Poxviral protein A52 stimulates p38 mitogen-activated protein kinase (MAPK) activation by causing tumor necrosis factor receptor-associated factor 6 (TRAF6) self-association leading to transforming growth factor β-activated kinase 1 (TAK1) recruitment

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 33642-33653

  Stack, Julianne ^a   Hurst, Tara P ^a   Flannery, Sinead M ^a   Brennan, Kiva ^a   Rupp, Sebastian ^a   Oda, Shun Ichiro ^a   Khan, Amir R ^a   Bowie, Andrew G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER INTERFACE; INNATE IMMUNES; MOLECULAR MECHANISM; P38 MITOGEN-ACTIVATED PROTEIN KINASE; SELF-ASSOCIATIONS; SIGNALING PATHWAYS; TRANSFORMING GROWTH FACTORS; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED FACTORS;

DIMERS; ENZYME ACTIVITY; PROTEINS; VIRUSES;

ASSOCIATION REACTIONS;

GAL 4 CHOP FUSION PROTEIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HYBRID PROTEIN; I KAPPA B; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 2; INTERLEUKIN 8; LUCIFERASE; METHIONINE; MITOGEN ACTIVATED PROTEIN KINASE P38; POXVIRUS A52 PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CYTOKINE PRODUCTION; DIMERIZATION; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION; UBIQUITINATION;

NF-KAPPA B (NF-KB); P38 MAPK; POX VIRUSES; SIGNAL TRANSDUCTION; TRAF6; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ANIMALS; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-10; MAP KINASE KINASE KINASES; MICE; MICE, KNOCKOUT; MUTATION, MISSENSE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; TNF RECEPTOR-ASSOCIATED FACTOR 6; VACCINIA; VACCINIA VIRUS; VIRAL PROTEINS;

EID: 84888349515     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.485490     Document Type: Article

References (48)

1. Bowie, A. G., and Unterholzner, L. (2008) Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev. Immunol. 8, 911-922
2. Stack, J., Haga, I. R., Schröder, M., Bartlett, N. W., Maloney, G., Reading, P. C., Fitzgerald, K. A., Smith, G. L., and Bowie, A. G. (2005) Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. J. Exp. Med. 201, 1007-1018
3. Harte, M. T., Haga, I. R., Maloney, G., Gray, P., Reading, P. C., Bartlett, N. W., Smith, G. L., Bowie, A., and O'Neill, L. A. (2003) The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J. Exp. Med. 197, 343-351
4. Di Perna, G., Stack, J., Bowie, A. G., Boyd, A., Kotwal, G., Zhang, Z., Arvikar, S., Latz, E., Fitzgerald, K. A., and Marshall, W. L. (2004) Poxvirus protein N1L targets the I-kB kinase complex, inhibits signaling to NF-kB by the tumor necrosis factor superfamily of receptors, and inhibits NF-kB and IRF3 signaling by toll-like receptors. J. Biol. Chem. 279, 36570-36578
5. Chen, R. A., Ryzhakov, G., Cooray, S., Randow, F., and Smith, G. L. (2008) Inhibition of IkB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4, e22
6. Schröder, M., Baran, M., and Bowie, A. G. (2008) Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKe-mediated IRF activation. EMBOJ. 27, 2147-2157
7. Unterholzner, L., Sumner, R. P., Baran, M., Ren, H., Mansur, D. S., Bourke, N. M., Randow, F., Smith, G. L., and Bowie, A. G. (2011) Vaccinia virus protein C6 is a virulence factor that binds TBK-1 adaptor proteins and inhibits activation of IRF3 and IRF7. PLoS Pathog. 7, e1002247
8. Mansur, D. S., Maluquer De Motes, C., Unterholzner, L., Sumner, R. P., Ferguson, B. J., Ren, H., Strnadova, P., Bowie, A. G., and Smith, G. L. (2013) Poxvirus targeting of E3 ligase β-TrCP by molecular mimicry: a mechanism to inhibit NF-kB activation and promote immune evasion and virulence. PLoSPathog 9, e1003183
9. Blasius, A. L., and Beutler, B. (2010) Intracellular toll-like receptors. Immunity 32, 305-315
10. O'Neill, L. A., and Bowie, A. G. (2007) The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nature reviews. Immunology 7, 353-364
11. Takeuchi, O., and Akira, S. (2002) MyD88 as a bottle neck in Toll/IL-1 signaling. Curr. Top. Microbiol. Immunol. 270, 155-167
12. Lin, S. C., Lo, Y. C., and Wu, H. (2010) Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature 465, 885-890
13. Kawagoe, T., Sato, S., Matsushita, K., Kato, H, Matsui, K., Kumagai, Y., Saitoh, T., Kawai, T., Takeuchi, O., and Akira, S. (2008) Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat. Immunol. 9, 684-691
14. Kawai, T., and Akira, S. (2007) TLR signaling. Semin Immunol. 19, 24-32
15. Stack, J., and Bowie, A. G. (2012) Poxviral protein A46 antagonizes Tolllike receptor 4 signaling by targeting BB loop motifs in Toll-IL-1 receptor adaptor proteins to disrupt receptor: adaptor interactions. J. Biol. Chem. 287, 22672-22682
16. Maloney, G., Schröder, M., and Bowie, A. G. (2005) Vaccinia virus protein A52R activates p38 mitogen-activated protein kinase and potentiates lipopolysaccharide-induced interleukin-10. J. Biol. Chem. 280, 30838-30844
17. Assarsson, E., Greenbaum, J. A., Sundström, M., Schaffer, L., Hammond, J. A., Pasquetto, V., Oseroff, C., Hendrickson, R. C., Lefkowitz, E. J., Tscharke, D. C., Sidney, J., Grey, H. M., Head, S. R., Peters, B., and Sette, A. (2008) Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc. Natl. Acad. Sci. U. S. A. 105, 2140-2145
18. Bowie, A., Kiss-Toth, E., Symons, J. A., Smith, G. L., Dower, S. K., and O'Neill, L. A. (2000) A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl. Acad. Sci. U. S. A. 97, 10162-10167
19. Keating, S. E., Maloney, G. M., Moran, E. M., and Bowie, A. G. (2007) IRAK-2 participates in multiple toll-like receptor signaling pathways to NFkappaB via activation of TRAF6 ubiquitination. The Journal of biological chemistry 282, 33435-33443
20. Landström, M. (2010) The TAK1-TRAF6 signalling pathway. Int. J. Biochem. Cell Biol. 42, 585-589
21. Uemura, N, Kajino, T., Sanjo, H, Sato, S., Akira, S., Matsumoto, K., and Ninomiya-Tsuji, J. (2006) TAK1 is a component of the Epstein-Barr virus LMP1 complex and is essential for activation of JNK but not of NF-kB. J. Biol. Chem. 281, 7863-7872
22. Poole, E., King, C. A., Sinclair, J. H, and Alcami, A. (2006) TheUL144gene product of human cytomegalovirus activates NFkB via a TRAF6-dependent mechanism. EMBOJ. 25, 4390-4399
23. La Monica, R., Kocer, S. S., Nazarova, J., Dowling, W., Geimonen, E., Shaw, R. D., and Mackow, E. R. (2001) VP4 differentially regulates TRAF2 signaling, disengaging JNK activation while directing NF-kB to effect rotavirus-specific cellular responses. J. Biol. Chem. 276, 19889-19896
24. Adhikari, A., Xu, M., and Chen, Z. J. (2007) Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26, 3214-3226
25. Kumar, H, Kawai, T., and Akira, S. (2009) Pathogen recognition in the innate immune response. Biochem. J. 420, 1-16
26. Ye, H., Arron, J. R., Lamothe, B., Cirilli, M., Kobayashi, T., Shevde, N. K., Segal, D., Dzivenu, O. K., Vologodskaia, M., Yim, M., Du, K., Singh, S., Pike, J. W., Darnay, B. G., Choi, Y., and Wu, H. (2002) Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418, 443-447
27. Noels, H, Van Loo, G., Hagens, S., Broeckx, V., Beyaert, R., Marynen, P., and Baens, M. (2007) A Novel TRAF6 binding site in MALT1 defines distinct mechanisms of NF-kB activation by API2-MALT1 fusions. J. Biol. Chem. 282, 10180-10189
28. Meads, M. B., Li, Z. W., and Dalton, W. S. (2010) A novel TNF receptor-associated factor 6 binding domain mediates NF-kB signaling by the common cytokine receptor β subunit. J. Immunol. 185, 1606-1615
29. Gentry, J. J., Rutkoski, N. J., Burke, T. L., and Carter, B. D. (2004) A functional interaction between the p75 neurotrophin receptor interacting factors, TRAF6 and NRIF. J. Biol. Chem. 279, 16646-16656
30. Wang, C, Deng, L., Hong, M., Akkaraju, G. R., Inoue, J., and Chen, Z. J. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351
31. Yamashita, M., Fatyol, K., Jin, C, Wang, X., Liu, Z., and Zhang, Y. E. (2008) TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-/3. Mol. Cell 31, 918-924
32. Sorrentino, A., Thakur, N., Grimsby, S., Marcusson, A., Von Bulow, V., Schuster, N., Zhang, S., Heldin, C. H, and Landström, M. (2008) The type I TGF-/3 receptor engages TRAF6 to activate TAK1 in a receptor kinaseindependent manner. Nat. Cell Biol. 10, 1199-1207
33. Yu, X., Yi, H., Guo, C, Zuo, D., Wang, Y., Kim, H. L., Subjeck, J. R., and Wang, X. Y. (2011) Pattern recognition scavenger receptor CD204 attenuates Toll-like receptor 4-induced NF-kB activation by directly inhibiting ubiquitination of tumor necrosis factor (TNF) receptor-associated factor 6. J. Biol. Chem. 286, 18795-18806
34. Katsoulidis, E., Li, Y., Mears, H., and Platanias, L. C. (2005) The p38 mitogen-activated protein kinase pathway in interferon signal transduction. J. Interferon Cytokine Res. 25, 749-756
35. Graham, S. C, Bahar, M. W., Cooray, S., Chen, R. A., Whalen, D. M., Abrescia, N. G., Alderton, D., Owens, R. J., Stuart, D. I., Smith, G. L., and Grimes, J. M. (2008) Vaccinia virus proteins A52 and B14 Share a Bcl-2-like fold but have evolved to inhibit NF-kB rather than apoptosis. PLoS Pathog. 4, e1000128
36. Benfield, C. T., Mansur, D. S., McCoy, L. E., Ferguson, B. J., Bahar, M. W., Oldring, A. P., Grimes, J. M., Stuart, D. I., Graham, S. C, and Smith, G. L. (2011) Mapping the IkB kinase beta (IKK/3)-binding interface of the B14 protein, a vaccinia virus inhibitor of IKK/3-mediated activation of nuclear factor kB. J. Biol. Chem. 286, 20727-20735
37. Park, K. J., Choi, S. H., Choi, D. H., Park, J. M., Yie, S. W., Lee, S. Y., and Hwang, S. B. (2003) 1Hepatitis C virus NS5A protein modulates c-Jun. N-terminal kinase through interaction with tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 278, 30711-30718
38. Shisler, J. L., and Jin, X. L. (2004) The vaccinia virus K1L gene product inhibits host NF-kB activation by preventing I'Ba degradation. J. Virol. 78, 3553-3560
39. Ember, S. W., Ren, H., Ferguson, B. J., and Smith, G. L. (2012) Vaccinia virus protein C4 inhibits NF-kB activation and promotes virus virulence. J. Gen. Virol. 93, 2098-2108
40. Hu, N., Yu, R., Shikuma, C, Shiramizu, B., Ostrwoski, M. A., and Yu, Q. (2009) Role of cell signaling in poxvirus-mediated foreign gene expression in mammalian cells. Vaccine 27, 2994-3006
41. Kanayama, A., Seth, R. B., Sun, L., Ea, C K., Hong, M., Shaito, A., Chiu, Y. H., Deng, L., and Chen, Z. J. (2004) TAB2 and TAB3 activate the NF-kB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548
42. Liu, S., and Chen, Z. J. (2011) Expanding role of ubiquitination in NF-kB signaling. CellRes. 21, 6-21
43. Cooray, S., Bahar, M. W., Abrescia, N. G., McVey, C. E., Bartlett, N. W., Chen, R. A., Stuart, D. I., Grimes, J. M., and Smith, G. L. (2007) Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. J. Gen. Virol. 88, 1656-1666
44. Kalverda, A. P., Thompson, G. S., Vogel, A., Schröder, M., Bowie, A. G., Khan, A. R., and Homans, S. W. (2009) Poxvirus K7 protein adopts a Bcl-2 fold: biochemical mapping of its interactions with human DEAD box RNA helicase DDX3. J. Mol. Biol. 385, 843-853
45. Oda, S., Schröder, M., and Khan, A. R. (2009) Structural basis for targeting of human RNA helicase DDX3 by poxvirus protein K7. Structure 17, 1528-1537
46. Maluquer De Motes, C, Cooray, S., Ren, H., Almeida, G. M., McGourty, K., Bahar, M. W., Stuart, D. I., Grimes, J. M., Graham, S. C, and Smith, G. L. (2011) Inhibition of apoptosis and NF-kB activation by vaccinia protein N1 occur via distinct binding surfaces and make different contributions to virulence. PLoS Pathog. 7, e1002430
47. Yin, Q., Lin, S. C, Lamothe, B., Lu, M., Lo, Y. C, Hura, G., Zheng, L., Rich, R. L., Campos, A. D., Myszka, D. G., Lenardo, M. J., Darnay, B. G., and Wu, H. (2009) E2 interaction and dimerization in the crystal structure of TRAF6. Nat. Struct. Mol. Biol. 16, 658-666
48. Laskowski, R. A. (2009) PDBsum new things. Nucleic Acids Res. 37, D355-D359