Vaccinia virus K1 ankyrin repeat protein inhibits NF-κB activation by preventing RelA acetylation

Journal of General Virology

Volumn 97, Issue 10, 2016, Pages 2691-2702

  Bravo Cruz, Ariana G ^a   Shisler, Joanna L ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Ankyrin; K1; NF B; Poxvirus; RelA; Vaccinia

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OLIGONUCLEOTIDE; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; VACCINIA VIRUS K1 PROTEIN; VIRAL PROTEIN; ANKYRIN; PROTEIN BINDING;

ANKYRIN REPEAT DOMAIN; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; TRANSCRIPTION INITIATION; VACCINIA VIRUS; ACETYLATION; CHEMISTRY; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; VACCINIA; VIROLOGY;

ACETYLATION; ANKYRIN REPEAT; HUMANS; NF-KAPPA B; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; VACCINIA; VACCINIA VIRUS; VIRAL PROTEINS;

EID: 84991730506     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000576     Document Type: Article

References (73)

1. Aravalli, R. N., Hu, S. & Lokensgard, J. R. (2008). Inhibition of toll-like receptor signaling in primary murine microglia. J Neuroimmune Pharmacol 3, 5-11.
2. Bhatt, D. & Ghosh, S. (2014). Regulation of the NF-κB-mediated transcription of inflammatory genes. Front Immunol 5, 71.
3. Bitra, K., Suderman, R. J. & Strand, M. R. (2012). Polydnavirus Ank proteins bind NF-κB homodimers and inhibit processing of Relish. PLoS Pathog 8, e1002722.
4. Bowie, A., Kiss-Toth, E., Symons, J. A., Smith, G. L., Dower, S. K. & 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.
5. Burles, K., van Buuren, N. & Barry, M. (2014). Ectromelia virus encodes a family of Ankyrin/F-box proteins that regulate NFκB. Virology 468-470, 351-362.
6. Buttigieg, K., Laidlaw, S. M., Ross, C., Davies, M., Goodbourn, S. & Skinner, M. A. (2013). Genetic screen of a library of chimeric poxviruses identifies an ankyrin repeat protein involved in resistance to the avian type I interferon response. J Virol 87, 5028-5040.
7. Cabanski, M., Steinmüller, M., Marsh, L. M., Surdziel, E., Seeger, W. & Lohmeyer, J. (2008). PKR regulates TLR2/TLR4-dependent signaling in murine alveolar macrophages. Am J Respir Cell Mol Biol 38, 26-31.
8. Camus-Bouclainville, C., Fiette, L., Bouchiha, S., Pignolet, B., Counor, D., Filipe, C., Gelfi, J. & Messud-Petit, F. (2004). A virulence factor of myxoma virus colocalizes with NF-B in the nucleus and interferes with inflammation. J Virol 78, 2510-2516.
9. Chang, S. J., Hsiao, J. C., Sonnberg, S., Chiang, C. T., Yang, M. H., Tzou, D. L., Mercer, A. A. & Chang, W. (2009). Poxvirus host range protein CP77 contains an F-box-like domain that is necessary to suppress NFkappaB activation by tumor necrosis factor alpha but is independent of its host range function. J Virol 83, 4140-4152.
10. Chen, J. & Chen, L. F. (2015). Methods to detect NF-κB acetylation and methylation. Methods Mol Biol 1280, 395-409.
11. Chen, L., Fischle, W., Verdin, E. & Greene, W. C. (2001). Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293, 1653-1657.
12. Chen, R. A., Ryzhakov, G., Cooray, S., Randow, F. & Smith, G. L. (2008). Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog 4, e22.
13. Chen, Z., Hagler, J., Palombella, V. J., Melandri, F., Scherer, D., Ballard, D. & Maniatis, T. (1995). Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev 9, 1586-1597.
14. da Silva Correia, J. & Ulevitch, R. J. (2002). MD-2 and TLR4 N-linked glycosylations are important for a functional lipopolysaccharide receptor. J Biol Chem 277, 1845-1854.
15. Diel, D. G., Luo, S., Delhon, G., Peng, Y., Flores, E. F. & Rock, D. L. (2011). A nuclear inhibitor of NF-kappaB encoded by a poxvirus. J Virol 85, 264-275.
16. DiPerna, G., Stack, J., Bowie, A. G., Boyd, A., Kotwal, G., Zhang, Z., Arvikar, S., Latz, E., Fitzgerald, K. A. & other authors (2004). Poxvirus protein N1L targets the I-kappaB kinase complex, inhibits signaling to NFkappaB by the tumor necrosis factor superfamily of receptors, and inhibits NF-kappaB and IRF3 signaling by toll-like receptors. J Biol Chem 279, 36570-36578.
17. Dreyfus, D. H., Liu, Y., Ghoda, L. Y. & Chang, J. T. (2011). Analysis of an ankyrin-like region in Epstein Barr Virus encoded (EBV) BZLF-1 (ZEBRA) protein: implications for interactions with NF-κB and p53. Virol J 8, 422.
18. Drillien, R., Koehren, F. & Kirn, A. (1981). Host range deletion mutant of vaccinia virus defective in human cells. Virology 111, 488-499.
19. Ember, S. W., Ren, H., Ferguson, B. J. & Smith, G. L. (2012). Vaccinia virus protein C4 inhibits NF-κB activation and promotes virus virulence. J Gen Virol 93, 2098-2108.
20. Friedrich, K., Hanauer, J. R., Prüfer, S., Münch, R. C., Völker, I., Filippis, C., Jost, C., Hanschmann, K. M., Cattaneo, R. & other authors (2013). DARPin-targeting of measles virus: unique bispecificity, effective oncolysis, and enhanced safety. Mol Ther 21, 849-859.
21. Gates, L. T. & Shisler, J. L. (2016). cFLIPL interrupts IRF3-CBP-DNA interactions to inhibit IRF3-driven transcription. J Immunol 197, 923-933.
22. Gedey, R., Jin, X. L., Hinthong, O. & Shisler, J. L. (2006). Poxviral regulation of the host NF-kappaB response: the vaccinia virus M2L protein inhibits induction of NF-kappaB activation via an ERK2 pathway in virusinfected human embryonic kidney cells. J Virol 80, 8676-8685.
23. Gerritsen, M. E., Williams, A. J., Neish, A. S., Moore, S., Shi, Y. & Collins, T. (1997). CREB-binding protein/p300 are transcriptional coactivators of p65. Proc Natl Acad Sci U S A 94, 2927-2932.
24. Gilbert, S. C. (2013). Clinical development of modified vaccinia virus ankara vaccines. Vaccine 31, 4241-4246.
25. Hayden, M. S. & Ghosh, S. (2008). Shared principles in NF-kappaB signaling. Cell 132, 344-362.
26. Hayden, M. S. & Ghosh, S. (2014). Regulation of NF-κB by TNF family cytokines. Semin Immunol 26, 253-266.
27. Herbert, M. H., Squire, C. J. & Mercer, A. A. (2015). Poxviral ankyrin proteins. Viruses 7, 709-738.
28. Hinz, M., Arslan, SÇ. & Scheidereit, C. (2012). It takes two to tango: IkBs, the multifunctional partners of NF-κB. Immunol Rev 246, 59-76.
29. Hinz, M. & Scheidereit, C. (2014). The IkB kinase complex in NF-κB regulation and beyond. EMBO Rep 15, 46-61.
30. Huang, B., Yang, X. D., Lamb, A. & Chen, L. F. (2010). Posttranslational modifications of NF-kappaB: another layer of regulation for NF-kappaB signaling pathway. Cell Signal 22, 1282-1290.
31. Hyndman, B. D., Thompson, P., Bayly, R., Côté, G. P. & LeBrun, D. P. (2012). E2A proteins enhance the histone acetyltransferase activity of the transcriptional co-activators CBP and p300. Biochim Biophys Acta 1819, 446-453.
32. Li, J., Mahajan, A. & Tsai, M. D. (2006). Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry 45, 15168-15178.
33. Li, Y., Meng, X., Xiang, Y. & Deng, J. (2010). Structure function studies of vaccinia virus host range protein k1 reveal a novel functional surface for ankyrin repeat proteins. J Virol 84, 3331-3338.
34. Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
35. Mansur, D. S., Maluquer de Motes, C., Unterholzner, L., Sumner, R. P., Ferguson, B. J., Ren, H., Strnadova, P., Bowie, A. G. & Smith, G. L. (2013). Poxvirus targeting of E3 ligase b-TrCP by molecular mimicry: a mechanism to inhibit NF-κB activation and promote immune evasion and virulence. PLoS Pathog 9, e1003183.
36. McCraith, S., Holtzman, T., Moss, B. & Fields, S. (2000). Genome-wide analysis of vaccinia virus protein-protein interactions. Proc Natl Acad Sci U S A 97, 4879-4884.
37. Meng, X. & Xiang, Y. (2006). Vaccinia virus K1L protein supports viral replication in human and rabbit cells through a cell-type-specific set of its ankyrin repeat residues that are distinct from its binding site for ACAP2. Virology 353, 220-233.
38. Meng, X., Schoggins, J., Rose, L., Cao, J., Ploss, A., Rice, C. M. & Xiang, Y. (2012). C7L family of poxvirus host range genes inhibits antiviral activities induced by type I interferons and interferon regulatory factor 1. J Virol 86, 4538-4547.
39. Mohamed, M. R., Rahman, M. M., Lanchbury, J. S., Shattuck, D., Neff, C., Dufford, M., van Buuren, N., Fagan, K., Barry, M. & other authors (2009). Proteomic screening of variola virus reveals a unique NFkappaB inhibitor that is highly conserved among pathogenic orthopoxviruses. Proc Natl Acad Sci U S A 106, 9045-9050.
40. Mosavi, L. K., Cammett, T. J., Desrosiers, D. C. & Peng, Z. Y. (2004). The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13, 1435-1448.
41. Moss, B. (2013). Poxviridae. In Fields Virology, 6th edn, pp. 2129-2159. Edited by P. M. H. David & M. Knipe. Philadelphia, PA: Lippincott Williams & Wilkins.
42. Mukherjee, S. P., Behar, M., Birnbaum, H. A., Hoffmann, A., Wright, P. E. & Ghosh, G. (2013). Analysis of the RelA:CBP/p300 interaction reveals its involvement in NF-κB-driven transcription. PLoS Biol 11, e1001647.
43. Myskiw, C., Arsenio, J., van Bruggen, R., Deschambault, Y. & Cao, J. (2009). Vaccinia virus E3 suppresses expression of diverse cytokines through inhibition of the PKR, NF-kappaB, and IRF3 pathways. J Virol 83, 6757-6768.
44. Oda, S., Schröder, M. & Khan, A. R. (2009). Structural basis for targeting of human RNA helicase DDX3 by poxvirus protein K7. Structure 17, 1528-1537.
45. Oie, K. L. & Pickup, D. J. (2001). Cowpox virus and other members of the orthopoxvirus genus interfere with the regulation of NF-kappaB activation. Virology 288, 175-187.
46. Orphanides, G., Lagrange, T. & Reinberg, D. (1996). The general transcription factors of RNA polymerase II. Genes Dev 10, 2657-2683.
47. Perkus, M. E., Panicali, D., Mercer, S. & Paoletti, E. (1986). Insertion and deletion mutants of vaccinia virus. Virology 152, 285-297.
48. Randall, C. M., Jokela, J. A. & Shisler, J. L. (2012). The MC159 protein from the molluscum contagiosum poxvirus inhibits NF-κB activation by interacting with the IkB kinase complex. J Immunol 188, 2371-2379.
49. Randall, C. M., Biswas, S., Selen, C. V. & Shisler, J. L. (2014). Inhibition of interferon gene activation by death-effector domain-containing proteins from the molluscum contagiosum virus. Proc Natl Acad Sci U S A 111, E265-272.
50. Revilla, Y., Callejo, M., Rodriguez, J. M., Culebras, E., Nogal, M. L., Salas, M. L., Vinuela, E. & Fresno, M. (1998). Inhibition of nuclear factor kappa B activation by a virus-encoded Ikappa B-like protein. J Biol Chem 273, 5405-5411.
51. Sánchez-Sampedro, L., Perdiguero, B., Mejías-Pérez, E., García-Arriaza, J., Di Pilato, M. & Esteban, M. (2015). The evolution of poxvirus vaccines. Viruses 7, 1726-1803.
52. Scherer, D. C., Brockman, J. A., Chen, Z., Maniatis, T. & Ballard, D. W. (1995). Signal-induced degradation of I kappa B alpha requires site-specific ubiquitination. Proc Natl Acad Sci U S A 92, 11259-11263.
53. Schröder, M., Baran, M. & Bowie, A. G. (2008). Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J 27, 2147-2157.
54. Schweizer, A., Rusert, P., Berlinger, L., Ruprecht, C. R., Mann, A., Corthésy, S., Turville, S. G., Aravantinou, M., Fischer, M. & other authors (2008). CD4-specific designed ankyrin repeat proteins are novel potent HIV entry inhibitors with unique characteristics. PLoS Pathog 4, e1000109.
55. Sette, A., Grey, H., Oseroff, C., Peters, B., Moutaftsi, M., Crotty, S., Assarsson, E., Greenbaum, J., Kim, Y. & other authors (2009). Definition of epitopes and antigens recognized by vaccinia specific immune responses: their conservation in variola virus sequences, and use as a model system to study complex pathogens. Vaccine 27, G21-G26.
56. Shisler, J. L. & Jin, X. L. (2004). The vaccinia virus K1L gene product inhibits host NF-kappaB activation by preventing IkappaBalpha degradation. J Virol 78, 3553-3560.
57. Sivan, G., Ormanoglu, P., Buehler, E. C., Martin, S. E. & Moss, B. (2015). Identification of restriction factors by human genome-wide rna interference screening of viral host range mutants exemplified by discovery of SAMD9 and WDR6 as inhibitors of the vaccinia virus K1L-C7L-Mutant. MBio 6, e01122.
58. Smith, G. L., Benfield, C. T., Maluquer de Motes, C., Mazzon, M., Ember, S. W., Ferguson, B. J. & Sumner, R. P. (2013). Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J Gen Virol 94, 2367-2392.
59. Sonnberg, S., Seet, B. T., Pawson, T., Fleming, S. B. & Mercer, A. A. (2008). Poxvirus ankyrin repeat proteins are a unique class of F-box proteins that associate with cellular SCF1 ubiquitin ligase complexes. Proc Natl Acad Sci U S A 105, 10955-10960.
60. Sperling, K. M., Schwantes, A., Schnierle, B. S. & Sutter, G. (2008). The highly conserved orthopoxvirus 68k ankyrin-like protein is part of a cellular SCF ubiquitin ligase complex. Virology 374, 234-239.
61. Stumpp, M. T. & Amstutz, P. (2007). DARPins: a true alternative to antibodies. Curr Opin Drug Discov Devel 10, 153-159.
62. Sumner, R. P., Maluquer de Motes, C., Veyer, D. L. & Smith, G. L. (2014). Vaccinia virus inhibits NF-κB-dependent gene expression downstream of p65 translocation. J Virol 88, 3092-3102.
63. Takada, Y., Ichikawa, H., Pataer, A., Swisher, S. & Aggarwal, B. B. (2007). Genetic deletion of PKR abrogates TNF-induced activation of IkappaBalpha kinase, JNK, Akt and cell proliferation but potentiates p44/p42 MAPK and p38 MAPK activation. Oncogene 26, 1201-1212.
64. Van Antwerp, D. J. & Verma, I. M. (1996). Signal-induced degradation of I (kappa)B(alpha): association with NF-kappaB and the PEST sequence in I (kappa)B(alpha) are not required. Mol Cell Biol 16, 6037-6045.
65. Van Buuren, N., Couturier, B., Xiong, Y. & Barry, M. (2008). Ectromelia virus encodes a novel family of F-box proteins that interact with the SCF complex. J Virol 82, 9917-9927.
66. Wang, R. & Brattain, M. G. (2007). The maximal size of protein to diffuse through the nuclear pore is larger than 60kDa. FEBS Lett 581, 3164-3170.
67. Werden, S. J., Lanchbury, J., Shattuck, D., Neff, C., Dufford, M. & McFadden, G. (2009). The myxoma virus m-t5 ankyrin repeat host range protein is a novel adaptor that coordinately links the cellular signaling pathways mediated by Akt and Skp1 in virus-infected cells. J Virol 83, 12068-12083.
68. Willis, K. L., Patel, S., Xiang, Y. & Shisler, J. L. (2009). The effect of the vaccinia K1 protein on the PKR-eIF2alpha pathway in RK13 and HeLa cells. Virology 394, 73-81.
69. Willis, K. L., Langland, J. O. & Shisler, J. L. (2011). Viral dsRNAs from vaccinia virus early or intermediate gene transcripts possess PKR activating function, resulting in NF-{kappa}B activation, when the K1 protein is absent or mutated. J Biol Chem 286, 7765-7778.
70. Yim, H. C. & Williams, B. R. (2014). Protein kinase R and the inflammasome. J Interferon Cytokine Res 34, 447-454.
71. Zamanian-Daryoush, M., Mogensen, T. H., DiDonato, J. A. & Williams, B. R. (2000). NF-kappaB activation by double-stranded-RNAactivated protein kinase (PKR) is mediated through NF-kappaB-inducing kinase and IkappaB kinase. Mol Cell Biol 20, 1278-1290.
72. Zhang, P., Jacobs, B. L. & Samuel, C. E. (2008). Loss of protein kinase PKR expression in human HeLa cells complements the vaccinia virus E3L deletion mutant phenotype by restoration of viral protein synthesis. J Virol 82, 840-848.
73. Zhou, Y., Chase, B. I., Whitmore, M., Williams, B. R. & Zhou, A. (2005). Double-stranded RNA-dependent protein kinase (PKR) is downregulated by phorbol ester. FEBS J 272, 1568-1576.