Vaccinia virus-mediated inhibition of type I interferon responses is a multifactorial process involving the soluble type I interferon receptor B18 and intracellular components

Journal of Virology

Volumn 83, Issue 4, 2009, Pages 1563-1571

  Waibler, Zoe ^a   Anzaghe, Martina ^a   Frenz, Theresa ^a   Schwantes, Astrid ^a   Pöhlmann, Christopher ^a   Ludwig, Holger ^a   Palomo Otero, Marcos ^b   Alcamí, Antonio ^b   Sutter, Gerd ^a   Kalinke, Ulrich ^a,c  

^a PAUL EHRLICH INSTITUT   (Germany)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; INTERFERON RECEPTOR; INTERFERON RECEPTOR B8; UNCLASSIFIED DRUG; VACCINIA VACCINE;

ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL CULTURE; CEREBROVASCULAR ACCIDENT; CHICK EMBRYO; CHICKEN; CHORIOALLANTOIS; CONTROLLED STUDY; DENDRITIC CELL; EMBRYO; FIBROBLAST; GENE MUTATION; GENOME; IMMUNE RESPONSE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUPERNATANT; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIRUS INFECTION; VIRUS ISOLATION; VIRUS STRAIN;

ANIMALS; CELLS, CULTURED; HOST-PATHOGEN INTERACTIONS; INTERFERON TYPE I; MICE; MICE, INBRED C57BL; PROTEINS; VACCINIA VIRUS; VIRAL PROTEINS;

MUS; VACCINIA VIRUS; VACCINIA VIRUS ANKARA; VESICULAR STOMATITIS VIRUS;

EID: 59649093180     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01617-08     Document Type: Article

References (62)

1. Alcamí, A. 2003. Viral mimicry of cytokines, chemokines and their receptors. Nat. Rev. Immunol. 3:36-50.
2. Alcamí, A. 2007. New insights into the subversion of the chemokine system by poxviruses. Eur. J. Immunol. 37:880-883.
3. Alcamí, A., and U. H. Koszinowski. 2000. Viral mechanisms of immune evasion. Immunol. Today 21:447-455.
4. Alcamí, A., and G. L. Smith. 1995. Cytokine receptors encoded by poxviruses: a lesson in cytokine biology. Immunol. Today 16:474-478.
5. Alcamí, A., J. A. Symons, P. D. Collins, T. J. Williams, and G. L. Smith. 1998. Blockade of chemokine activity by a soluble chemokine binding protein from vaccinia virus. J. Immunol. 160:624-633.
6. Alcamí, A., J. A. Symons, and G. L. Smith. 2000. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J. Virol. 74:11230-11239.
7. Altenburger, W., C. P. Suter, and J. Altenburger. 1989. Partial deletion of the human host range gene in the attenuated vaccinia virus MVA. Arch. Virol. 105:15-27.
8. Antoine, G., F. Scheiflinger, F. Dorner, and F. G. Falkner. 1998. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365-396.
9. Asselin-Paturel, C., A. Boonstra, M. Dalod, I. Durand, N. Yessaad, C. zutter-Dambuyant, A. Vicari, A. O'Garra, C. Biron, F. Briere, and G. Trinchieri. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2:1144-1150.
10. Asselin-Paturel, C., and G. Trinchieri. 2005. Production of type I interferons: plasmacytoid dendritic cells and beyond. J. Exp. Med. 202:461-465.
11. Barchet, W., M. Cella, and M. Colonna. 2005. Plasmacytoid dendritic cells - virus experts of innate immunity. Semin. Immunol. 17:253-261.
12. Barchet, W., M. Cella, B. Odermatt, C. Asselin-Paturel, M. Colonna, and U. Kalinke. 2002. Virus-induced interferon alpha production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195:507-516.
13. Blanchard, T. J., A. Alcamí, P. Andrea, and G. L. Smith. 1998. Modified vaccinia virus Ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. J. Gen. Virol. 79(Pt. 5):1159-1167.
14. Chahroudi, A., D. A. Garber, P. Reeves, L. Liu, D. Kalman, and M. B. Feinberg. 2006. Differences and similarities in viral life cycle progression and host cell physiology after infection of human dendritic cells with modified vaccinia virus Ankara and vaccinia virus. J. Virol. 80:8469-8481.
15. Chang, T. H., C. L. Liao, and Y. L. Lin. 2006. Flavivirus induces interferon-beta gene expression through a pathway involving RIG-I-dependent IRF-3 and PI3K-dependent NF-κB activation. Microbes Infect. 8:157-171.
16. + cell subsets in human peripheral blood. Immunology 68:486-490.
17. Chen, R. A., N. Jacobs, and G. L. Smith. 2006. Vaccinia virus strain Western Reserve protein B14 is an intracellular virulence factor. J. Gen. Virol. 87: 1451-1458.
18. Chen, R. A., G. Ryzhakov, S. Cooray, F. Randow, and G. L. Smith. 2008. Inhibition of NF-κB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4:e22.
19. Colamonici, O. R., P. Domanski, S. M. Sweitzer, A. Larner, and R. M. Buller. 1995. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J. Biol. Chem. 270:15974-15978.
20. Colonna, M., G. Trinchieri, and Y. J. Liu. 2004. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5:1219-1226.
21. Decker, T., M. Muller, and S. Stockinger. 2005. The yin and yang of type I interferon activity in bacterial infection. Nat. Rev. Immunol. 5:675-687.
22. Diebold, S. S., M. Montoya, H. Unger, L. Alexopoulou, P. Roy, L. E. Haswell, A. Al Shamkhani, R. Flavell, P. Borrow, and Reis e Sousa. 2003. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 424:324-328.
23. DiPerna, G., J. Stack, A. G. Bowie, A. Boyd, G. Kotwal, Z. Zhang, S. Arvikar, E. Latz, K. A. Fitzgerald, and W. L. Marshall. 2004. Poxvirus protein N1L targets the I-κB kinase complex, inhibits signaling to NF-κB by the tumor necrosis factor superfamily of receptors, and inhibits NF-κB and IRF3 signaling by Toll-like receptors. J. Biol. Chem. 279:36570-36578.
24. Drillien, R., D. Spehner, and D. Hanau. 2004. Modified vaccinia virus Ankara induces moderate activation of human dendritic cells. J. Gen. Virol. 85:2167-2175.
25. Engelmayer, J., M. Larsson, M. Subklewe, A. Chahroudi, W. I. Cox, R. M. Steinman, and N. Bhardwaj. 1999. Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J. Immunol. 163:6762-6768.
26. Georgel, P., Z. Jiang, S. Kunz, E. Janssen, J. Mols, K. Hoebe, S. Bahram, M. B. Oldstone, and B. Beutler. 2007. Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 362:304-313.
27. Goebel, S. J., G. P. Johnson, M. E. Perkus, S. W. Davis, J. P. Winslow, and E. Paoletti. 1990. The complete DNA sequence of vaccinia virus. Virology 179:247-263.
28. Honda, K., A. Takaoka, and T. Taniguchi. 2006. Type I interferon gene induction by the interferon regulatory factor family of transcription factors. Immunity 25:349-360.
29. Hornemann, S., O. Harlin, C. Staib, S. Kisling, V. Erfle, B. Kaspers, G. Hacker, and G. Sutter. 2003. Replication of modified vaccinia virus Ankara in primary chicken embryo fibroblasts requires expression of the interferon resistance gene E3L. J. Virol. 77:8394-8407.
30. Huang, S., W. Hendriks, A. Althage, S. Hemmi, H. Bluethmann, R. Kamijo, J. Vilcek, R. M. Zinkernagel, and M. Aguet. 1993. Immune response in mice that lack the interferon-gamma receptor. Science 259:1742-1745.
31. Isaacs, A., and J. Lindenmann. 1957. Virus interference. I. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 147:258-267.
32. Karupiah, G., T. N. Fredrickson, K. L. Holmes, L. H. Khairallah, and R. M. Buller. 1993. Importance of interferons in recovery from mousepox. J. Virol. 67:4214-4226.
33. Kato, H., S. Sato, M. Yoneyama, M. Yamamoto, S. Uematsu, K. Matsui, T. Tsujimura, K. Takeda, T. Fujita, O. Takeuchi, and S. Akira. 2005. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23:19-28.
34. Lund, J. M., L. Alexopoulou, A. Sato, M. Karow, N. C. Adams, N. W. Gale, A. Iwasaki, and R. A. Flavell. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101:5598-5603.
35. Mayr, A., H. Stickl, H. K. Muller, K. Danner, and H. Singer. 1978. The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism. Zentralbl. Bakteriol. B 167:375-390.
36. Meyer, H., G. Sutter, and A. Mayr. 1991. Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J. Gen. Virol. 72(Pt. 5):1031-1038.
37. Moss, B., and J. L. Shisler. 2001. Immunology 101 at poxvirus U: immune evasion genes. Semin. Immunol. 13:59-66.
38. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
39. Noppert, S. J., K. A. Fitzgerald, and P. J. Hertzog. 2007. The role of type I interferons in TLR responses. Immunol. Cell Biol. 85:446-457.
40. Ploegh, H. L. 1998. Viral strategies of immune evasion. Science 280:248-253.
41. Reis e Sousa, C. 2004. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 16:21-25.
42. Rodriguez, J. R., D. Rodriguez, and M. Esteban. 1991. Interferon treatment inhibits early events in vaccinia virus gene expression in infected mice. Virology 185:929-933.
43. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
44. Shisler, J. L., and X.-L. Jin. 2004. The vaccinia virus K1L gene product inhibits host NF-κB activation by preventing NF-κBα degradation. J. Virol. 78:3553-3560.
45. Shortman, K., and Y. J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2:151-161.
46. Smith, G. L., J. A. Symons, A. Khanna, A. Vanderplasschen, and A. Alcamí. 1997. Vaccinia virus immune evasion. Immunol. Rev. 159:137-154.
47. Smith, V. P., and A. Alcamí. 2002. Inhibition of interferons by ectromelia virus. J. Virol. 76:1124-1134.
48. Stack, J., I. R. Haga, M. Schroder, N. W. Bartlett, G. Maloney, P. C. Reading, K. A. Fitzgerald, G. L. Smith, and A. G. Bowie. 2005. Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. J. Exp. Med. 201:1007-1018.
49. Staib, C., and G. Sutter. 2003. Live viral vectors: vaccinia virus. Methods Mol. Med. 87:51-68.
50. Stojdl, D. F., B. D. Lichty, B. R. tenOever, J. M. Paterson, A. T. Power, S. Knowles, R. Marius, J. Reynard, L. Poliquin, H. Atkins, E. G. Brown, R. K. Durbin, J. E. Durbin, J. Hiscott, and J. C. Bell. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
51. Symons, J. A., A. Alcamí, and G. L. Smith. 1995. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81:551-560.
52. Tailor, P., T. Tamura, and K. Ozato. 2006. IRF family proteins and type I interferon induction in dendritic cells. Cell Res. 16:134-140.
53. Thompson, L. J., G. A. Kolumam, S. Thomas, and K. Murali-Krishna. 2006. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J. Immunol. 177:1746-1754.
54. Toma-Hirano, M., S. Namiki, S. Miyatake, K. Arai, and Y. Kamogawa-Schifter. 2007. Type I interferon regulates pDC maturation and Ly49Q expression. Eur. J. Immunol. 37:2707-2714.
55. van den Broek, M. F., U. Muller, S. Huang, M. Aguet, and R. M. Zinkernagel. 1995. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J. Virol. 69:4792-4796.
56. van den Broek, M. F., U. Muller, S. Huang, R. M. Zinkernagel, and M. Aguet. 1995. Immune defence in mice lacking type I and/or type II interferon receptors. Immunol. Rev. 148:5-18.
57. Waibler, Z., M. Anzaghe, H. Ludwig, S. Akira, S. Weiss, G. Sutter, and U. Kalinke. 2007. Modified vaccinia virus Ankara induces Toll-like receptor independent type I interferon responses. J. Virol. 81:12102-12110.
58. Weber, F., and O. Haller. 2007. Viral suppression of the interferon system. Biochimie 89:836-842.
59. Weber, F., G. Kochs, and O. Haller. 2004. Inverse interference: how viruses fight the interferon system. Viral Immunol. 17:498-515.
60. Wilson, N. S., G. M. Behrens, R. J. Lundie, C. M. Smith, J. Waithman, L. Young, S. P. Forehan, A. Mount, R. J. Steptoe, K. D. Shortman, T. F. de Koning-Ward, G. T. Belz, F. R. Carbone, B. S. Crabb, W. R. Heath, and J. A. Villadangos. 2006. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 7:165-172.
61. + T cells: a potential mechanism for direct presentation. Virology 359:349-361.
62. Zhu, J., J. Martinez, X. Huang, and Y. Yang. 2007. Innate immunity against vaccinia virus is mediated by TLR2 and requires TLR-independent production of IFN-β. Blood 109:619-625.