Inhibition of Double-Stranded RNA-Dependent Protein Kinase PKR by Vaccinia Virus E3: Role of Complex Formation and the E3 N-Terminal Domain

REFERENCES

• Akkaraju, G. R., P. Whitaker-Dowling, I. S. Younger, and R. Jagus 1989. Vaccinia specific kinase inhibitory factor prevents translational inhibition by double-stranded RNA in rabbit reticulocyte lysate. J. Biol. Chem. 264: 10321–10325.
   PubMed Web of Science ®Google Scholar
• Beattie, E., K. L. Denzler, J. Tartaglia, M. E. Perkus, E. Paoletti, and B. L. Jacobs 1995. Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene. J. Virol. 69: 499–505.
   PubMedGoogle Scholar
• Beattie, E., E. Paoletti, and J. Tartaglia 1995. Distinct patterns of IFN sensitivity observed in cells infected with vaccinia K3L− and E3L− mutant viruses. Virology 210: 254–263.
   PubMed Web of Science ®Google Scholar
• Benkirane, M., C. Neuveut, R. F. Chun, S. M. Smith, C. E. Samuel, A. Gatignol, and K. T. Jeang 1997. Oncogenic potential of TAR RNA binding protein TRBP and its regulatory interaction with RNA-dependent protein kinase PKR. EMBO J. 16: 611–624.
   PubMedGoogle Scholar
• Carpick, B. W., V. Graziano, D. Schneider, R. K. Maitra, X. Lee, and B. R. G. Williams 1997. Characterization of the solution complex between the interferon-induced, double-stranded RNA-activated protein kinase and HIV-1 trans-activating region RNA. J. Biol. Chem. 272: 9510–9516.
   PubMedGoogle Scholar
• Carroll, K., O. Elroy-Stein, B. Moss, and R. Jagus 1993. Recombinant vaccinia virus K3L gene product prevents activation of double-stranded RNA-dependent, initiation factor 2α-specific protein kinase. J. Biol. Chem. 268: 12837–12842.
   PubMed Web of Science ®Google Scholar
• Cesareni, G., and J. A. H. Murray Plasmid vectors carrying the replication origin of filamentous single-stranded phages Genetic engineering: principals and methods In: Setlow, J. K., and A. Hollaender91987135–154Plenum Press, New York, N.Y.
   Google Scholar
• Chang, H. W., J. C. Watson, and B. L. Jacobs 1992. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 89: 4825–4829.
   PubMed Web of Science ®Google Scholar
• Chang, H.-W., and B. L. Jacobs 1993. Identification of a conserved motif that is necessary for binding of the vaccinia virus E3L gene products to double-stranded. Virology 194: 537–547.
   PubMedGoogle Scholar
• Chang, H.-W., L. H. Uribe, and B. L. Jacobs 1995. Rescue of vaccinia virus lacking the E3L gene by mutants of E3L. J. Virol. 69: 6605–6608.
   PubMed Web of Science ®Google Scholar
• Chong, K. L., L. Feng, K. Schappert, E. Meurs, T. F. Donahue, J. D. Friesen, A. G. Hovanessian, and B. R. G. Williams 1992. Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. EMBO J. 11: 1553–1562.
   PubMed Web of Science ®Google Scholar
• Clemens, M. J. 1996. Protein kinases that phosphorylate eIF2 and eIF2B, and their role in eukaryotic cell translational control Translational control. In: Hershey, J. W. B., M. B. Mathews, and N. Sonenberg139–172Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Cosentino, G. P., S. Venkatesan, F. C. Serluca, S. R. Green, M. B. Mathews, and N. Sonenberg 1995. Double-stranded-RNA-dependent protein kinase and TAR RNA-binding protein form homo- and heterodimers in vivo. Proc. Natl. Acad. Sci. USA 92: 9445–9449.
   PubMedGoogle Scholar
• Craig, A. W. B., G. P. Cosentino, O. Donze, and N. Sonenberg 1996. The kinase insert domain of interferon-induced protein kinase PKR is required for activity but not for interaction with the pseudosubstrate K3L. J. Biol. Chem. 271: 24526–24533.
   PubMedGoogle Scholar
• Davies, M. V., H. W. Chang, B. L. Jacobs, and R. J. Kaufman 1993. 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: 1688–1692.
   PubMed Web of Science ®Google Scholar
• Dever, T. E., J. J. Chen, G. N. Barber, A. M. Cigan, L. Feng, T. F. Donahue, I. M. London, M. G. Katze, and A. G. Hinnebusch 1993. Mammalian eukaryotic initiation factor 2α kinases functionally substitute for GCN2 in the GCN4 translational control mechanism of yeast. Proc. Natl. Acad. Sci. USA 90: 4616–4620.
   PubMed Web of Science ®Google Scholar
• Dever, T. E., L. Feng, R. C. Wek, A. M. Cigan, T. D. Donahue, and A. G. Hinnebusch 1992. Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585–596.
   PubMed Web of Science ®Google Scholar
• Dever, T. E., R. Sripriya, J. R. McLachlin, J. Lu, J. R. Fabian, S. R. Kimball, and L. K. Miller 1998. Disruption of cellular translational control by a viral truncated eukaryotic translation initiation factor 2α kinase homolog. Proc. Natl. Acad. Sci. USA 95: 4164–4169.
   PubMedGoogle Scholar
• Feilotter, H. E., G. J. Hannon, C. J. Ruddell, and D. Beach 1994. Construction of an improved host strain for two hybrid screening. Nucleic Acids Res. 22: 1502–1503.
   PubMed Web of Science ®Google Scholar
• Gale, M., S.-L. Tan, M. Wambach, and M. G. Katze 1996. Interaction of the interferon-induced PKR protein kinase with inhibitory proteins P58IPK and vaccinia virus K3L is mediated by unique domains: implications for kinase regulation. Mol. Cell. Biol. 16: 4172–4181.
   PubMedGoogle Scholar
• Gale, M. J., M. J. Korth, N. M. Tang, S. L. Tab, D. A. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katze 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230: 217–227.
   PubMed Web of Science ®Google Scholar
• Haig, D. M., C. J. McInnes, J. Thomson, A. Wood, K. Bunyan, and A. Mercer 1998. The orf virus OV20.0L gene product is involved in interferon resistance and inhibits an interferon-inducible, double-stranded RNA-dependent kinase. Immunology 93: 335–340.
   PubMedGoogle Scholar
• Ho, C. K., and S. Shuman 1996. Physical and functional characterization of the double-stranded RNA binding protein encoded by the vaccinia virus E3 gene. Virology 217: 272–284.
   PubMedGoogle Scholar
• Hu, J. C., E. K. O’Shea, P. S. Kim, and R. T. Sauer 1990. Sequence requirements for coiled coils: analysis with lambda repressor-GCN4 leucine zipper fusions. Science 250: 1400–1403.
   PubMed Web of Science ®Google Scholar
• Hunter, T., T. Hunt, R. J. Jackson, and H. D. Robertson 1975. The characteristics of inhibition of protein synthesis by double-stranded ribonucleic acid in reticulocyte lysates. J. Biol. Chem. 250: 409–417.
   PubMedGoogle Scholar
• Ito, H., Y. Fukada, K. Murata, and A. Kimura 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153: 163–168.
   PubMed Web of Science ®Google Scholar
• Jagus, R., and M. M. Gray 1994. Proteins that interact with PKR. Biochimie 76: 779–791.
   PubMedGoogle Scholar
• Kawagishi-Kobayashi, M., J. B. Silverman, T. K. Ung, and T. E. Dever 1997. Regulation of the protein kinase PKR by the vaccinia virus pseudosubstrate inhibitor K3L is dependent on residues conserved between the K3L protein and the PKR substrate eIF2α. Mol. Cell. Biol. 17: 4146–4158.
   PubMedGoogle Scholar
• Kostura, M., and M. B. Mathews 1989. Purification and activation of the double-stranded RNA-dependent eIF-2 kinase DAI. Mol. Cell. Biol. 9: 1576–1586.
   PubMedGoogle Scholar
• Kozak, M. 1983. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol. Rev. 47: 1–45.
   PubMedGoogle Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
   PubMed Web of Science ®Google Scholar
• Langland, J. O., and B. L. Jacobs 1992. Cytosolic double-stranded RNA-dependent protein kinase is likely a dimer of partially phosphorylated Mr = 66,000 subunits. J. Biol. Chem. 267: 10729–10736.
   PubMed Web of Science ®Google Scholar
• Langland, J. O., S. M. Pettiford, B. Jiang, and B. L. Jacobs 1994. Products of the porcine N5P3 gene bind specifically to double-stranded RNA and inhibit activation of the interferon-induced protein kinase, PKR. J. Virol. 68: 3821–3829.
   PubMed Web of Science ®Google Scholar
• Mathews, M. B. 1993. Viral evasion of cellular defense mechanisms: regulation of the protein kinase DAI by RNA effectors. Semin. Virol. 4: 247–257.
   Google Scholar
• McMillan, N. A., B. W. Carpick, B. Hollis, W. M. Toone, M. Zamanian-Daryoush, and B. R. G. Williams 1995. Mutational analysis of the double-stranded RNA (dsRNA) binding domain of the dsRNA-activated protein kinase, PKR. J. Biol. Chem. 270: 2601–2606.
   PubMedGoogle Scholar
• Ortega, L. G., M. D. McCotter, G. L. Henry, S. J. McCormack, D. C. Thomis, and C. E. Samuel 1996. Mechanism of interferon action. Biochemical and genetic evidence for the intermolecular association of the RNA-dependent protein kinase PkR from human cells. Virology 215: 31–39.
   PubMedGoogle Scholar
• Park, H., M. V. Davies, J. O. Langland, H. W. Chang, Y. S. Nam, J. Tartaglia, E. Paoletti, B. L. Jacobs, R. J. Kaufman, and S. Venkatesan 1994. TAR RNA-binding protein is an inhibitor of the interferon-induced protein kinase PKR. Proc. Natl. Acad. Sci. USA 91: 4713–4717.
   PubMed Web of Science ®Google Scholar
• Patel, R. C., P. Stanton, N. M. J. McMillan, B. R. G. Williams, and G. C. Sen 1995. The interferon-inducible double-stranded RNA-activated protein kinase self-associates in vitro and in vivo. Proc. Natl. Acad. Sci. USA 92: 8283–8287.
   PubMedGoogle Scholar
• Patel, R. C., P. Stanton, and G. C. Sen 1996. Specific mutations near the amino terminus of double-stranded RNA-dependent protein kinase (PKR) differentially affect its double-stranded RNA binding and dimerization properties. J. Biol. Chem. 271: 25657–25663.
   PubMedGoogle Scholar
• Pavitt, G. D., W. Yang, and A. G. Hinnebusch 1997. Homologous segments in three subunits of the guanine nucleotide exchange factor eIF2B mediate translational regulation by phosphorylation of eIF2. Mol. Cell. Biol. 17: 1298–1313.
   PubMed Web of Science ®Google Scholar
• Romano, P. R., S. R. Green, G. N. Barber, M. B. Mathews, and A. G. Hinnebusch 1995. Structural requirements for double-stranded RNA binding, dimerization, and activation of the human eIF-2α kinase DAI in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 365–378.
   PubMedGoogle Scholar
• Schmedt, C., S. R. Green, L. Manche, D. R. Taylor, Y. Ma, and M. B. Mathews 1995. Functional characterization of the RNA-binding domain and motif of the double-stranded RNA-dependent protein kinase DAI (PKR). J. Mol. Biol. 249: 29–44.
   PubMedGoogle Scholar
• Sharp, T. V., A. Romashko, F. Moonan, B. Joshi, G. N. Barber, and R. Jagus. The vaccinia virus E3L gene product interacts with both the regulatory and substrate binding regions of PKR: implications for PKR autoregulation. Virology, in press.
   Google Scholar
• Sherman, F., G. R. Fink, and C. W. Lawrence 1974. Methods of yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Shors, T., and B. L. Jacobs 1997. Complementation of deletion of the vaccinia virus E3L gene by the Escherichia coli RNase III gene. Virology 227: 77–87.
   PubMedGoogle Scholar
• Shors, T., K. V. Kibler, K. B. Perkins, R. Seidler-Wulff, M. P. Banaszak, and B. L. Jacobs 1997. Complementation of vaccinia virus deleted of the E3L gene by mutants of E3L. Virology 239: 269–272.
   PubMedGoogle Scholar
• Sikorski, R. S., and P. Hieter 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19–27.
   PubMed Web of Science ®Google Scholar
• St Johnston, D., N. H. Brown, J. G. Gall, and M. Jantsch 1992. A conserved double-stranded RNA-binding domain. Proc. Natl. Acad. Sci. USA 89: 10979–10983.
   PubMed Web of Science ®Google Scholar
• Tan, S. L., M. J. Gale, and M. G. Katze 1998. Double-stranded RNA-independent dimerization of the interferon-induced protein kinase PKR and inhibition of dimerization by the cellular P58IPK inhibitor. Mol. Cell. Biol. 18: 2431–2443.
   PubMedGoogle Scholar
• Watson, J. C., H. W. Chang, and B. L. Jacobs 1991. Characterization of a vaccinia virus-encoded double-stranded RNA-binding protein that may be involved in inhibition of the double-stranded RNA-dependent protein kinase. Virology 185: 206–216.
   PubMedGoogle Scholar
• Wu, S., and R. J. Kaufman 1996. Double-stranded (ds) RNA binding and not dimerization correlates with the activation of the dsRNA-dependent protein kinase (PKR). J. Biol. Chem. 271: 1756–1763.
   PubMedGoogle Scholar
• Wu, S., and R. J. Kaufman 1997. A model for the double-stranded RNA (dsRNA)-dependent dimerization and activation of the dsRNA-activated protein kinase PKR. J. Biol. Chem. 272: 1291–1296.
   PubMedGoogle Scholar
• Yon, J., and M. Fried 1988. Precise gene fusion by PCR. Nucleic Acids Res. 17: 4895.
   Google Scholar
• Yuwen, H., J. H. Cox, J. W. Yewdell, J. R. Bennink, and B. Moss 1993. Nuclear localization of a double-stranded RNA-binding protein encoded by the vaccinia virus E3L gene. Virology 195: 732–744.
   PubMedGoogle Scholar
• Zhu, S., P. R. Romano, and R. C. Wek 1997. Ribosome targeting of PKR is mediated by two double-stranded RNA-binding domains and facilitates in vivo phosphorylation of eukaryotic initiation factor-2. J. Biol. Chem. 272: 14434–14441.
   PubMedGoogle Scholar