Modified vaccinia virus Ankara can activate NF-κB transcription factors through a double-stranded RNA-activated protein kinase (PKR)-dependent pathway during the early phase of virus replication

Virology

Volumn 391, Issue 2, 2009, Pages 177-186

  Lynch, Heather E ^a   Ray, Caroline A ^a   Oie, Katrina L ^a   Pollara, Justin J ^b   Petty, Ian T D ^b   Sadler, Anthony J ^c   Williams, Bryan R G ^c   Pickup, David J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Cowpox; CP77; I kappaB; K1L; MVA; NF kappaB; Orthopoxvirus; PKR; Vaccine; Vaccinia

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE R; VIRUS DNA; VIRUS PROTEIN; VIRUS VECTOR;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CELL TYPE; CHO CELL; CONTROLLED STUDY; COWPOX VIRUS; DNA REPLICATION; EMBRYO; FEMALE; FIBROBLAST; GENE ACTIVATION; GENE INACTIVATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOPOXVIRUS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RABBIT; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION; VACCINIA VIRUS; VIRUS INACTIVATION; VIRUS REPLICATION;

ANIMALS; CELL LINE; CRICETINAE; EIF-2 KINASE; HUMANS; I-KAPPA B PROTEINS; MICE; NF-KAPPA B; VACCINIA VIRUS; VIRUS REPLICATION;

COWPOX VIRUS; ORTHOPOXVIRUS; VACCINIA VIRUS; VACCINIA VIRUS ANKARA;

EID: 68549125060     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.06.012     Document Type: Article

References (81)

1. Antoine G., Scheiflinger F., Dorner F., and Falkner F.G. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244 2 (1998) 365-396
2. Barton G.M. Viral recognition by Toll-like receptors. Semin. Immunol. 19 1 (2007) 33-40
3. Beattie E., Tartaglia J., and Paoletti E. Vaccinia virus-encoded eIF-2 alpha homolog abrogates the antiviral effect of interferon. Virology 183 1 (1991) 419-422
4. Boone R.F., Parr R.P., and Moss B. Intermolecular duplexes formed from polyadenylylated vaccinia virus RNA. J. Virol. 30 1 (1979) 365-374
5. Bowie A.G., and Haga I.R. The role of Toll-like receptors in the host response to viruses. Mol. Immunol. 42 8 (2005) 859-867
6. Bowie A.G., and Fitzgerald K.A. RIG-I: tri-ing to discriminate between self and non-self RNA. Trends Immunol. 28 4 (2007) 147-150
7. Bowie A., Kiss-Toth E., Symons J.A., Smith G.L., Dower S.K., and O'Neill L.A. 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 18 (2000) 10162-10167
8. Brandt T.A., and Jacobs B.L. Both carboxy- and amino-terminal domains of the vaccinia virus interferon resistance gene, E3L, are required for pathogenesis in a mouse model. J. Virol. 75 2 (2001) 850-856
9. Brandt T., Heck M.C., Vijaysri S., Jentarra G.M., Cameron J.M., and Jacobs B.L. The N-terminal domain of the vaccinia virus E3L-protein is required for neurovirulence, but not induction of a protective immune response. Virology 333 2 (2005) 263-270
10. Carmody R.J., and Chen Y.H. Nuclear factor-kappaB: activation and regulation during toll-like receptor signaling. Cell. Mol. Immunol. 4 1 (2007) 31-41
11. Carroll M.W., and Moss B. Host range and cytopathogenicity of the highly attenuated MVA strain of vaccinia virus: propagation and generation of recombinant viruses in a nonhuman mammalian cell line. Virology 238 2 (1997) 198-211
12. Chang H.W., Watson J.C., and Jacobs B.L. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc. Natl. Acad. Sci. U. S. A. 89 11 (1992) 4825-4829
13. Chen R.A., Ryzhakov G., Cooray S., Randow F., and Smith G.L. Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4 2 (2008) e22
14. Colby C., Jurale C., and Kates J.R. Mechanism of synthesis of vaccinia virus double-stranded ribonucleic acid in vivo and in vitro. J. Virol. 7 1 (1971) 71-76
15. Davies M.V., Elroy-Stein O., Jagus R., Moss B., and Kaufman R.J. The vaccinia virus K3L gene product potentiates translation by inhibiting double-stranded-RNA-activated protein kinase and phosphorylation of the alpha subunit of eukaryotic initiation factor 2. J. Virol. 66 4 (1992) 1943-1950
16. Davies M.V., Chang H.W., Jacobs B.L., and Kaufman R.J. The E3L and K3L vaccinia virus gene products stimulate translation through inhibition of the double-stranded RNA-dependent protein kinase by different mechanisms. J. Virol. 67 3 (1993) 1688-1692
17. Deb A., Zamanian-Daryoush M., Xu Z., Kadereit S., and Williams B.R. Protein kinase PKR is required for platelet-derived growth factor signaling of c-fos gene expression via Erks and Stat3. EMBO J. 20 10 (2001) 2487-2496
18. Deng L., Dai P., Ding W., Granstein R.D., and Shuman S. Vaccinia virus infection attenuates innate immune responses and antigen presentation by epidermal dendritic cells. J. Virol. 80 20 (2006) 9977-9987
19. Dignam J.D., Lebovitz R.M., and Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11 5 (1983) 1475-1489
20. DiPerna G., Stack J., Bowie A.G., Boyd A., Kotwal G., Zhang Z., Arvikar S., Latz E., Fitzgerald K.A., and Marshall W.L. Poxvirus protein N1L targets the I-kappaB kinase complex, inhibits signaling to NF-kappaB by the tumor necrosis factor superfamily of receptors, and inhibits NF-kappaB and IRF3 signaling by toll-like receptors. J. Biol. Chem. 279 35 (2004) 36570-36578
21. Doyle S.L., and O'Neill L.A. Toll-like receptors: from the discovery of NFkappaB to new insights into transcriptional regulations in innate immunity. Biochem. Pharmacol. 72 9 (2006) 1102-1113
22. Drillien R., Spehner D., and Kirn A. Host range restriction of vaccinia virus in Chinese hamster ovary cells: relationship to shutoff of protein synthesis. J. Virol. 28 3 (1978) 843-850
23. Earl P.L., Cooper N., and Moss B. Preparation of cell cultures and vaccinia virus stocks. In: Ausubel R.E.B.F.M., Kingston D.D., Moore J.D., Seidman J.A., Smith J.A., and Struhl K. (Eds). Current Protocols in Molecular Biology 2 (1991), Greene Publishing Associates, Wiley-Interscience, New York 16.16.1-16.16.7.
24. Enesa K., Zakkar M., Chaudhury H., Luong le A., Rawlinson L., Mason J.C., Haskard D.O., Dean J.L., and Evans P.C. NF-kappaB suppression by the deubiquitinating enzyme Cezanne: a novel negative feedback loop in pro-inflammatory signaling. J. Biol. Chem. 283 11 (2008) 7036-7045
25. Finberg R.W., and Kurt-Jones E.A. Viruses and Toll-like receptors. Microbes Infect. 6 15 (2004) 1356-1360
26. Gallego-Gomez J.C., Risco C., Rodriguez D., Cabezas P., Guerra S., Carrascosa J.L., and Esteban M. Differences in virus-induced cell morphology and in virus maturation between MVA and other strains (WR, Ankara, and NYCBH) of vaccinia virus in infected human cells. J. Virol. 77 19 (2003) 10606-10622
27. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., and Esteban M. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70 4 (2006) 1032-1060
28. Garcia M.A., Meurs E.F., and Esteban M. The dsRNA protein kinase PKR: Virus and cell control. Biochimie 89 6-7 (2007) 799-811
29. Gedey R., Jin X.L., Hinthong O., and Shisler J.L. Poxviral regulation of the host NF-kappaB response: the vaccinia virus M2L protein inhibits induction of NF-kappaB activation via an ERK2 pathway in virus-infected human embryonic kidney cells. J. Virol. 80 17 (2006) 8676-8685
30. Goh K.C., deVeer M.J., and Williams B.R. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J. 19 16 (2000) 4292-4297
31. Guerra S., Lopez-Fernandez L.A., Conde R., Pascual-Montano A., Harshman K., and Esteban M. Microarray analysis reveals characteristic changes of host cell gene expression in response to attenuated modified vaccinia virus Ankara infection of human HeLa cells. J. Virol. 78 11 (2004) 5820-5834
32. Guerra S., Lopez-Fernandez L.A., Pascual-Montano A., Najera J.L., Zaballos A., and Esteban M. Host response to the attenuated poxvirus vector NYVAC: upregulation of apoptotic genes and NF-kappaB-responsive genes in infected HeLa cells. J. Virol. 80 2 (2006) 985-998
33. Hanson C.V. Photochemical inactivation of viruses with psoralens: an overview. Blood Cells 18 1 (1992) 7-25
34. 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. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J. Exp. Med. 197 3 (2003) 343-351
35. Hayden M.S., West A.P., and Ghosh S. NF-kappaB and the immune response. Oncogene 25 51 (2006) 6758-6780
36. Heyninck K., and Beyaert R. A20 inhibits NF-kappaB activation by dual ubiquitin-editing functions. Trends Biochem. Sci. 30 1 (2005) 1-4
37. Hiscott J., Kwon H., and Genin P. Hostile takeovers: viral appropriation of the NF-kappaB pathway. J. Clin. Invest. 107 2 (2001) 143-151
38. Hiscott J., Nguyen T.L., Arguello M., Nakhaei P., and Paz S. Manipulation of the nuclear factor-kappaB pathway and the innate immune response by viruses. Oncogene 25 51 (2006) 6844-6867
39. Hoffmann A., and Baltimore D. Circuitry of nuclear factor kappaB signaling. Immunol. Rev. 210 (2006) 171-186
40. Hoffmann A., Natoli G., and Ghosh G. Transcriptional regulation via the NF-kappaB signaling module. Oncogene 25 51 (2006) 6706-6716
41. Hsiao J.C., Chung C.S., Drillien R., and Chang W. The cowpox virus host range gene, CP77, affects phosphorylation of eIF2 alpha and vaccinia viral translation in apoptotic HeLa cells. Virology 329 1 (2004) 199-212
42. Hu F.Q., Smith C.A., and Pickup D.J. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 204 1 (1994) 343-356
43. Humlova Z., Vokurka M., Esteban M., and Melkova Z. Vaccinia virus induces apoptosis of infected macrophages. J. Gen. Virol. 83 Pt 11 (2002) 2821-2832
44. Jentarra G.M., Heck M.C., Youn J.W., Kibler K., Langland J.O., Baskin C.R., Ananieva O., Chang Y., and Jacobs B.L. Vaccinia viruses with mutations in the E3L gene as potential replication-competent, attenuated vaccines: scarification vaccination. Vaccine 26 23 (2008) 2860-2872
45. Kibler K.V., Shors T., Perkins K.B., Zeman C.C., Banaszak M.P., Biesterfeldt J., Langland J.O., and Jacobs B.L. Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells. J. Virol. 71 3 (1997) 1992-2003
46. Kirchhoff S., Koromilas A.E., Schaper F., Grashoff M., Sonenberg N., and Hauser H. IRF-1 induced cell growth inhibition and interferon induction requires the activity of the protein kinase PKR. Oncogene 11 3 (1995) 439-445
47. Kumar A., Haque J., Lacoste J., Hiscott J., and Williams B.R. Double-stranded RNA-dependent protein kinase activates transcription factor NF-kappa B by phosphorylating I kappa B. Proc. Natl. Acad. Sci. U. S. A. 91 14 (1994) 6288-6292
48. Kumar A., Yang Y.L., Flati V., Der S., Kadereit S., Deb A., Haque J., Reis L., Weissmann C., and Williams B.R. Deficient cytokine signaling in mouse embryo fibroblasts with a targeted deletion in the PKR gene: role of IRF-1 and NF-kappaB. EMBO J. 16 2 (1997) 406-416
49. Laegreid A., Medvedev A., Nonstad U., Bombara M.P., Ranges G., Sundan A., and Espevik T. Tumor necrosis factor receptor p75 mediates cell-specific activation of nuclear factor kappa B and induction of human cytomegalovirus enhancer. J. Biol. Chem. 269 10 (1994) 7785-7791
50. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 5259 (1970) 680-685
51. Langland J.O., and Jacobs B.L. The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. Virology 299 1 (2002) 133-141
52. Langland J.O., Kash J.C., Carter V., Thomas M.J., Katze M.G., and Jacobs B.L. Suppression of proinflammatory signal transduction and gene expression by the dual nucleic acid binding domains of the vaccinia virus E3L proteins. J. Virol. 80 20 (2006) 10083-10095
53. Loparev V.N., Parsons J.M., Knight J.C., Panus J.F., Ray C.A., Buller R.M., Pickup D.J., and Esposito J.J. A third distinct tumor necrosis factor receptor of orthopoxviruses. Proc. Natl. Acad. Sci. U. S. A. 95 7 (1998) 3786-3791
54. Ludwig H., Suezer Y., Waibler Z., Kalinke U., Schnierle B.S., and Sutter G. Double-stranded RNA-binding protein E3 controls translation of viral intermediate RNA, marking an essential step in the life cycle of modified vaccinia virus Ankara. J. Gen. Virol. 87 Pt 5 (2006) 1145-1155
55. Mathes E., O'Dea E.L., Hoffmann A., and Ghosh G. NF-kappaB dictates the degradation pathway of IkappaBalpha. EMBO J. 27 9 (2008) 1357-1367
56. Meyer H., Sutter G., and Mayr A. Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J. Gen. Virol. 72 Pt 5 (1991) 1031-1038
57. Meylan E., and Tschopp J. Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol. Cell 22 5 (2006) 561-569
58. Moss B., and Shisler J.L. Immunology 101 at poxvirus U: immune evasion genes. Semin. Immunol. 13 1 (2001) 59-66
59. Moss B.L., Gross S., Gammon S.T., Vinjamoori A., and Piwnica-Worms D. Identification of a ligand-induced transient refractory period in nuclear factor-kappaB signaling. J. Biol. Chem. 283 13 (2008) 8687-8698
60. Oie K.L., and Pickup D.J. Cowpox virus and other members of the orthopoxvirus genus interfere with the regulation of NF-kappaB activation. Virology 288 1 (2001) 175-187
61. Panus J.F., Smith C.A., Ray C.A., Smith T.D., Patel D.D., and Pickup D.J. Cowpox virus encodes a fifth member of the tumor necrosis factor receptor family: a soluble, secreted CD30 homologue. Proc. Natl. Acad. Sci. U. S. A. 99 12 (2002) 8348-8353
62. Perkins N.D., and Gilmore T.D. Good cop, bad cop: the different faces of NF-kappaB. Cell Death Differ. 13 5 (2006) 759-772
63. Perkus M.E., Limbach K., and Paoletti E. Cloning and expression of foreign genes in vaccinia virus, using a host range selection system. J. Virol. 63 9 (1989) 3829-3836
64. Perkus M.E., Goebel S.J., Davis S.W., Johnson G.P., Limbach K., Norton E.K., and Paoletti E. Vaccinia virus host range genes. Virology 179 1 (1990) 276-286
65. Pickup D.J. Understanding orthopoxvirus interference with host immune responses to inform novel vaccine design. Expert Rev. Vaccines 6 1 (2007) 87-95
66. Ramsey-Ewing A.L., and Moss B. Complementation of a vaccinia virus host-range K1L gene deletion by the nonhomologous CP77 gene. Virology 222 1 (1996) 75-86
67. Sancho M.C., Schleich S., Griffiths G., and Krijnse-Locker J. The block in assembly of modified vaccinia virus Ankara in HeLa cells reveals new insights into vaccinia virus morphogenesis. J. Virol. 76 16 (2002) 8318-8334
68. Saraiva M., and Alcami A. CrmE, a novel soluble tumor necrosis factor receptor encoded by poxviruses. J. Virol. 75 1 (2001) 226-233
69. Scheidereit C. IkappaB kinase complexes: gateways to NF-kappaB activation and transcription. Oncogene 25 51 (2006) 6685-6705
70. Seet B.T., Johnston J.B., Brunetti C.R., Barrett J.W., Everett H., Cameron C., Sypula J., Nazarian S.H., Lucas A., and McFadden G. Poxviruses and immune evasion. Annu. Rev. Immunol. 21 (2003) 377-423
71. Shisler J.L., and Jin X.L. The vaccinia virus K1L gene product inhibits host NF-kappaB activation by preventing IkappaBalpha degradation. J. Virol. 78 7 (2004) 3553-3560
72. Smith C.A., Hu F.Q., Smith T.D., Richards C.L., Smolak P., Goodwin R.G., and Pickup D.J. Cowpox virus genome encodes a second soluble homologue of cellular TNF receptors, distinct from CrmB, that binds TNF but not LT alpha. Virology 223 1 (1996) 132-147
73. Southern E.M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98 3 (1975) 503-517
74. Spehner D., Gillard S., Drillien R., and Kirn A. A cowpox virus gene required for multiplication in Chinese hamster ovary cells. J. Virol. 62 4 (1988) 1297-1304
75. Staib C., Drexler I., and Sutter G. Construction and isolation of recombinant MVA. Methods Mol. Biol. 269 (2004) 77-100
76. Sutter G., and Moss B. Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proc. Natl. Acad. Sci. U. S. A. 89 22 (1992) 10847-10851
77. Sutter G., Ramsey-Ewing A., Rosales R., and Moss B. Stable expression of the vaccinia virus K1L gene in rabbit cells complements the host range defect of a vaccinia virus mutant. J. Virol. 68 7 (1994) 4109-4116
78. Tsung K., Yim J.H., Marti W., Buller R.M., and Norton J.A. Gene expression and cytopathic effect of vaccinia virus inactivated by psoralen and long-wave UV light. J. Virol. 70 1 (1996) 165-171
79. Vijaysri S., Jentarra G., Heck M.C., Mercer A.A., McInnes C.J., and Jacobs B.L. Vaccinia viruses with mutations in the E3L gene as potential replication-competent, attenuated vaccines: intra-nasal vaccination. Vaccine 26 5 (2008) 664-676
80. Yang Y.L., Reis L.F., Pavlovic J., Aguzzi A., Schafer R., Kumar A., Williams B.R., Aguet M., and Weissmann C. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14 24 (1995) 6095-6106
81. Zhang P., and Samuel C.E. Induction of protein kinase PKR-dependent activation of interferon regulatory factor 3 by vaccinia virus occurs through adapter IPS-1 signaling. J. Biol. Chem. 283 50 (2008) 34580-34587