Herpes simplex virus US3 tegument protein inhibits Toll-like receptor 2 signaling at or before TRAF6 ubiquitination

Virology

Volumn 439, Issue 2, 2013, Pages 65-73

  Sen, Jayita ^a   Liu, Xueqiao ^a,c   Roller, Richard ^b   Knipe, David M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

HSV; NF kB; Tegument protein; TRAF6; US3

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MYELOID DIFFERENTIATION FACTOR 88; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; US3 PROTEIN; VIRUS PROTEIN; ZYMOSAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; INHIBITION KINETICS; MOLECULAR LIBRARY; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION; VIRUS MUTANT;

CELL LINE; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNE EVASION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOLL-LIKE RECEPTOR 2; UBIQUITINATION; VIRAL PROTEINS; VIRULENCE FACTORS;

SIMPLEXVIRUS;

EID: 84875808016     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.01.026     Document Type: Article

References (57)

1. Amici C., Belardo G., Rossi A., Santoro M.G. Activation of IkB kinase by herpes simplex virus type 1. A novel target for anti-herpetic therapy. J. Biol. Chem. 2001, 276:28759-28766.
2. Aravalli R.N., Hu S., Lokensgard J.R. Toll-like receptor 2 signaling is a mediator of apoptosis in herpes simplex virus-infected microglia. J. Neuroinflamm. 2007, 4:11.
3. Aravalli R.N., Hu S., Rowen T.N., Palmquist J.M., Lokensgard J.R. Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J. Immunol. 2005, 175(7):4189-4193.
4. Barbalat R., Lau L., Locksley R.M., Barton G.M. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 2009, 10:1200-1207.
5. Benetti L., Roizman B. Herpes simplex virus protein kinase US3 activates and functionally overlaps protein kinase A to block apoptosis. Proc. Nat. Acad. Sci. U.S.A. 2004, 101(25):9411-9416.
6. Benetti L., Roizman B. In transduced cells, the US3 protein kinase of herpes simplex virus 1 precludes activation and induction of apoptosis by transfected procaspase 3. J. Virol. 2007, 81:10242-10248.
7. Bochud P.Y., Magaret A.S., Koelle D.M., Aderem A., Wald A. Polymorphisms in TLR2 are associated with increased viral shedding and lesional rate in patients with genital herpes simplex virus Type 2 infection. J. Infect. Dis. 2007, 196:505-509.
8. Chen Z.J. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 2005, 7:758-765.
9. Cheng X.J., Fisone G., Aizman O., Aizman R., Levenson R., Greengard P., Aperia A. PKA-mediated phosphorylation and inhibition of Na(+)-K(+)-ATPase in response to beta-adrenergic hormone. Am. J. Physiol. 1997, 273:C893-C901.
10. Cholay M., Reverdy C., Benarous R., Colland F., Daviet L. Functional interaction between the ubiquitin-specific protease 25 and the SYK tyrosine kinase. Exp. Cell. Res. 2010, 316:667-675.
11. Chuluunbaatar U., Roller R., Feldman M.E., Brown S., Shokat K.M., Mohr I. Constitutive mTORC1 activation by a herpesvirus Akt surrogate stimulates mRNA translation and viral replication. Genes Dev. 2010, 24:2627-2639.
12. Favoreel H.W., Van Minnebruggen G., Adriaensen D., Nauwynck H.J. Cytoskeletal rearrangements and cell extensions induced by the US3 kinase of an alphaherpesvirus are associated with enhanced spread. Proc. Nat. Acad. Sci. U.S.A. 2005, 102:8990-8995.
13. Fitzgerald K.A., Palsson-McDermott E.M., Bowie A.G., Jefferies C.A., Mansell A.S., Brady G., Brint E., Dunne A., Gray P., Harte M.T., McMurray D., Smith D.E., Sims J.E., Bird T.A., O'Neill L.A. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 2001, 413:78-83.
14. Frame M.C., Purves F.C., McGeoch D.J., Marsden H.S., Leader D.P. Identification of the herpes simplex virus protein kinase as the product of viral gene US3. J. Gen. Virol. 1987, 68(10):2699-2704.
15. Gack M.U., Nistal-Villán E., Inn K.S., García-Sastre A., Jung J.U. Phosphorylation-mediated negative regulation of RIG-I antiviral activity. J. Virol. 2010, 84:3220-3229.
16. Gerlo S., Kooijman R., Beck I.M., Kolmus K., Spooren A., Haegeman G. Cyclic AMP: a selective modulator of NF-κB action. Cell. Mol. Life Sci. 2011, 68:3823-3841.
17. Gu H., Liang Y., Mandel G., Roizman B. Components of the REST/CoREST/histone deacetylase repressor complex are disrupted, modified, and translocated in HSV-1-infected cells. Proc. Nat. Acad. Sci. U.S.A. 2005, 102:7571-7576.
18. Hargett D., Rice S., Bachenheimer S.L. Herpes simplex virus type 1 ICP27-dependent activation of NF{kappa}B. J. Virol. 2006, 80:10565-10578.
19. Hata S., Koyama A.H., Shiota H., Adachi A., Goshima F., Nishiyama Y. Antiapoptotic activity of herpes simplex virus type 2: the role of US3 protein kinase gene 1999, 1:601-607.
20. Hayden M.S., West A.P., Ghosh S. NF-kappaB and the immune response. Oncogene 2006, 25:6758-6780.
21. Hilton M.J., Mounghane D., McLean T., Contractor N.V., O'Neil J., Carpenter K., Bachenheimer S.L. Induction by herpes simplex virus of free and heteromeric forms of E2F transcription factor. Virology 1995, 213:624-638.
22. Keepers T.R., Gross L.K., Obrig T.G. Monocyte chemoattractant protein 1, macrophage inflammatory protein 1 alpha, and RANTES recruit macrophages to the kidney in a mouse model of hemolytic-uremic syndrome. Infect. Immun. 2007, 75:1229-1236.
23. Koga T., Lim J.H., Jono H., Ha U.H., Xu H., Ishinaga H., Morino S., Xu X., Yan C., Kai H., Li J.D. Tumor suppressor cylindromatosis acts as a negative regulator for Streptococcus pneumoniae-induced NFAT signaling. J. Biol. Chem. 2008, 283:12546-12554.
24. Kurt-Jones E.A., Belko J., Yu C., Newburger P.E., Wang J., Chan M., Knipe D.M., Finberg R.W. The role of toll-like receptors in herpes simplex infection in neonates. J. Infect. Dis. 2005, 191:746-748.
25. Kurt-Jones E.A., Chan M., Zhou S., Wang J., Reed G., Bronson R., Arnold M.M., Knipe D.M., Finberg R.W. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc. Nat. Acad. Sci. U.S.A. 2004, 101:1315-1320.
26. Kurt-Jones E.A., Mandell L., Whitney C., Padgett A., Gosselin K., Newburger P.E., Finberg R.W. Role of toll-like receptor 2 (TLR2) in neutrophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils. Blood 2002, 100:1860-1868.
27. Leoni V., Gianni T., Salvioli S., Campadelli-Fiume G. Herpes simplex virus glycoproteins gH/gL and gB bind Toll-like receptor 2, and soluble gH/gL is sufficient to activate NF-kappaB. J. Virol. 2012, 86:6555-6562.
28. Leopardi R., Van Sant C., Roizman B. The herpes simplex virus 1 protein kinase US3 is required for protection from apoptosis induced by the virus. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:7891-7896.
29. Liang L., Roizman B. Expression of gamma interferon-dependent genes is blocked independently by virion host shutoff RNase and by US3 protein kinase. J. Virol. 2008, 82:4688-4696.
30. Lima G.K., Zolini G.P., Mansur D.S., Freire Lima B.H., Wischhoff U., Astigarraga R.G., Dias M.F., das Gracas Almeida Silva M., Bela S.R., do Valle Antonelli L.R., Arantes R.M., Gazzinelli R.T., Bafica A., Kroon E.G., Campos M.A. Toll-like receptor (TLR) 2 and TLR9 expressed in trigeminal ganglia are critical to viral control during herpes simplex virus 1 infection. Am. J. Pathol. 2010, 177(5):2433-2445.
31. Liu X., Fitzgerald K., Kurt-Jones E., Finberg R., Knipe D.M. Herpesvirus tegument protein activates NF-kappaB signaling through the TRAF6 adaptor protein. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:11335-11339.
32. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
33. Matsuzaki A., Yamauchi Y., Kato A., Goshima F., Kawaguchi Y., Yoshikawa T., Nishiyama Y. US3 protein kinase of herpes simplex virus type 2 is required for the stability of the UL46-encoded tegument protein and its association with virus particles. J. Gen. Virol. 2005, 86:1979-1985.
34. McGeoch D.J., Davison A.J. Alphaherpesviruses possess a gene homologous to the protein kinase gene family of eukaryotes and retroviruses. Nucleic Acids Res. 1986, 14(4):1765-1777.
35. Medici M.A., Sciortino M.T., Perri D., Amici C., Avitabile E., Ciotti M., Balestrieri E., De Smaele E., Franzoso G., Mastino A. Protection by herpes simplex virus glycoprotein d against Fas-mediated apoptosis: role of nuclear factor kappaB. J. Biol. Chem. 2003, 278:36059-36067.
36. S3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J. Virol. 2007, 81:6459-6470.
37. Munger J., Roizman B. The US3 protein kinase of herpes simplex virus 1 mediates the posttranslational modification of BAD and prevents BAD-induced programmed cell death in the absence of other viral proteins. Proc. Nat. Acad. Sci. U.S.A. 2001, 98:1410-1415.
38. S3 protein kinase is sufficient to block apoptosis induced by overexpression of a variety of Bcl-2 family members. Virology 2004, 319:212-224.
39. Oliveira-Nascimento L., Massari P., Wetzler L.M. The role of TLR2 in infection and immunity. Front. Immunol. 2012, 3:79.
40. Orzalli M.J.H., DeLuca N.A., Knipe D.M. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection: degradation of IFI16 by nuclear HSV ICP0 protein. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:E3008-E3017.
41. Patel A., Hanson J., McLean R.I., Olgiate J., Hilton M., Miller W.E., Bachenheimer S.L. Herpes simplex virus type 1 induction of persistent NF-kB nuclear translocation increases the efficiency of virus replication. Virology 1998, 247:212-222.
42. S3.5 protein kinases of herpes simplex virus 1 differ with respect to their functions in blocking apoptosis and in virion maturation and egress. J. Virol. 2006, 80:3752-3764.
43. S3 gene mediates posttranslational modification of the phosphoprotein encoded by the UL34 gene. J. Virol. 1991, 65:5757-5764.
44. Rasmussen S.B., Sorensen L.N., Malmgaard L., Ank N., Baines J.D., Chen Z.J., Paludan S.R. Type I interferon production during herpes simplex virus infection is controlled by cell-type-specific viral recognition through Toll-like receptor 9, the mitochondrial antiviral signaling protein pathway, and novel recognition systems. J. Virol. 2007, 81:13315-13324.
45. Rathinam V.A., Fitzgerald K.A. Innate immune sensing of DNA viruses. Virology 2011, 411:153-162.
46. Reynolds A.E., Wills E.G., Roller R.J., Ryckman B.J., Baines J.D. Ultrastructural localization of the herpes simplex virus type 1 u(l)31, u(l)34, and u(s)3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 2002, 76:8939-8952.
47. Roizman B., Knipe D.M., Whitley R.J. Herpes simplex viruses. Fields Virology Fifth edition. 2007, 2501-2602. Lippincott, Williams and Wilkins, Philadelphia.
48. Ryckman B.J., Roller R.J. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J. Virol. 2004, 78:399-412.
49. Santoro M.G., Rossi A., Amici C. NF-kB and virus infection: who controls whom. EMBO J. 2003, 22. 2552-2260.
50. Sarangi P.P., Kim B., Kurt-Jones E., Rouse B.T. Innate recognition network driving herpes simplex virus-induced corneal immunopathology: role of the toll pathway in early inflammatory events in stromal keratitis. J. Virol. 2007, 81:11128-11138.
51. Sato A., Linehan M.M., Iwasaki A. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:17343-17348.
52. Sciortino M.T., Medici M.A., Marino-Merlo F., Zaccaria D., Giuffre-Cuculletto M., Venuti A., Grelli S., Bramanti P., Mastino A. Involvement of gD/HVEM interaction in NF-kB-dependent inhibition of apoptosis by HSV-1 gD. Biochem. Pharmacol. 2008, 76:1522-1532.
53. Shembade N., Ma A., Harhaj E.W. Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010, 327:1135-1139.
54. Sorensen L.N., Reinert L.S., Malmgaard L., Bartholdy C., Thomsen A.R., Paludan S.R. TLR2 and TLR9 synergistically control herpes simplex virus infection in the brain. J. Immunol. 2008, 181:8604-8612.
55. van Lint A.L., Murawski M.R., Goodbody R.E., Severa M., Fitzgerald K.A., Finberg R.W., Knipe D.M., Kurt-Jones E.A. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2-dependent inflammatory responses and NF-kappaB signaling. J. Virol. 2010, 84:10802-10811.
56. Wisner T.W., Wright C.C., Kato A., Kawaguchi Y., Mou F., Baines J.D., Roller R.J., Johnson D.C. Herpesvirus gB-induced fusion between the virion envelope and outer nuclear membrane during virus egress is regulated by the viral US3 kinase. J. Virol. 2009, 83:3115-3126.
57. Zhong B., Liu X., Wang X., Chang S.H., Liu X., Wang A., Reynolds J.M., Dong C. Negative regulation of IL-17-mediated signaling and inflammation by the ubiquitin-specific protease USP25. Nat. Immunol. 2012, 13:1110-1117.