Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway

Virology

Volumn 362, Issue 2, 2007, Pages 304-313

  Georgel, Philippe ^a,c   Jiang, Zhengfan ^a   Kunz, Stefan ^a   Janssen, Edith ^b   Mols, Johann ^a   Hoebe, Kasper ^a   Bahram, Siamak ^c   Oldstone, Michael B A ^a   Beutler, Bruce ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c EA 3431   (France)

Author keywords

Antiviral; Immunity; Innate; Interferon; TLR; VSV

Indexed keywords

CD14 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 7; MYELOID DIFFERENTIATION FACTOR 88; THROMBOSPONDIN; TOLL LIKE RECEPTOR 4; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DENDRITIC CELL; DOWNSTREAM PROCESSING; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS VIRUS;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL LINE; CELL SURVIVAL; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTOR-7; INTERFERON TYPE I; MACROPHAGES, PERITONEAL; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; MYELIN PROTEINS; MYELOID DIFFERENTIATION FACTOR 88; PROTEOLIPIDS; RECEPTORS, INTERLEUKIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; VESICULAR STOMATITIS-INDIANA VIRUS; VIRAL ENVELOPE PROTEINS;

VESICULAR STOMATITIS VIRUS;

EID: 34247577195     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.12.032     Document Type: Article

References (45)

1. Alexopoulou L., Holt A.C., Medzhitov R., and Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001) 732-738
2. Barnes B.J., Richards J., Mancl M., Hanash S., Beretta L., and Pitha P.M. Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J. Biol. Chem. 279 (2004) 45194-45207
3. Berczi I., Bertok L., and Bereznai T. Comparative studies on the toxicity of Escherichia coli lipopolysaccharide endotoxin in various animal species. Can. J. Microbiol. 12 (1966) 1070-1071
4. Beutler B., Jiang Z., Georgel P., Crozat K., Croker B., Rutschmann S., Du X., and Hoebe K. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24 (2006) 353-389
5. Boehme K.W., Guerrero M., and Compton T. Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J. Immunol. 177 (2006) 7094-7102
6. Brawand P., Fitzpatrick D.R., Greenfield B.W., Brasel K., Maliszewski C.R., and De S.T. Murine plasmacytoid pre-dendritic cells generated from Flt3 ligand-supplemented bone marrow cultures are immature APCs. J. Immunol. 169 (2002) 6711-6719
7. Burzyn D., Rassa J.C., Kim D., Nepomnaschy I., Ross S.R., and Piazzon I. Toll-like receptor 4-dependent activation of dendritic cells by a retrovirus. J. Virol. 78 (2004) 576-584
8. Caput D., Beutler B., Hartog K., Thayer R., Brown-Shimer S., and Cerami A. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 1670-1674
9. Colonna M., Krug A., and Cella M. Interferon-producing cells: on the front line in immune responses against pathogens. Curr. Opin. Immunol. 14 (2002) 373-379
10. Diao J., Winter E., Chen W., Cantin C., and Cattral M.S. Characterization of distinct conventional and plasmacytoid dendritic cell-committed precursors in murine bone marrow. J. Immunol. 173 (2004) 826-833
11. Diebold S.S., Montoya M., Unger H., Alexopoulou L., Roy P., Haswell L.E., Al-Shamkhani A., Flavell R., and Borrow P. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424 (2003) 324-328
12. Ehl S., Bischoff R., Ostler T., Vallbracht S., Schulte-Monting J., Poltorak A., and Freudenberg M. The role of Toll-like receptor 4 versus interleukin-12 in immunity to respiratory syncytial virus. Eur. J. Immunol. 34 (2004) 1146-1153
13. Fitzgerald K.A., Rowe D.C., Barnes B.J., Caffrey D.R., Visintin A., Latz E., Monks B., Pitha P.M., and Golenbock D.T. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198 (2003) 1043-1055
14. Haynes L.M., Moore D.D., Kurt-Jones E.A., Finberg R.W., Anderson L.J., and Tripp R.A. Involvement of Toll-like receptor 4 in innate immunity to respiratory syncytial virus. J. Virol. 75 (2001) 10730-10737
15. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., and Bauer S. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303 (2004) 1526-1529
16. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., and Akira S. A Toll-like receptor recognizes bacterial DNA. Nature 408 (2000) 740-745
17. Hoebe K., Du X., Georgel P., Janssen E., Tabeta K., Kim S.O., Goode J., Lin P., Mann N., Mudd S., Crozat K., Sovath S., Han J., and Beutler B. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424 (2003) 743-748
18. Hoffmann B., Beer M., Schutze H., and Mettenleiter T.C. Fish rhabdoviruses: molecular epidemiology and evolution. Curr. Top. Microbiol. Immunol. 292 (2005) 81-117
19. Janssen E., Tabeta K., Barnes M.J., Rutschmann S., McBride S., Bahjat K.S., Schoenberger S.P., Theofilopoulos A.N., Beutler B., and Hoebe K. Efficient T cell activation via a Toll-interleukin 1 receptor-independent pathway. Immunity 24 (2006) 787-799
20. Jault C., Pichon L., and Chluba J. Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol. Immunol. 40 (2004) 759-771
21. Jiang Z., Georgel P., Du X., Shamel L., Sovath S., Mudd S., Huber M., Kalis C., Keck S., Galanos C., Freudenberg M., and Beutler B. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6 (2005) 565-570
22. Jude B.A., Pobezinskaya Y., Bishop J., Parke S., Medzhitov R.M., Chervonsky A.V., and Golovkina T.V. Subversion of the innate immune system by a retrovirus. Nat. Immunol. 4 (2003) 573-578
23. Kato H., Sato S., Yoneyama M., Yamamoto M., Uematsu S., Matsui K., Tsujimura T., Takeda K., Fujita T., Takeuchi O., and Akira S. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23 (2005) 19-28
24. Kato H., Sato S., Yoneyama M., Yamamoto M., Uematsu S., Matsui K., Tsujimura T., Takeda K., Fujita T., Takeuchi O., and Akira S. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23 (2005) 19-28
25. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., and Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6 (2005) 981-988
26. Krug A., French A.R., Barchet W., Fischer J.A., Dzionek A., Pingel J.T., Orihuela M.M., Akira S., Yokoyama W.M., and Colonna M. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21 (2004) 107-119
27. Kuate S., Stahl-Hennig C., Stoiber H., Nchinda G., Floto A., Franz M., Sauermann U., Bredl S., Deml L., Ignatius R., Norley S., Racz P., Tenner-Racz K., Steinman R.M., Wagner R., and Uberla K. Immunogenicity and efficacy of immunodeficiency virus-like particles pseudotyped with the G protein of vesicular stomatitis virus. Virology 351 (2006) 133-144
28. Kumar H., Kawai T., Kato H., Sato S., Takahashi K., Coban C., Yamamoto M., Uematsu S., Ishii K.J., Takeuchi O., and Akira S. Essential role of IPS-1 in innate immune responses against RNA viruses. J. Exp. Med. 203 (2006) 1795-1803
29. Kurt-Jones E.A., Popova L., Kwinn L., Haynes L.M., Jones L.P., Tripp R.A., Walsh E.E., Freeman M.W., Golenbock D.T., Anderson L.J., and Finberg R.W. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1 (2000) 398-401
30. Lund J.M., Alexopoulou L., Sato A., Karow M., Adams N.C., Gale N.W., Iwasaki A., and Flavell R.A. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 5598-5603
31. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., and Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437 (2005) 1167-1172
32. Monath T.P., Cropp C.B., Frazier C.L., Murphy F.A., and Whitfield S.G. Viruses isolated from reptiles: identification of three new members of the family Rhabdoviridae. Arch. Virol. 60 (1979) 1-12
33. Pillai R.S., Bhattacharyya S.N., Artus C.G., Zoller T., Cougot N., Basyuk E., Bertrand E., and Filipowicz W. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309 (2005) 1573-1576
34. Poltorak A., He X., Smirnova I., Liu M.Y., Van H.C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., and Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282 (1998) 2085-2088
35. Rassa J.C., Meyers J.L., Zhang Y., Kudaravalli R., and Ross S.R. Murine retroviruses activate B cells via interaction with Toll-like receptor 4. Proc.Natl. Acad. Sci. U.S.A. 99 (2002) 2281-2286
36. Roche S., Bressanelli S., Rey F.A., and Gaudin Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313 (2006) 187-191
37. Sato A., Linehan M.M., and Iwasaki A. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 17343-17348
38. Seth R.B., Sun L., Ea C.K., and Chen Z.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF3. Cell 122 (2005) 669-682
39. Smirnova I., Poltorak A., Chan E.K., McBride C., and Beutler B. Phylogenetic variation and polymorphism at the Toll-like receptor 4 locus (TLR4). Genome Biol. 1 (2000) 1-10
40. Tabeta K., Georgel P., Janssen E., Du X., Hoebe K., Crozat K., Mudd S., Shamel L., Sovath S., Goode J., Alexopoulou L., Flavell R.A., and Beutler B. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 3516-3521
41. Tabeta K., Hoebe K., Janssen E.M., Du X., Georgel P., Crozat K., Mudd S., Mann N., Sovath S., Goode J., Shamel L., Herskovits A.A., Portnoy D.A., Cooke M., Tarantino L.M., Wiltshire T., Steinberg B.E., Grinstein S., and Beutler B. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 7 (2006) 156-164
42. Xu L.G., Wang Y.Y., Han K.J., Li L.Y., Zhai Z., and Shu H.B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19 (2005) 727-740
43. Yamamoto M., Sato S., Hemmi H., Hoshino K., Kaisho T., Sanjo H., Takeuchi O., Sugiyama M., Okabe M., Takeda K., and Akira S. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301 (2003) 640-643
44. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
45. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale Jr. M., Akira S., Yonehara S., Kato A., and Fujita T. Shared and unique functions of the DExD/H-Box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175 (2005) 2851-2858