Herpes simplex virus 1 tegument protein US11 downmodulates the RLR signaling pathway via direct interaction with RIG-I and MDA-5

Journal of Virology

Volumn 86, Issue 7, 2012, Pages 3528-3540

  Xing, Junji ^a   Wang, Shuai ^a   Lin, Rongtuan ^b   Mossman, Karen L ^c   Zheng, Chunfu ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b MCGILL UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; CYTOKINE; DOUBLE STRANDED RNA; INTERFERON REGULATORY FACTOR 3; MEMBRANE RECEPTOR; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; PROTEIN MDA 5; PROTEIN US11; RETINOIC ACID INDUCIBLE PROTEIN I; RIG 1 LIKE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CYTOKINE PRODUCTION; DOWN REGULATION; GENETIC TRANSFECTION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MIXED INFECTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; SENDAI VIRUS; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS MUTANT; WILD TYPE;

CELL LINE; DEAD-BOX RNA HELICASES; DOWN-REGULATION; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; INTERFERON-BETA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; VIRAL PROTEINS;

DNA VIRUSES; HUMAN HERPESVIRUS 1; SENDAI VIRUS;

EID: 84861320795     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06713-11     Document Type: Article

References (96)

1. 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.
2. Andrejeva J, et al. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFNbeta promoter. Proc. Natl. Acad. Sci. U. S. A. 101:17264 -17269.
3. Barral PM, et al. 2007. MDA-5 is cleaved in poliovirus-infected cells. J. Virol. 81:3677-3684.
4. Barral PM, Sarkar D, Fisher PB, Racaniello VR. 2009. RIG-I is cleaved during picornavirus infection. Virology 391:171-176.
5. Basler CF, et al. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
6. Bryant KF, et al. 2005. Binding of herpes simplex virus-1 US11 to specific RNA sequences. Nucleic Acids Res. 33:6090-6100.
7. Burckstummer T, et al. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10:266 -272.
8. Cassady KA. 2005. Human cytomegalovirus TRS1 and IRS1 gene products block the double-stranded-RNA-activated host protein shutoff response induced by herpes simplex virus type 1 infection. J. Virol. 79:8707- 8715.
9. Cassady KA, Gross M. 2002. The herpes simplex virus type 1 U(S)11 protein interacts with protein kinase R in infected cells and requires a 30-amino-acid sequence adjacent to a kinase substrate domain. J. Virol. 76:2029 -2035.
10. Catez F, et al. 2002. Unique motif for nucleolar retention and nuclear export regulated by phosphorylation. Mol. Cell. Biol. 22:1126 -1139.
11. 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.
12. Cheng G, Zhong J, Chung J, Chisari FV. 2007. Double-stranded DNA and double-stranded RNA induce a common antiviral signaling pathway in human cells. Proc. Natl. Acad. Sci. U. S. A. 104:9035-9040.
13. Child SJ, Hakki M, De Niro KL, Geballe AP. 2004. Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J. Virol. 78:197-205.
14. Child SJ, Hanson LK, Brown CE, Janzen DM, Geballe AP. 2006. Double-stranded RNA binding by a heterodimeric complex of murine cytomegalovirus m142 and m143 proteins. J. Virol. 80:10173-10180.
15. Childs KS, Andrejeva J, Randall RE, Goodbourn S. 2009. Mechanism of mda-5 inhibition by paramyxovirus V proteins. J. Virol. 83:1465-1473.
16. Chiu YH, Macmillan JB, Chen ZJ. 2009. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138:576 -591.
17. Choi MK, et al. 2009. A selective contribution of the RIG-I-like receptor pathway to type I interferon responses activated by cytosolic DNA. Proc. Natl. Acad. Sci. U. S. A. 106:17870 -17875.
18. Devaraj SG, et al. 2007. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J. Biol. Chem. 282:32208 -32221.
19. Diaz JJ, et al. 1996. Post-transcriptional transactivation of human retroviral envelope glycoprotein expression by herpes simplex virus Us11 protein. Nature 379:273-277.
20. Donelan NR, Basler CF, Garcia-Sastre A. 2003. A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J. Virol. 77:13257- 13266.
21. Ehrhardt C, et al. 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.
22. 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.
23. Fan L, Briese T, Lipkin WI. 2010. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J. Virol. 84: 1785-1791.
24. Fitzgerald KA, et al. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491- 496.
25. Haasnoot J, et al. 2007. The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog. 3:e86.
26. He B, et al. 1997. Suppression of the phenotype of gamma(1)34.5-herpes simplex virus 1: failure of activated RNA-dependent protein kinase to shut off protein synthesis is associated with a deletion in the domain of the alpha47 gene. J. Virol. 71:6049-6054.
27. Hornung V, et al. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514 -518.
28. Hornung V, et al. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314:994 -997.
29. Iwamura T, et al. 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.
30. 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.
31. Johnson PA, MacLean C, Marsden HS, Dalziel RG, Everett RD. 1986. The product of gene US11 of herpes simplex virus type 1 is expressed as a true late gene. J. Gen. Virol. 67(Pt 5):871- 883.
32. 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.
33. Kawai T, Akira S. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7:131-137.
34. Kawai T, et al. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981-988.
35. Khoo D, Perez C, Mohr I. 2002. Characterization of RNA determinants recognized by the arginine- and proline-rich region of Us11, a herpes simplex virus type 1-encoded double-stranded RNA binding protein that prevents PKR activation. J. Virol. 76:11971-11981.
36. Kim T, et al. 2010. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 107:15181-15186.
37. Kochs G, Garcia-Sastre A, Martinez-Sobrido L. 2007. Multiple antiinterferon actions of the influenza A virus NS1 protein. J. Virol. 81:7011- 7021.
38. Kok KG, et al. 2011. The double-stranded RNA-binding protein PACT functions as a cellular activator of RIG-I to facilitate innate antiviral response. Cell Host Microbe 9:299 -309.
39. 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.
40. Lei X, et al. 2010. The 3C protein of enterovirus 71 inhibits retinoid acid-inducible gene I-mediated interferon regulatory factor 3 activation and type I interferon responses. J. Virol. 84:8051- 8061.
41. Leib DA. 2002. Counteraction of interferon-induced antiviral responses by herpes simplex viruses. Curr. Top. Microbiol. Immunol. 269:171-185.
42. Li K, et al. 2005. Immune evasion by hepatitis C virus NS3/4A proteasemediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. U.S.A. 102:2992-2997.
43. Li M, Wang L, Ren X, Zheng C. 2011. Host cell targets of tegument protein VP22 of herpes simplex virus 1. Arch. Virol. 156:1079 -1084.
44. 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.
45. 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.
46. Lin F, Ren X, Guo H, Ding Q, Zheng AC. 2010. Expression, purification of the UL3 protein of herpes simplex virus type 1, and production of UL3 polyclonal antibody. J. Virol. Methods 166:72-76.
47. Lin R, et al. 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.
48. 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.
49. Ling Z, Tran KC, Teng MN. 2009. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J. Virol. 83:3734 -3742.
50. Melchjorsen J, et al. 2010. Early innate recognition of herpes simplex virus in human primary macrophages is mediated via the MDA5/MAVSdependent and MDA5/MAVS/RNA polymerase III-independent pathways. J. Virol. 84:11350 -11358.
51. 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.
52. Mibayashi M, et al. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 81:514 -524.
53. Mossman K. 2005. Analysis of anti-interferon properties of the herpes simplex virus type I ICP0 protein. Methods Mol. Med. 116:195-205.
54. Mossman KL, Ashkar AA. 2005. Herpesviruses and the innate immune response. Viral Immunol. 18:267-281.
55. Mossman KL, et al. 2001. Herpes simplex virus triggers and then disarms a host antiviral response. J. Virol. 75:750 -758.
56. 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.
57. 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.
58. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. 2003. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 4:161-167.
59. 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.
60. 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.
61. Paladino P, Mossman KL. 2009. Mechanisms employed by herpes simplex virus 1 to inhibit the interferon response. J. Interferon Cytokine Res. 29:599-607.
62. Pan W, Ren X, Guo H, Ding Q, Zheng AC. 2010. Expression, purification of herpes simplex virus type 1 UL4 protein, and production and characterization of UL4 polyclonal antibody. J. Virol. Methods 163:465- 469.
63. Papon L, et al. 2009. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology 393:311- 318.
64. Paz S, et al. 2009. Ubiquitin-regulated recruitment of IkappaB kinase epsilon to the MAVS interferon signaling adapter. Mol. Cell. Biol. 29: 3401-3412.
65. Pichlmair A, Reis e Sousa C. 2007. Innate recognition of viruses. Immunity 27:370 -383.
66. Pichlmair A, et al. 2006. RIG-I-mediated antiviral responses to singlestranded RNA bearing 5=-phosphates. Science 314:997-1001.
67. Poppers J, Mulvey M, Khoo D, Mohr I. 2000. Inhibition of PKR activation by the proline-rich RNA binding domain of the herpes simplex virus type 1 Us11 protein. J. Virol. 74:11215-11221.
68. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1- 47.
69. Rasmussen SB, et al. 2009. Herpes simplex virus infection is sensed by both Toll-like receptors and retinoic acid-inducible gene-like receptors, which synergize to induce type I interferon production. J. Gen. Virol. 90:74 -78.
70. Roller RJ, Monk LL, Stuart D, Roizman B. 1996. Structure and function in the herpes simplex virus 1 RNA-binding protein U(s)11: mapping of the domain required for ribosomal and nucleolar association and RNA binding in vitro. J. Virol. 70:2842-2851.
71. Roller RJ, Roizman B. 1992. The herpes simplex virus 1 RNA binding protein US11 is a virion component and associates with ribosomal 60S subunits. J. Virol. 66:3624 -3632.
72. Roller RJ, Roizman B. 1990. The herpes simplex virus Us11 open reading frame encodes a sequence-specific RNA-binding protein. J. Virol. 64: 3463-3470.
73. Sanchez R, Mohr I. 2007. Inhibition of cellular 2′-5′ oligoadenylate synthetase by the herpes simplex virus type 1 Us11 protein. J. Virol. 81: 3455-3464.
74. Sarkar SN, Sen GC. 2004. Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol. Ther. 103:245-259.
75. 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.
76. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300:1148 -1151.
77. Smiley JR. 2004. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? J. Virol. 78:1063-1068.
78. Smith EJ, Marie I, Prakash A, Garcia-Sastre A, Levy DE. 2001. IRF3 and IRF7 phosphorylation in virus-infected cells does not require doublestranded RNA-dependent protein kinase R or Ikappa B kinase but is blocked by Vaccinia virus E3L protein. J. Biol. Chem. 276:8951- 8957.
79. Strelow LI, Leib DA. 1995. Role of the virion host shutoff (vhs) of herpes simplex virus type 1 in latency and pathogenesis. J. Virol. 69:6779-6786.
80. Takahasi K, et al. 2008. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 29:428-440.
81. Takaoka A, et al. 2007. DAI (DLM-1/ZBP1) is a cytosolicDNAsensor and an activator of innate immune response. Nature 448:501-505.
82. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75- 86.
83. Talon J, et al. 2000. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:7989 -7996.
84. Unterholzner L, et al. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11:997-1004.
85. Vandevenne P, Sadzot-Delvaux C, Piette J. 2010. Innate immune response and viral interference strategies developed by human herpesviruses. Biochem. Pharmacol. 80:1955-1972.
86. 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.
87. Xiang Y, et al. 2002. Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J. Virol. 76:5251-5259.
88. Xing J, et al. 2011. Comprehensive characterization of interaction complexes of herpes simplex virus type 1 ICP22, UL3, UL4, and UL20.5. J. Virol. 85:1881-1886.
89. 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.
90. Xu LG, et al. 2005. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19:727-740.
91. Yang P, et al. 2010. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat. Immunol. 11:487- 494.
92. Yoneyama M, Fujita T. 2007. Function of RIG-I-like receptors in antiviral innate immunity. J. Biol. Chem. 282:15315-15318.
93. Yoneyama M, et al. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730 -737.
94. Zhao T, et al. 2007. The NEMO adaptor bridges the nuclear factorkappaB and interferon regulatory factor signaling pathways. Nat. Immunol. 8:592- 600.
95. Zhong B, et al. 2008. The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation. Immunity 29:538 -550.
96. Zhu H, et al. 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.