Translational resistance of late alphavirus mRNA to eIF2α phosphorylation: A strategy to overcome the antiviral effect of protein kinase PKR

Genes and Development

Volumn 20, Issue 1, 2006, Pages 87-100

  Ventoso, Iván ^a   Sanz, Miguel Angel ^b   Molina, Susana ^b   Berlanga, Juan José ^b   Carrasco, Luis ^b   Esteban, Mariano ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Alphaviruses; Antiviral response; eIF2; eIF2A; PKR; Translation

Indexed keywords

INITIATION FACTOR 2ALPHA; PROTEIN KINASE R; VIRUS MESSENGER RNA;

ALPHA VIRUS; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CHEMICAL ANALYSIS; CODON; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GENETIC ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RIBOSOME; RNA TRANSLATION; SEMLIKI FOREST ALPHAVIRUS; SINDBIS VIRUS; TRANSLATION INITIATION; TRANSLATION REGULATION; VIRUS REPLICATION;

ALPHAVIRUS INFECTIONS; ANIMALS; CELLS, CULTURED; CODON, INITIATOR; EIF-2 KINASE; ENZYME INDUCTION; EUKARYOTIC INITIATION FACTOR-2; FIBROBLASTS; GENE SILENCING; MICE; MICE, KNOCKOUT; NUCLEIC ACID CONFORMATION; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, VIRAL; SEMLIKI FOREST VIRUS; SINDBIS VIRUS; VIRUS REPLICATION;

ALPHAVIRUS; ANIMALIA; EUKARYOTA; MAMMALIA; RNA VIRUSES; SEMLIKI FOREST VIRUS; SINDBIS VIRUS;

EID: 29944433224     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.357006     Document Type: Article

References (59)

1. Adams, S.L., Safer, B., Anderson, W.F., and Merrick, W.C. 1975. Eukaryotic initiation complex formation. Evidence for two distinct pathways. J. Biol. Chem. 250: 9083-9089.
2. Anthony, D.D. and Merrick, W.C. 1992. Analysis of 40 S and 80 S complexes with mRNA as measured by sucrose density gradients and primer extension inhibition. J. Biol. Chem. 267: 1554-1562.
3. Balachandran, S. and Barber, G.N. 2004. Defective translational control facilitates vesicular stomatitis virus oncolysis. Cancer Cell 5: 51-65.
4. Balachandran, S., Roberts, P.C., Brown, L.E., Truong, H., Pattnaik, A.K., Archer, D.R., and Barber, G.N. 2000. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13: 129-141.
5. Bergmann, M., Garcia-Sastre, A., Carnero, E., Pehamberger, H., Wolff, K., Palese, P., and Muster, T. 2000. Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J. Virol. 74: 6203-6206.
6. Bischoff, J.R. and Samuel, C.E. 1989. Mechanism of interferon action. Activation of the human P1/eIF-2 α protein kinase by individual reovirus s-class mRNAs: s1 mRNA is a potent activator relative to s4 mRNA. Virology 172: 106-115.
7. Black, T.L., Barber, G.N., and Katze, M.G. 1993. Degradation of the interferon-induced 68,000-M(r) protein kinase by poliovirus requires RNA. J. Virol. 67: 791-800.
8. Carroll, K., Elroy-Stein, O., Moss, B., and Jagus, R. 1993. Recombinant vaccinia virus K3L gene product prevents activation of double-stranded RNA-dependent, initiation factor 2 α-specific protein kinase. J. Biol. Chem. 268: 12837-12842.
9. Davies, M.V., Chang, H.W., Jacobs, B.L., and Kaufman, R.J. 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.
10. de Haro, C., Mendez, R., and Santoyo, J. 1996. The eIF-2α kinases and the control of protein synthesis. FASEB J. 10: 1378-1387.
11. Dever, T.E. 2002. Gene-specific regulation by general translation factors. Cell 108: 545-556.
12. Frolov, I. and Schlesinger, S. 1994a. Comparison of the effects of Sindbis virus and Sindbis virus replicons on host cell protein synthesis and cytopathogenicity in BHK cells. J. Virol. 68: 1721-1727.
13. -. 1994b. Translation of Sindbis virus mRNA: Effects of sequences downstream of the initiating codon. J. Virol. 68: 8111-8117.
14. -. 1996. Translation of Sindbis virus mRNA: Analysis of sequences downstream of the initiating AUG codon that enhance translation. J. Virol. 70: 1182-1190.
15. Gale Jr., M., Blakely, C.M., Kwieciszewski, B., Tan, S.L., Dossett, M., Tang, N.M., Korth, M.J., Polyak, S.J., Gretch, D.R., and Katze, M.G. 1998. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: Molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18: 5208-5218.
16. Gingras, A.C., Raught, B., and Sonenberg, N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68: 913-963.
17. Goossens, A., Dever, T.E., Pascual-Ahuir, A., and Serrano, R. 2001. The protein kinase Gcn2p mediates sodium toxicity in yeast. J. Biol. Chem. 276: 30753-30760.
18. Gorchakov, R., Frolova, E., Williams, B.R., Rice, C.M., and Frolov, I. 2004. PKR-dependent and -independent mechanisms are involved in translational shutoff during Sindbis virus infection. J. Virol. 78: 8455-8467.
19. Gunnery, S. and Mathews, M.B. 1998. RNA binding and modulation of PKR activity. Methods 15: 189-198.
20. Harding, H.P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M., and Ron, D. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6: 1099-1108.
21. He, B., Gross, M., and Roizman, B. 1997. The γ(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1α to dephosphorylate the α subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. 94: 843-848.
22. Hershey, J.W. 1991. Translational control in mammalian cells. Annu. Rev. Biochem. 60: 717-755.
23. Kaufman, R.J. 1999. Double-stranded RNA-activated protein kinase mediates virus-induced apoptosis: A new role for an old actor. Proc. Natl. Acad. Sci. 96: 11693-11695.
24. Kimball, S.R. 1999. Eukaryotic initiation factor eIF2. Int. J. Biochem. Cell Biol. 31: 25-29.
25. Kimball, S.R., Fabian, J.R., Pavitt, G.D., Hinnebusch, A.G., and Jefferson, L.S. 1998. Regulation of guanine nucleotide exchange through phosphorylation of eukaryotic initiation factor eIF2α. Role of the α- and δ-subunits of eiF2b. J. Biol. Chem. 273: 12841-12845.
26. Kitajewski, J., Schneider, R.J., Safer, B., Munemitsu, S.M., Samuel, C.E., Thimmappaya, B., and Shenk, T. 1986. Adenovirus VAI RNA antagonizes the antiviral action of interferon by preventing activation of the interferon-induced eIF-2 α kinase. Cell 45: 195-200.
27. Komar, A.A., Gross, S.R., Barth-Baus, D., Strachan, R., Hensold, J.O., Goss Kinzy, T., and Merrick, W.C. 2005. Novel characteristics of the biological properties of the yeast Saccharomyces cerevisiae eukaryotic initiation factor 2A. J. Biol. Chem. 280: 15601-15611.
28. Kozak, M. 1980. Evaluation of the 'scanning model' for initiation of protein synthesis in eucaryotes. Cell 22 (1 Pt 1): 7-8.
29. -. 1990. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc. Natl. Acad. Sci. 87: 8301-8305.
30. -. 1998. Primer extension analysis of eukaryotic ribosome-mRNA complexes. Nucleic Acids Res. 26: 4853-4859.
31. Krishnamoorthy, T., Pavitt, G.D., Zhang, F., Dever, T.E., and Hinnebusch, A.G. 2001. Tight binding of the phosphorylated α subunit of initiation factor 2 (eIF2α) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol. Cell. Biol. 21: 5018-5030.
32. Levis, R., Schlesinger, S., and Huang, H.V. 1990. Promoter for Sindbis virus RNA-dependent subgenomic RNA transcription. J. Virol. 64: 1726-1733.
33. Lu, Y., Wambach, M., Katze, M.G., and Krug, R.M. 1995. Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214: 222-228.
34. Manche, L., Green, S.R., Schmedt, C., and Mathews, M.B. 1992. Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol. Cell. Biol. 12: 5238-5248.
35. Maroto, B., Ramirez, J.C., and Almendral, J.M. 2000. Phosphorylation status of the parvovirus minute virus of mice particle: Mapping and biological relevance of the major phosphorylation sites. J. Virol. 74: 10892-10902.
36. Merrick, W.C. and Anderson, W.F. 1975. Purification and characterization of homogeneous protein synthesis initiation factor M1 from rabbit reticulocytes. J. Biol. Chem. 250: 1197-1206.
37. Meurs, E., Chong, K., Galabru, J., Thomas, N.S., Kerr, I.M., Williams, B.R., and Hovanessian, A.G. 1990. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62: 379-390.
38. Mueller, P.P. and Hinnebusch, A.G. 1986. Multiple upstream AUG codons mediate translational control of GCN4. Cell 45: 201-207.
39. Pestova, T.V. and Hellen, C.U. 2003. Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes & Dev. 17: 181-186.
40. Pestova, T.V., Borukhov, S.I., and Hellen, C.U. 1998. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394: 854-859.
41. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I., and Hellen, C.U. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. 98: 7029-7036.
42. Sanz, M.A., Madan, V., Carrasco, L., and Nieva, J.L. 2003. Interfacial domains in Sindbis virus 6K protein. Detection and functional characterization. J. Biol. Chem. 278: 2051-2057.
43. Savinova, O. and Jagus, R. 1997. Use of vertical slab isoelectric focusing and immunoblotting to evaluate steady-state phosphorylation of eIF2 α in cultured cells. Methods 11: 419-425.
44. Stark, G.R., Kerr, I.M., Williams, B.R., Silverman, R.H., and Schreiber, R.D. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227-264.
45. Stojdl, D.F., Abraham, N., Knowles, S., Marius, R., Brasey, A., Lichty, B.D., Brown, E.G., Sonenberg, N., and Bell, J.C. 2000. The murine double-stranded RNA-dependent protein kinase PKR is required for resistance to vesicular stomatitis virus. J. Virol. 74: 9580-9585.
46. Strauss, J.H. and Strauss, E.G. 1994. The alphaviruses: Gene expression, replication, and evolution. Microbiol. Rev. 58: 491-562.
47. Sudhakar, A., Ramachandran, A., Ghosh, S., Hasnain, S.E., Kaufman, R.J., and Ramaiah, K.V. 2000. Phosphorylation of serine 51 in initiation factor 2 α (eIF2 α) promotes complex formation between eIF2 α(P) and eIF2B and causes inhibition in the guanine nucleotide exchange activity of eIF2B. Biochemistry 39: 12929-12938.
48. Suzuki, H. and Goldberg, I.H. 1974. Reversal of pactamycin inhibition of methionyl-puromycin synthesis and 80S initiation complex formation by a ribosomal joining factor. Proc. Natl. Acad. Sci. 71: 4259-4263.
49. Taylor, D.R., Shi, S.T., Romano, P.R., Barber, G.N., and Lai, M.M. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285: 107-110.
50. Vattem, K.M. and Wek, R.C. 2004. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. 101: 11269-11274.
51. Ventoso, I. and Carrasco, L. 1995. A poliovirus 2A(pro) mutant unable to cleave 3CD shows inefficient viral protein synthesis and transactivation defects. J. Virol. 69: 6280-6288.
52. Williams, B.R. 1999. PKR: A sentinel kinase for cellular stress. Oncogene 18: 6112-6120.
53. Wilson, J.E., Pestova, T.V., Hellen, C.U., and Sarnow, P. 2000. Initiation of protein synthesis from the A site of the ribosome. Cell 102: 511-520.
54. Xiang, Y., Condit, R.C., Vijaysri, S., Jacobs, B., Williams, B.R., and Silverman, R.H. 2002. Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J. Virol. 76: 5251-5259.
55. Yaman, I., Fernandez, J., Liu, H., Caprara, M., Komar, A.A., Koromilas, A.E., Zhou, L., Snider, M.D., Scheuner, D., Kaufman, R.J., et al. 2003. The zipper model of translational control: A small upstream ORF is the switch that controls structural remodeling of an mRNA leader. Cell 113: 519-531.
56. Yang, W. and Hinnebusch, A.G. 1996. Identification of a regulatory subcomplex in the guanine nucleotide exchange factor eIF2B that mediates inhibition by phosphorylated eIF2. Mol. Cell. Biol. 16: 6603-6616.
57. Yang, Y.L., Reis, L.F., Pavlovic, J., Aguzzi, A., Schafer, R., Kumar, A., Williams, B.R., Aguet, M., and Weissmann, C. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14: 6095-6106.
58. Yue, Z. and Shatkin, A.J. 1997. Double-stranded RNA-dependent protein kinase (PKR) is regulated by reovirus structural proteins. Virology 234: 364-371.
59. Zoll, W.L., Horton, L.E., Komar, A.A., Hensold, J.O., and Merrick, W.C. 2002. Characterization of mammalian eIF2A and identification of the yeast homolog. J. Biol. Chem. 277: 37079-37087.