-5244.
32. Chou J, Roizman B. 1989. Characterization of DNA sequence-common and sequence-specific proteins binding to cis-acting sites for cleavage of the terminal a sequence of the herpes simplex virus 1 genome. J. Virol. 63:1059-1068.
33. 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.
34. Fuchs W, Klupp BG, Granzow H, Mettenleiter TC. 2004. Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J. Virol. 78:11879-11889.
35. Lee JI, Luxton GW, Smith GA. 2006. Identification of an essential domain in the herpesvirus VP1/2 tegument protein: the carboxy terminus directs incorporation into capsid assemblons. J. Virol. 80:12086-12094.
36. 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. 80:201-209.37
37. 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.
38. 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.
39. Shanda SK, Wilson DW. 2008. UL36p is required for efficient transport of membrane-associated herpes simplex virus type 1 along microtubules. J. Virol. 82:7388-7394.
40. Zaichick SV, Bohannon KP, Hughes A, Sollars PJ, Pickard GE, Smith GA. 2013. The herpesvirus VP1/2 protein is an effector of dyneinmediated capsid transport and neuroinvasion. Cell Host Microbe 13:193-203.
41. Zhou ZH, Chen DH, Jakana J, Rixon FJ, Chiu W. 1999. Visualization of tegument-capsid interactions andDNAin intact herpes simplex virus type 1 virions. J. Virol. 73:3210-3218.
42. 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.
43. 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.
44. 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.
45. Bottcher S, Maresch C, Granzow H, Klupp BG, Teifke JP, Mettenleiter TC. 2008. Mutagenesis of the active-site cysteine in the ubiquitin-specific protease contained in large tegument protein pUL36 of pseudorabies virus impairs viral replication in vitro and neuroinvasion in vivo. J. Virol. 82: 6009-6016.
46. Jarosinski K, Kattenhorn L, Kaufer B, Ploegh H, Osterrieder N. 2007. A herpesvirus ubiquitin-specific protease is critical for efficient T cell lymphoma formation. Proc. Natl. Acad. Sci. U. S. A. 104:20025-20030.
47. Wang J, Loveland AN, Kattenhorn LM, Ploegh HL, Gibson W. 2006. High-molecular-weight protein (pUL48) of human cytomegalovirus is a competent deubiquitinating protease: mutant viruses altered in its activesite cysteine or histidine are viable. J. Virol. 80:6003-6012.
48. Schlieker C, Weihofen WA, Frijns E, Kattenhorn LM, Gaudet R, Ploegh HL. 2007. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes. Mol. Cell 25:677-687.
49. Gonzalez CM, Wang L, Damania B. 2009. Kaposi's sarcoma-associated herpesvirus encodes a viral deubiquitinase. J. Virol. 83:10224-10233.
50. Gredmark-Russ S, Isaacson MK, Kattenhorn L, Cheung EJ, Watson N, Ploegh HL. 2009. A gammaherpesvirus ubiquitin-specific protease is involved in the establishment of murine gammaherpesvirus 68 infection. J. Virol. 83:10644-10652.
51. Shackelford J, Pagano JS. 2005. Targeting of host-cell ubiquitin pathways by viruses. Essays Biochem. 41:139-156.
52. Sulea T, Lindner HA, Menard R. 2006. Structural aspects of recently discovered viral deubiquitinating activities. Biol. Chem. 387:853-862.
53. 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-kappaB signaling during productive replication. J. Virol. 87:4060-4070.
54. 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.
55. Xing J, Wang S, Li Y, Guo H, Zhao L, Pan W, Lin F, Zhu H, Wang L, Li M, Zheng C. 2011. Characterization of the subcellular localization of herpes simplex virus type 1 proteins in living cells. Med. Microbiol. Immunol. 200:61-68.
56. Ehrhardt C, Kardinal C, Wurzer WJ, WolffT, 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.
57. 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.
58. Zhao T, Yang L, Sun Q, Arguello M, Ballard DW, Hiscott J, Lin R. 2007.The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat. Immunol. 8:592-600.
59. 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.
60. 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.
61. Kochs G, Garcia-Sastre A, Martinez-Sobrido L. 2007. Multiple antiinterferon actions of the influenza A virus NS1 protein. J. Virol. 81:7011-7021.
62. 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.
63. Wang S, Liu N, Chen AJ, Zhao XF, Wang JX. 2009. TRBP homolog interacts with eukaryotic initiation factor 6 (eIF6) in Fenneropenaeus chinensis. J. Immunol. 182:5250-5258.
64. 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.
65. 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.
66. Iwamura T, Yoneyama M, Yamaguchi K, Suhara W, Mori W, Shiota K, Okabe Y, Namiki H, Fujita T. 2001. Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection: common and unique pathways. Genes Cells 6:375-388.
67. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step Red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40:191-197.
68. Li Y, Wang S, Zhu H, Zheng C. 2011. Cloning of the herpes simplex virus type 1 genome as a novel luciferase-tagged infectious bacterial artificial chromosome. Arch. Virol. 156:2267-2272.
69. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor Nature 413:732-738.70.
70. Takahasi K, Yoneyama M, Nishihori T, Hirai R, Kumeta H, Narita R, Gale M, Jr, Inagaki F, Fujita T. 2008. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 29:428-440.
71. 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 sarcoma-associated herpesvirus-encoded deubiquitinase ORF64. J. Virol. 85: 10899-10904.
72. Wang G, Chen G, Zheng D, Cheng G, Tang H. 2011. PLP2 of mouse hepatitis virus A59 (MHV-A59) targets TBK1 to negatively regulate the cellular type I interferon signaling pathway. PLoS One 6:e17192. doi:10.1371/journal.pone.0017192.
73. Wang D, Fang L, Li P, Sun L, Fan J, Zhang Q, Luo R, Liu X, Li K, Chen H, Chen Z, Xiao S. 2011. The leader proteinase of foot-and-mouth disease virus negatively regulates the type I interferon pathway by acting as a viral deubiquitinase. J. Virol. 85:3758-3766.
74. Jiang J, Tang H. 2010. Mechanism of inhibiting type I interferon induction by hepatitis B virus X protein. Protein Cell 1:1106-1117.
75. Sun Z, Chen Z, Lawson SR, Fang Y. 2010. The cysteine protease domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions. J. Virol. 84:7832-7846.
76. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79:15189-15198.
77. Lindner HA, Fotouhi-Ardakani N, Lytvyn V, Lachance P, Sulea T, Menard R. 2005. The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J. Virol. 79: 15199-15208.
78. van Kasteren PB, Bailey-Elkin BA, James TW, Ninaber DK, Beugeling C, Khajehpour M, Snijder EJ, Mark BL, Kikkert M. 2013. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc. Natl. Acad. Sci. U. S. A. 110:E838-E847.
79. Lee JI, Sollars PJ, Baver SB, Pickard GE, Leelawong M, Smith GA. 2009. A herpesvirus encoded deubiquitinase is a novel neuroinvasive determinant. PLoS Pathog. 5:e1000387. doi:10.1371/journal.ppat.1000387.