Measles virus V protein is a decoy substrate for IκB kinase α and prevents toll-like receptor 7/9-mediated interferon induction

Journal of Virology

Volumn 82, Issue 24, 2008, Pages 12365-12373

  Pfaller, Christian K ^a   Conzelmann, Karl Klaus ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GENE PRODUCT; I KAPPA B KINASE ALPHA; INTERFERON REGULATORY FACTOR 7; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; VIRUS PROTEIN V;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; GENE CONSTRUCT; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; INTERFERON PRODUCTION; MEASLES VIRUS; NONHUMAN; PARAMYXOVIRUS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

CELL LINE; DNA, COMPLEMENTARY; HUMANS; I-KAPPA B KINASE; INTERFERON REGULATORY FACTOR-7; INTERFERON-ALPHA; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9; VIRAL PROTEINS;

MEASLES VIRUS; PARAMYXOVIRIDAE;

EID: 57349113096     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01321-08     Document Type: Article

References (62)

1. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. USA 101:17264-17269.
2. 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.
3. Bellini, W. J., G. Englund, S. Rozenblatt, H. Arnheiter, and C. D. Richardson. 1985. Measles virus P gene codes for two proteins. J. Virol. 53:908-919.
4. Brzózka, K., S. Finke, and K.-K. Conzelmann. 2005. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79:7673-7681.
5. Brzózka, K., S. Finke, and K. K. Conzelmann. 2006. Inhibition of interferon signaling by rabies virus phosphoprotein P: activation-dependent binding of STAT1 and STAT2. J. Virol. 80:2675-2683.
6. Brzózka, K., C. Pfaller, and K. K. Conzelmann. 2007. Signal transduction in the type I interferon system and viral countermeasures. Signal Transduction 7:15-19.
7. Caignard, G., M. Guerbois, J. L. Labernardiere, Y. Jacob, L. M. Jones, F. Wild, F. Tangy, and P. O. Vidalain. 2007. Measles virus V protein blocks Jak1-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signaling. Virology 368:351-362.
8. Cao, W., and Y. J. Liu. 2007. Innate immune functions of plasmacytoid dendritic cells. Curr. Opin. Immunol. 19:24-30.
9. Cattaneo, R., K. Kaelin, K. Baczko, and M. A. Billeter. 1989. Measles virus editing provides an additional cysteine-rich protein. Cell 56:759-764.
10. Chen, M., J. C. Cortay, and D. Gerlier. 2003. Measles virus protein interactions in yeast: new findings and caveats. Virus Res. 98:123-129.
11. Childs, K., N. Stock, C. Ross, J. Andrejeva, L. Hilton, M. Skinner, R. Randall, and S. Goodbourn. 2007. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359:190-200.
12. Cruz, C. D., H. Palosaari, J.-P. Parisien, P. Devaux, R. Cattaneo, T. Ouchi, and C. M. Horvath. 2006. Measles virus V protein inhibits p53 family member p73. J. Virol. 80:5644-5650.
13. Cui, S., K. Eisenacher, A. Kirchhofer, K. Brzózka, A. Lammens, K. Lammens, T. Fujita, K. K. Conzelmann, A. Krug, and K. P. Hopfner. 2008. The C-terminal regulatory domain is the RNA 5′-triphosphate sensor of RIG-I. Mol. Cell 29:169-179.
14. Delgado, M. A., R. A. Elmaoued, A. S. Davis, G. Kyei, and V. Deretic. 2008. Toll-like receptors control autophagy. EMBO J. 27:1110-1121.
15. Devaux, P., and R. Cattaneo. 2004. Measles virus phosphoprotein gene products: conformational flexibility of the P/V protein amino-terminal domain and C protein infectivity factor function. J. Virol. 78:11632- 11640.
16. Devaux, P., G. Hodge, M. B. McChesney, and R. Cattaneo. 2008. Attenuation of V- or C-defective measles viruses: infection control by the inflammatory and interferon responses of rhesus monkeys. J. Virol. 82:5359-5367.
17. Devaux, P., V. von Messling, W. Songsungthong, C. Springfeld, and R. Cattaneo. 2007. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72-83.
18. Fitzgerald-Bocarsly, P., and D. Feng. 2007. The role of type I interferon production by dendritic cells in host defense. Biochimie 89:843-855.
19. Griffin, D. E. 2007. Measles virus, p. 1551-1586. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. Straus (ed.), Fields virology. Lippincott Williams and Wilkins, Philadelphia, PA.
20. Griffin, D. E., C. H. Pan, and W. J. Moss. 2008. Measles vaccines. Front. Biosci. 13:1352-1370.
21. Hahm, B., J. H. Cho, and M. B. Oldstone. 2007. Measles virus-dendritic cell interaction via SLAM inhibits innate immunity: selective signaling through TLR4 but not other TLRs mediates suppression of IL-12 synthesis. Virology 358:251-257.
22. Hemmi, H., T. Kaisho, O. Takeuchi, S. Sato, H. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira. 2002. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3:196-200.
23. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-745.
24. Honda, K., Y. Ohba, H. Yanai, H. Negishi, T. Mizutani, A. Takaoka, C. Taya, and T. Taniguchi. 2005. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434:1035-1040.
25. Honda, K., H. Yanai, T. Mizutani, H. Negishi, N. Shimada, N. Suzuki, Y. Ohba, A. Takaoka, W. C. Yeh, and T. Taniguchi. 2004. Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 101:15416-15421.
26. Honda, K., H. Yanai, H. Negishi, M. Asagiri, M. Sato, T. Mizutani, N. Shimada, Y. Ohba, A. Takaoka, N. Yoshida, and T. Taniguchi. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434:772-777.
27. Hornung, V., J. Ellegast, S. Kim, K. Brzózka, A. Jung, H. Kato, H. Poeck, S. Akira, K. K. Conzelmann, M. Schlee, S. Endres, and G. Hartmann. 2006. 5′-triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
28. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdorfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168:4531-4537.
29. Hoshino, K., T. Sugiyama, M. Matsumoto, T. Tanaka, M. Saito, H. Hemmi, O. Ohara, S. Akira, and T. Kaisho. 2006. IkappaB kinase-alpha is critical for interferon-alpha production induced by Toll-like receptors 7 and 9. Nature 440:949-953.
30. Ishii, K. J., S. Koyama, A. Nakagawa, C. Coban, and S. Akira. 2008. Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 3:352-363.
31. Ito, T., R. Amakawa, M. Inaba, T. Hori, M. Ota, K. Nakamura, M. Takebayashi, M. Miyaji, T. Yoshimura, K. Inaba, and S. Fukuhara. 2004. Plasmacytoid dendritic cells regulate Th cell responses through OX40 ligand and type I IFNs. J. Immunol. 172:4253-4259.
32. Izaguirre, A., B. J. Barnes, S. Amrute, W. S. Yeow, N. Megjugorac, J. Dai, D. Feng, E. Chung, P. M. Pitha, and P. Fitzgerald-Bocarsly. 2003. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J. Leukoc. Biol. 74:1125-1138.
33. Kawai, T., S. Sato, K. J. Ishii, C. Coban, H. Hemmi, M. Yamamoto, K. Terai, M. Matsuda, J. Inoue, S. Uematsu, O. Takeuchi, and S. Akira. 2004. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 5:1061-1068.
34. Kim, T. W., K. Staschke, K. Bulek, J. Yao, K. Peters, K. H. Oh, Y. Vandenburg, H. Xiao, W. Qian, T. Hamilton, B. Min, G. Sen, R. Gilmour, and X. Li. 2007. A critical role for IRAK4 kinase activity in Toll-like receptor-mediated innate immunity. J. Exp. Med. 204:1025-1036.
35. Krieg, A. M., and J. Vollmer. 2007. Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Immunol. Rev. 220:251-269.
36. Krug, A. 2008. Nucleic acid recognition receptors in autoimmunity. Handb. Exp. Pharmacol. 183:129-151.
37. Lee, H. K., J. M. Lund, B. Ramanathan, N. Mizushima, and A. Iwasaki. 2007. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 315:1398-1401.
38. Lin, R., Y. Mamane, and J. Hiscott. 2000. Multiple regulatory domains control IRF-7 activity in response to virus infection. J. Biol. Chem. 275:34320-34327.
39. Liston, P., and D. J. Briedis. 1994. Measles virus V protein binds zinc. Virology 198:399-404.
40. Lu, L. L., M. Puri, C. M. Horvath, and G. C. Sen. 2008. Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for IKKE/TBK1. J. Biol. Chem. 283:14269-14276.
41. Moss, W. J., M. O. Ota, and D. E. Griffin. 2004. Measles: immune suppression and immune responses. Int. J. Biochem. Cell Biol. 36:1380-1385.
42. Nakatsu, Y., M. Takeda, S. Ohno, R. Koga, and Y. Yanagi. 2006. Translational inhibition and increased interferon induction in cells infected with C protein-deficient measles virus. J. Virol. 80:11861-11867.
43. Ohno, S., N. Ono, M. Takeda, K. Takeuchi, and Y. Yanagi. 2004. Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. J. Gen. Virol. 85:2991-2999.
44. Palosaari, H., J.-P. Parisien, J. J. Rodriguez, C. M. Ulane, and C. M. Horvath. 2003. STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J. Virol. 77:7635-7644.
45. Paterson, R. G., G. P. Leser, M. A. Shaughnessy, and R. A. Lamb. 1995. The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 208:121-131.
46. Plumet, S., F. Herschke, J. M. Bourhis, H. Valentin, S. Longhi, and D. Gerlier. 2007. Cytosolic 5-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS ONE 2:e279.
47. Rao, N., S. Nguyen, K. Ngo, and W.-P. Fung-Leung. 2005. A novel splice variant of interleukin-1 receptor (IL-1R)-associated kinase 1 plays a negative regulatory role in Toll/IL-1R-induced inflammatory signaling. Mol. Cell. Biol. 25:6521-6532.
48. Schlender, J., V. Hornung, S. Finke, M. Günthner-Biller, S. Marozin, K. Brzózka, S. Moghim, S. Endres, G. Hartmann, and K.-K. Conzelmann. 2005. Inhibition of Toll-like receptor 7- and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79:5507-5515.
49. Schlender, J., J. J. Schnorr, P. Spielhoffer, T. Cathomen, R. Cattaneo, M. A. Billeter, V. ter Meulen, and S. Schneider-Schaulies. 1996. Interaction of measles virus glycoproteins with the surface of uninfected peripheral blood lymphocytes induces immunosuppression in vitro. Proc. Natl. Acad. Sci. USA 93:13194-13199.
50. Schneider-Schaulies, S., I. M. Klagge, and V. ter Meulen. 2003. Dendritic cells and measles virus infection. Curr. Top. Microbiol. Immunol. 276:77-101.
51. Servet-Delprat, C., P.-O. Vidalain, O. Azocar, F. Le Deist, A. Fischer, and C. Rabourdin-Combe. 2000. Consequences of Fas-mediated human dendritic cell apoptosis induced by measles virus. J. Virol. 74:4387-4393.
52. Servet-Delprat, C., P. O. Vidalain, H. Bausinger, S. Manie, F. Le Deist, O. Azocar, D. Hanau, A. Fischer, and C. Rabourdin-Combe. 2000. Measles virus induces abnormal differentiation of CD40 ligand-activated human dendritic cells. J. Immunol. 164:1753-1760.
53. Shaffer, J. A., W. J. Bellini, and P. A. Rota. 2003. The C protein of measles virus inhibits the type I interferon response. Virology 315:389-397.
54. Sumpter, R., Jr., Y.-M. Loo, E. Foy, K. Li, M. Yoneyama, T. Fujita, S. M. Lemon, and M. Gale, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
55. Takeuchi, K., S. I. Kadota, M. Takeda, N. Miyajima, and K. Nagata. 2003. Measles virus V protein blocks interferon (IFN)-alpha/beta but not IFN-gamma signaling by inhibiting STAT1 and STAT2 phosphorylation. FEBS Lett. 545:177-182.
56. Takeuchi, K., M. Takeda, N. Miyajima, Y. Ami, N. Nagata, Y. Suzaki, J. Shahnewaz, S.-I. Kadota, and K. Nagata. 2005. Stringent requirement for the C protein of wild-type measles virus for growth both in vitro and in macaques. J. Virol. 79:7838-7844.
57. Tamura, T., H. Yanai, D. Savitsky, and T. Taniguchi. 2008. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 26:535-584.
58. Uematsu, S., and S. Akira. 2007. Toll-like receptors and type I interferons. J. Biol. Chem. 282:15319-15323.
59. Uematsu, S., S. Sato, M. Yamamoto, T. Hirotani, H. Kato, F. Takeshita, M. Matsuda, C. Coban, K. J. Ishii, T. Kawai, O. Takeuchi, and S. Akira. 2005. Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7- and TLR9-mediated interferon-α induction. J. Exp. Med. 201:915-923.
60. Yang, K., A. Puel, S. Zhang, C. Eidenschenk, C. L. Ku, A. Casrouge, C. Picard, H. von Bernuth, B. Senechal, S. Plancoulaine, S. Al Hajjar, A. Al Ghonaium, L. Marodi, D. Davidson, D. Speert, C. Roifman, B. Z. Garty, A. Ozinsky, F. J. Barrat, R. L. Coffman, R. L. Miller, X. Li, P. Lebon, C. Rodriguez-Gallego, H. Chapel, F. Geissmann, E. Jouanguy, and J. L. Casanova. 2005. Human TLR-7-, -8-, and -9-mediated induction of IFN-alpha/ beta and -lambda is IRAK-4 dependent and redundant for protective immunity to viruses. Immunity 23:465-478.
61. Yokota, S., H. Saito, T. Kubota, N. Yokosawa, K. Amano, and N. Fujii. 2003. Measles virus suppresses interferon-alpha signaling pathway: suppression of Jak1 phosphorylation and association of viral accessory proteins, C and V, with interferon-alpha receptor complex. Virology 306:135-146.
62. Yount, J. S., L. Gitlin, T. M. Moran, and C. B. Lopez. 2008. MDA5 participates in the detection of paramyxovirus infection and is essential for the early activation of dendritic cells in response to Sendai virus defective interfering particles. J. Immunol. 180:4910-4918.