DNA sensing-independent inhibition of Herpes simplex virus 1 replication by DAI/ZBP1

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3076-3086

  Pham, Thanh H ^b   Kwon, Ki Mun ^a   Kim, Young Eui ^a   Kim, Kyeong Kyu ^a   Ahn, Jin Hyun ^a  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DNA; DNA DEPENDENT ACTIVATOR OF INTERFERON REGULATORY FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR 3; LENTIVIRUS VECTOR; RETROVIRUS VECTOR; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; IMMEDIATE EARLY PROTEIN; UBIQUITIN PROTEIN LIGASE; VIRUS DNA; VMW110 PROTEIN, HUMAN HERPESVIRUS 1; ZBP1 PROTEIN, HUMAN;

ARTICLE; CELL STRAIN HEPG2; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA SENSING; GENE EXPRESSION; GENETIC PROCEDURES; GENETIC TRANSFECTION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS INHIBITION; VIRUS REPLICATION; ANIMAL; CELL LINE; FIBROBLAST; IMMUNOLOGY; LIVER CELL; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN BINDING; VIROLOGY;

HUMAN HERPESVIRUS 1;

ANIMALS; CELL LINE; DNA, VIRAL; DNA-BINDING PROTEINS; FIBROBLASTS; HEPATOCYTES; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; MICE; PROTEIN BINDING; UBIQUITIN-PROTEIN LIGASES; VIRUS REPLICATION;

MLCS; MLOWN;

EID: 84876345677     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02860-12     Document Type: Article

References (47)

1. Fu Y, Comella N, Tognazzi K, Brown LF, Dvorak HF, Kocher O. 1999. Cloning of DLM-1, a novel gene that is up-regulated in activated macrophages, using RNA differential display. Gene 240:157-163.
2. Ha SC, Kim D, Hwang HY, Rich A, Kim YG, Kim KK. 2008. The crystal structure of the second Z-DNA binding domain of human DAI (ZBP1) in complex with Z-DNA reveals an unusual binding mode to Z-DNA. Proc. Natl. Acad. Sci. U. S. A. 105:20671-20676.
3. Kim K, Khayrutdinov BI, Lee CK, Cheong HK, Kang SW, Park H, Lee S, Kim YG, Jee J, Rich A, Kim KK, Jeon YH. 2011. Solution structure of the Zβ domain of human DNA-dependent activator of IFN-regulatory factors and its binding modes to B- and Z-DNAs. Proc. Natl. Acad. Sci. U. S. A. 108:6921-6926.
4. Rothenburg S, Schwartz T, Koch-Nolte F, Haag F. 2002. Complex regulation of the human gene for the Z-DNA binding protein DLM-1. Nucleic Acids Res. 30:993-1000.
5. Schwartz T, Behlke J, Lowenhaupt K, Heinemann U, Rich A. 2001. Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat. Struct. Biol. 8:761-765.
6. Rich A, Zhang S. 2003. Timeline: Z-DNA: the long road to biological function. Nat. Rev. Genet. 4:566-572.
7. Rothenburg S, Koch-Nolte F, Rich A, Haag F. 2001. A polymorphic dinucleotide repeat in the rat nucleolin gene forms Z-DNA and inhibits promoter activity. Proc. Natl. Acad. Sci. U. S. A. 98:8985-8990.
8. Wieland SF, Vega RG, Muller R, Evans CF, Hilbush B, Guidotti LG, Sutcliffe JG, Schultz PG, Chisari FV. 2003. Searching for interferoninduced genes that inhibit hepatitis B virus replication in transgenic mouse hepatocytes. J. Virol. 77:1227-1236.
9. Ishii KJ, Coban C, Kato H, Takahashi K, Torii Y, Takeshita F, Ludwig H, Sutter G, Suzuki K, Hemmi H, Sato S, Yamamoto M, Uematsu S, Kawai T, Takeuchi O, Akira S. 2006. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 7:40-48.
10. 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.
11. Wang Z, Choi MK, Ban T, Yanai H, Negishi H, Lu Y, Tamura T, Takaoka A, Nishikura K, Taniguchi T. 2008. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc. Natl. Acad. Sci. U. S. A. 105:5477-5482.
12. Kaiser WJ, Upton JW, Mocarski ES. 2008. Receptor-interacting protein homotypic interaction motif-dependent control of NF-κB activation via the DNA-dependent activator of IFN regulatory factors. J. Immunol. 181: 6427-6434.
13. Rebsamen M, Heinz LX, Meylan E, Michallet MC, Schroder K, Hofmann K, Vazquez J, Benedict CA, Tschopp J. 2009. DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF- B. EMBO Rep. 10:916-922.
14. Upton JW, Kaiser WJ, Mocarski ES. 2012. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11:290-297.
15. Lippmann J, Rothenburg S, Deigendesch N, Eitel J, Meixenberger K, van Laak V, Slevogt H, NGuessan DP, Hippenstiel S, Chakraborty T, Flieger A, Suttorp N, Opitz B. 2008. IFNα responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell Microbiol. 10:2579-2588.
16. Ishii KJ, Kawagoe T, Koyama S, Matsui K, Kumar H, Kawai T, Uematsu S, Takeuchi O, Takeshita F, Coban C, Akira S. 2008. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451:725-729.
17. Furr SR, Chauhan VS, Moerdyk-Schauwecker MJ, Marriott I. 2011. A role for DNA-dependent activator of interferon regulatory factor in the recognition of herpes simplex virus type 1 by glial cells. J. Neuroinflammation 8:99.
18. DeFilippis VR, Alvarado D, Sali T, Rothenburg S, Fruh K. 2010. Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J. Virol. 84:585-598.
19. DeFilippis VR, Sali T, Alvarado D, White L, Bresnahan W, Fruh KJ. 2010. Activation of the interferon response by human cytomegalovirus occurs via cytoplasmic double-stranded DNA but not glycoprotein B. J. Virol. 84:8913-8925.
20. Warner MS, Geraghty RJ, Martinez WM, Montgomery RI, Whitbeck JC, Xu R, Eisenberg RJ, Cohen GH, Spear PG. 1998. A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179-189.
21. Sacks WR, Schaffer PA. 1987. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture. J. Virol. 61:829-839.
22. Yao F, Schaffer PA. 1995. An activity specified by the osteosarcoma line U2OS can substitute functionally for ICP0, a major regulatory protein of herpes simplex virus type 1. J. Virol. 69:6249-6258.
23. Pham HT, Park MY, Kim KK, Kim YG, Ahn JH. 2006. Intracellular localization of human ZBP1: differential regulation by the Z-DNA binding domain, Zβ, in splice variants. Biochem. Biophys. Res. Commun. 348:145-152.
24. Green S, Issemann I, Sheer E. 1988. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 16:369.
25. Yu SS, Kim JM, Kim S. 2000. High efficiency retroviral vectors that contain no viral coding sequences. Gene Ther. 7:797-804.
26. Lee HR, Kim DJ, Lee JM, Choi CY, Ahn BY, Hayward GS, Ahn JH. 2004. Ability of the human cytomegalovirus IE1 protein to modulate sumoylation of PML correlates with its functional activities in transcriptional regulation and infectivity in cultured fibroblast cells. J. Virol. 78: 6527-6542.
27. Tavalai N, Papior P, Rechter S, Leis M, Stamminger T. 2006. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J. Virol. 80:8006-8018.
28. Everett RD, Parada C, Gripon P, Sirma H, Orr A. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82:2661-2672.
29. Lukashchuk V, Everett RD. 2010. Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J. Virol. 84:4026-4040.
30. Kawaguchi Y, Bruni R, Roizman B. 1997. Interaction of herpes simplex virus 1α regulatory protein ICP0 with elongation factor 1: ICP0 affects translational machinery. J. Virol. 71:1019-1024.
31. Lopez P, Van Sant C, Roizman B. 2001. Requirements for the nuclearcytoplasmic translocation of infected-cell protein 0 of herpes simplex virus 1. J. Virol. 75:3832-3840.
32. Maul GG, Everett RD. 1994. The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J. Gen. Virol. 75(Pt 6):1223-1233.
33. 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.
34. Orzalli MH, Deluca NA, Knipe DM. 2012. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. U. S. A. 109:E3008 -E3017.
35. Paludan SR, Bowie AG, Horan KA, Fitzgerald KA. 2011. Recognition of herpesviruses by the innate immune system. Nat. Rev. Immunol. 11:143-154.
36. Rathinam VA, Fitzgerald KA. 2011. Innate immune sensing of DNA viruses. Virology 411:153-162.
37. Cuchet-Lourenco D, Vanni E, Glass M, Orr A, Everett RD. 2012. Herpes simplex virus 1 ubiquitin ligase ICP0 interacts with PML isoform I and induces its SUMO-independent degradation. J. Virol. 86:11209-11222.
38. Upton JW, Kaiser WJ, Mocarski ES. 2010. Virus inhibition of RIP3- dependent necrosis. Cell Host. Microbe 7:302-313.
39. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137:1100-1111.
40. Gariano GR, Dell'Oste V, Bronzini M, Gatti D, Luganini A, Andrea MD, Gribaudo G, Gariglio M, Landolfo S. 2012. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog. 8:e1002498. doi:10.1371/journal.ppat.1002498.
41. Boutell C, Sadis S, Everett RD. 2002. Herpes simplex virus type 1 immediate- early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 76:841-850.
42. Van Sant C, Hagglund R, Lopez P, Roizman B. 2001. The infected cell protein 0 of herpes simplex virus 1 dynamically interacts with proteasomes, binds and activates the cdc34 E2 ubiquitin-conjugating enzyme, and possesses in vitro E3 ubiquitin ligase activity. Proc. Natl. Acad. Sci. U. S. A. 98:8815-8820.
43. Everett RD, Rechter S, Papior P, Tavalai N, Stamminger T, Orr A. 2006. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80:7995-8005.
44. Eidson KM, Hobbs WE, Manning BJ, Carlson P, DeLuca NA. 2002. Expression of herpes simplex virus ICP0 inhibits the induction of interferon- stimulated genes by viral infection. J. Virol. 76:2180-2191.
45. 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.
46. 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.
47. Melroe GT, Silva L, Schaffer PA, Knipe DM. 2007. Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-beta induction. Virology 360:305-321.