1887

Abstract

Most cellular and eukaryotic viral mRNAs have a cap structure at their 5′ end that is critical for efficient translation. Cap structures also aid in mRNA transport from nucleus to cytoplasm and, in addition, protect the mRNAs from degradation by 5′ exonucleases. Cap function is mediated by cap-binding proteins that play a key role in translational control. Recent structural studies on the cellular cap-binding complex, the eukaryotic translation initiation factor 4E and the vaccinia virus protein 39, suggest that these three evolutionary unrelated cap-binding proteins have evolved a common cap-binding pocket by convergent evolution. In this pocket the positively charged N-methylated guanine ring of the cap structure is stacked between two aromatic amino acids. In this review, the similarities and differences in cap binding by these three different cap-binding proteins are discussed. A comparison with new functional data for another viral cap-binding protein – the polymerase basic protein (PB2) of influenza virus – suggests that a similar cap-binding mechanism has also evolved in influenza virus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80755-0
2005-05-01
2020-01-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/5/vir861239.html?itemId=/content/journal/jgv/10.1099/vir.0.80755-0&mimeType=html&fmt=ahah

References

  1. Blaas, D., Patzelt, E. & Kuechler, E. ( 1982; ). Identification of the cap binding protein of influenza virus. Nucleic Acids Res 10, 4803–4812.[CrossRef]
    [Google Scholar]
  2. Blachut-Okrasinska, E., Bojarska, E., Niedzwiecka, A., Chlebicka, L., Darzynkiewicz, E., Stolarski, R., Stepinski, J. & Antosiewicz, J. M. ( 2000; ). Stopped-flow and Brownian dynamics studies of electrostatic effects in the kinetics of binding of 7-methyl-GpppG to the protein eIF4E. Eur Biophys J 29, 487–498.[CrossRef]
    [Google Scholar]
  3. Borman, A. M., Michel, Y. M. & Kean, K. M. ( 2000; ). Biochemical characterisation of cap-poly(A) synergy in rabbit reticulocyte lysates: the eIF4G-PABP interaction increases the functional affinity of eIF4E for the capped mRNA 5′-end. Nucleic Acids Res 28, 4068–4075.[CrossRef]
    [Google Scholar]
  4. Bouloy, M., Morgan, M. A., Shatkin, A. J. & Krug, R. M. ( 1979; ). Cap and internal nucleotides of reovirus mRNA primers are incorporated into influenza viral complementary RNA during transcription in vitro. J Virol 32, 895–904.
    [Google Scholar]
  5. Bouloy, M., Plotch, S. J. & Krug, R. M. ( 1980; ). Both the 7-methyl and the 2′-O-methyl groups in the cap of mRNA strongly influence its ability to act as primer for influenza virus RNA transcription. Proc Natl Acad Sci U S A 77, 3952–3956.[CrossRef]
    [Google Scholar]
  6. Brownlee, G. G., Fodor, E., Pritlove, D. C., Gould, K. G. & Dalluge, J. J. ( 1995; ). Solid phase synthesis of 5′-diphosphorylated oligoribonucleotides and their conversion to capped m7Gppp-oligoribonucleotides for use as primers for influenza A virus RNA polymerase in vitro. Nucleic Acids Res 23, 2641–2647.[CrossRef]
    [Google Scholar]
  7. Cai, A., Jankowska-Anyszka, M., Centers, A., Chlebicka, L., Stepinski, J., Stolarski, R., Darzynkiewicz, E. & Rhoads, R. E. ( 1999; ). Quantitative assessment of mRNA cap analogues as inhibitors of in vitro translation. Biochemistry 38, 8538–8547.[CrossRef]
    [Google Scholar]
  8. Calero, G., Wilson, K. F., Ly, T., Rios-Steiner, J. L., Clardy, J. C. & Cerione, R. A. ( 2002; ). Structural basis of m7GpppG binding to the nuclear cap-binding protein complex. Nat Struct Biol 9, 912–917.[CrossRef]
    [Google Scholar]
  9. Carberry, S. E., Rhoads, R. E. & Goss, D. J. ( 1989; ). A spectroscopic study of the binding of m7GTP and m7GpppG to human protein synthesis initiation factor 4E. Biochemistry 28, 8078–8083.[CrossRef]
    [Google Scholar]
  10. Carberry, S. E., Darzynkiewicz, E., Stepinski, J., Tahara, S. M., Rhoads, R. E. & Goss, D. J. ( 1990; ). A spectroscopic study of the binding of N-7-substituted cap analogues to human protein synthesis initiation factor 4E. Biochemistry 29, 3337–3341.[CrossRef]
    [Google Scholar]
  11. Carberry, S. E., Darzynkiewicz, E. & Goss, D. J. ( 1991; ). A comparison of the binding of methylated cap analogues to wheat germ protein synthesis initiation factors 4F and (iso)4F. Biochemistry 30, 1624–1627.[CrossRef]
    [Google Scholar]
  12. Chung, T. D., Cianci, C., Hagen, M., Terry, B., Matthews, J. T., Krystal, M. & Colonno, R. J. ( 1994; ). Biochemical studies on capped RNA primers identify a class of oligonucleotide inhibitors of the influenza virus RNA polymerase. Proc Natl Acad Sci U S A 91, 2372–2376.[CrossRef]
    [Google Scholar]
  13. Cianci, C., Tiley, L. & Krystal, M. ( 1995; ). Differential activation of the influenza virus polymerase via template RNA-binding. J Virol 69, 3995–3999.
    [Google Scholar]
  14. Clemens, M. J. ( 2001; ). Translational regulation in cell stress and apoptosis. Roles of the eIF4E binding proteins. J Cell Mol Med 5, 221–239.[CrossRef]
    [Google Scholar]
  15. Coffin, J. M. ( 1990; ). Retroviridae and their replication. In Fields Virology, pp. 1437–1500. Edited by P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  16. Condit, R. C. & Niles, E. G. ( 2002; ). Regulation of viral transcription elongation and termination during vaccinia virus infection. Biochim Biophys Acta 1577, 325–336.[CrossRef]
    [Google Scholar]
  17. Darzynkiewicz, E. & Lonnberg, H. ( 1989; ). Base stacking of simple mRNA cap analogues. Association of 7,9-dimethylguanine, 7-methylguanosine and 7-methylguanosine 5′-monophosphate with indole and purine derivatives in aqueous solution. Biophys Chem 33, 289–293.[CrossRef]
    [Google Scholar]
  18. Dostie, J., Ferraiuolo, M., Pause, A., Adam, S. A. & Sonenberg, N. ( 2000; ). A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5′ cap-binding protein, eIF4E. EMBO J 19, 3142–3156.[CrossRef]
    [Google Scholar]
  19. Egloff, M. P., Benarroch, D., Selisko, B., Romette, J. L. & Canard, B. ( 2002; ). An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J 21, 2757–2768.[CrossRef]
    [Google Scholar]
  20. Fechter, P., Mingay, L., Sharps, J., Chambers, A., Fodor, E. & Brownlee, G. G. ( 2003; ). Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. J Biol Chem 278, 20381–20388.[CrossRef]
    [Google Scholar]
  21. Flick, R., Neumann, G., Hoffmann, E., Neumeier, E. & Hobom, G. ( 1996; ). Promoter elements in the influenza vRNA terminal structure. RNA 2, 1046–1057.
    [Google Scholar]
  22. Flynn, A. & Proud, C. G. ( 1995; ). Serine 209, not serine 53, is the major site of phosphorylation in initiation factor eIF-4E in serum-treated Chinese hamster ovary cells. J Biol Chem 270, 21684–21688.[CrossRef]
    [Google Scholar]
  23. Fodor, E. & Brownlee, G. G. ( 2002; ). Influenza virus replication. In Influenza, pp. 1–29. Edited by C. W. Potter. Oxford: Elsevier.
  24. Fodor, E., Crow, M., Mingay, L. J., Deng, T., Sharps, J. & Brownlee, G. G. ( 2002; ). A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J Virol 76, 8989–9001.[CrossRef]
    [Google Scholar]
  25. Gingras, A. C., Raught, B. & Sonenberg, N. ( 1999; ). eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68, 913–963.[CrossRef]
    [Google Scholar]
  26. Goss, D. J., Carberry, S. E., Dever, T. E., Merrick, W. C. & Rhoads, R. E. ( 1990; ). Fluorescence study of the binding of m7GpppG and rabbit globin mRNA to protein synthesis initiation factors 4A, 4E, and 4F. Biochemistry 29, 5008–5012.[CrossRef]
    [Google Scholar]
  27. Gross, J. D., Moerke, N. J., von der Haar, T., Lugovskoy, A. A., Sachs, A. B., McCarthy, J. E. & Wagner, G. ( 2003; ). Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115, 739–750.[CrossRef]
    [Google Scholar]
  28. Haghighat, A. & Sonenberg, N. ( 1997; ). eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J Biol Chem 272, 21677–21680.[CrossRef]
    [Google Scholar]
  29. Hodel, A. E., Gershon, P. D., Shi, X. N., Wang, S. M. & Quiocho, F. A. ( 1997; ). Specific protein recognition of an mRNA cap through its alkylated base. Nat Struct Biol 4, 350–354.[CrossRef]
    [Google Scholar]
  30. Hodel, A. E., Gershon, P. D. & Quiocho, F. A. ( 1998; ). Structural basis for sequence-nonspecific recognition of 5′-capped mRNA by a cap-modifying enzyme. Mol Cell 1, 443–447.[CrossRef]
    [Google Scholar]
  31. Honda, A., Mizumoto, K. & Ishihama, A. ( 1999; ). Two separate sequences of PB2 subunit constitute the RNA cap-binding site of influenza virus RNA polymerase. Genes Cells 4, 475–485.[CrossRef]
    [Google Scholar]
  32. Hooker, L., Sully, R., Handa, B., Ono, N., Koyano, H. & Klumpp, K. ( 2003; ). Quantitative analysis of influenza virus RNP interaction with RNA cap structures and comparison to human cap binding protein eIF4E. Biochemistry 42, 6234–6240.[CrossRef]
    [Google Scholar]
  33. Hsu, P. C., Hodel, M. R., Thomas, J. W., Taylor, L. J., Hagedorn, C. H. & Hodel, A. E. ( 2000; ). Structural requirements for the specific recognition of an m7G mRNA cap. Biochemistry 39, 13730–13736.[CrossRef]
    [Google Scholar]
  34. Hu, G., Gershon, P. D., Hodel, A. E. & Quiocho, F. A. ( 1999; ). mRNA cap recognition: dominant role of enhanced stacking interactions between methylated bases and protein aromatic side chains. Proc Natl Acad Sci U S A 96, 7149–7154.[CrossRef]
    [Google Scholar]
  35. Hu, G., Oguro, A., Li, C., Gershon, P. D. & Quiocho, F. A. ( 2002; ). The “cap-binding slot” of an mRNA cap-binding protein: quantitative effects of aromatic side chain choice in the double-stacking sandwich with cap. Biochemistry 41, 7677–7687.[CrossRef]
    [Google Scholar]
  36. Hu, G., Tsai, A. L. & Quiocho, F. A. ( 2003; ). Insertion of an N7-methylguanine mRNA cap between two coplanar aromatic residues of a cap-binding protein is fast and selective for a positively charged cap. J Biol Chem 278, 51515–51520.[CrossRef]
    [Google Scholar]
  37. Ishida, T. & Inoue, M. ( 1981; ). An X-ray evidence for the charge-transfer interaction between adenine and indole rings: crystal structure of 1,9-dimethyladenine-indole-3-acetic acid trihydrate complex. Biochem Biophys Res Commun 99, 149–154.[CrossRef]
    [Google Scholar]
  38. Ishida, T., Doi, M. & Inoue, M. ( 1988; ). A selective recognition mode of a nucleic acid base by an aromatic amino acid: l-phenylalanine-7-methylguanosine 5′-monophosphate stacking interaction. Nucleic Acids Res 16, 6175–6190.[CrossRef]
    [Google Scholar]
  39. Izaurralde, E., Stepinski, J., Darzynkiewicz, E. & Mattaj, I. W. ( 1992; ). A cap binding protein that may mediate nuclear export of RNA polymerase II-transcribed RNAs. J Cell Biol 118, 1287–1295.[CrossRef]
    [Google Scholar]
  40. Joshi, B., Cai, A. L., Keiper, B. D. & 7 other authors ( 1995; ). Phosphorylation of eukaryotic protein synthesis initiation factor 4E at Ser-209. J Biol Chem 270, 14597–14603.[CrossRef]
    [Google Scholar]
  41. Kimball, S. R. ( 2001; ). Regulation of translation initiation by amino acids in eukaryotic cells. Prog Mol Subcell Biol 26, 155–184.
    [Google Scholar]
  42. Kleijn, M., Scheper, G. C., Voorma, H. O. & Thomas, A. A. ( 1998; ). Regulation of translation initiation factors by signal transduction. Eur J Biochem 253, 531–544.[CrossRef]
    [Google Scholar]
  43. Lamb, R. A. & Krug, R. M. ( 2001; ). Orthomyxoviridae: the viruses and their replication. In Fields Virology, 4th edn, pp. 1487–1579. Edited by P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  44. Lawrence, J. C. Jr, Fadden, P., Haystead, T. A. & Lin, T. A. ( 1997; ). PHAS proteins as mediators of the actions of insulin, growth factors and cAMP on protein synthesis and cell proliferation. Adv Enzyme Regul 37, 239–267.[CrossRef]
    [Google Scholar]
  45. Le, H., Tanguay, R. L., Balasta, M. L., Wei, C. C., Browning, K. S., Metz, A. M., Goss, D. J. & Gallie, D. R. ( 1997; ). The translation initiation factors eIFiso-4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J Biol Chem 272, 16247–16255.[CrossRef]
    [Google Scholar]
  46. Leahy, M. B., Dobbyn, H. C. & Brownlee, G. G. ( 2001; ). Hairpin loop structure in the 3′ arm of the influenza A virus virion RNA promoter is required for endonuclease activity. J Virology 75, 7042–7049.[CrossRef]
    [Google Scholar]
  47. Lewis, J. D. & Izaurralde, E. ( 1997; ). The role of cap structure in RNA processing and nuclear export. Eur J Biochem 247, 461–469.[CrossRef]
    [Google Scholar]
  48. Li, M. L., Ramirez, B. C. & Krug, R. M. ( 1998; ). RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding sites. EMBO J 17, 5844–5852.[CrossRef]
    [Google Scholar]
  49. Li, M. L., Rao, P. & Krug, R. M. ( 2001; ). The active sites of the influenza cap-dependent endonuclease are on different polymerase subunits. EMBO J 20, 2078–2086.[CrossRef]
    [Google Scholar]
  50. Lin, T. A., Kong, X., Haystead, T. A., Pause, A., Belsham, G., Sonenberg, N. & Lawrence, J. C., Jr ( 1994; ). PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266, 653–656.[CrossRef]
    [Google Scholar]
  51. Lockless, S. W., Cheng, H. T., Hodel, A. E., Quiocho, F. A. & Gershon, P. D. ( 1998; ). Recognition of capped RNA substrates by VP39, the vaccinia virus-encoded mRNA cap-specific 2′-O-methyltransferase. Biochemistry 37, 8564–8574.[CrossRef]
    [Google Scholar]
  52. Marcotrigiano, J., Gingras, A. C., Sonenberg, N. & Burley, S. K. ( 1997; ). Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89, 951–961.[CrossRef]
    [Google Scholar]
  53. Marcotrigiano, J., Gingras, A. C., Sonenberg, N. & Burley, S. K. ( 1999; ). Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3, 707–716.[CrossRef]
    [Google Scholar]
  54. Matsuo, H., Li, H. J., McGuire, A. M., Fletcher, C. M., Gingras, A. C., Sonenberg, N. & Wagner, G. ( 1997; ). Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol 4, 717–724.[CrossRef]
    [Google Scholar]
  55. Mazza, C., Ohno, M., Segref, A., Mattaj, I. W. & Cusack, S. ( 2001; ). Crystal structure of the human nuclear cap binding complex. Mol Cell 8, 383–396.[CrossRef]
    [Google Scholar]
  56. Mazza, C., Segref, A., Mattaj, I. W. & Cusack, S. ( 2002; ). Large-scale induced fit recognition of an m7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J 21, 5548–5557.[CrossRef]
    [Google Scholar]
  57. McKendrick, L., Pain, V. M. & Morley, S. J. ( 1999; ). Translation initiation factor 4E. Int J Biochem Cell Biol 31, 31–35.[CrossRef]
    [Google Scholar]
  58. Morino, S., Hazama, H., Ozaki, M., Teraoka, Y., Shibata, S., Doi, M., Ueda, H., Ishida, T. & Uesugi, S. ( 1996; ). Analysis of the mRNA cap-binding ability of human eukaryotic initiation factor-4E by use of recombinant wild-type and mutant forms. Eur J Biochem 239, 597–601.[CrossRef]
    [Google Scholar]
  59. Moss, B. ( 2001; ). Poxviridae: the viruses and their replication. In Fields Virology, 4th edn, vol. 2, pp. 2849–2883. Edited by D. M Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  60. Niedzwiecka, A., Marcotrigiano, J., Stepinski, J. & 9 other authors ( 2002; ). Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J Mol Biol 319, 615–635.[CrossRef]
    [Google Scholar]
  61. Pause, A., Belsham, G. J., Gingras, A. C., Donze, O., Lin, T. A., Lawrence, J. C., Jr & Sonenberg, N. ( 1994; ). Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371, 762–767.[CrossRef]
    [Google Scholar]
  62. Plotch, S. J., Bouloy, M., Ulmanen, I. & Krug, R. M. ( 1981; ). A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23, 847–858.[CrossRef]
    [Google Scholar]
  63. Portela, A., Zurcher, T., Nieto, A. & Ortín, J. ( 1999; ). Replication of orthomyxoviruses. Adv Virus Res 54, 319–348.
    [Google Scholar]
  64. Proud, C. G. ( 2002; ). Regulation of mammalian translation factors by nutrients. Eur J Biochem 269, 5338–5349.[CrossRef]
    [Google Scholar]
  65. Ptushkina, M., von der Haar, T., Vasilescu, S., Frank, R., Birkenhager, R. & McCarthy, J. E. ( 1998; ). Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5′ cap in yeast involves a site partially shared by p20. EMBO J 17, 4798–4808.[CrossRef]
    [Google Scholar]
  66. Quiocho, F. A., Hu, G. & Gershon, P. D. ( 2000; ). Structural basis of mRNA cap recognition by proteins. Curr Opin Struct Biol 10, 78–86.[CrossRef]
    [Google Scholar]
  67. Raught, B. & Gingras, A. C. ( 1999; ). eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31, 43–57.[CrossRef]
    [Google Scholar]
  68. Rom, E., Kim, H. C., Gingras, A. C., Marcotrigiano, J., Favre, D., Olsen, H., Burley, S. K. & Sonenberg, N. ( 1998; ). Cloning and characterization of 4EHP, a novel mammalian eIF4E-related cap-binding protein. J Biol Chem 273, 13104–13109.[CrossRef]
    [Google Scholar]
  69. Scheper, G. C. & Proud, C. G. ( 2002; ). Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation? Eur J Biochem 269, 5350–5359.[CrossRef]
    [Google Scholar]
  70. Scheper, G. C., van Kollenburg, B., Hu, J., Luo, Y., Goss, D. J. & Proud, C. G. ( 2002; ). Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J Biol Chem 277, 3303–3309.[CrossRef]
    [Google Scholar]
  71. Shi, L. C., Summers, D. F., Peng, Q. H. & Galarza, J. M. ( 1995; ). Influenza-A virus-RNA polymerase subunit PB2 is the endonuclease which cleaves host cell messenger RNA and functions only as the trimeric enzyme. Virology 208, 38–47.[CrossRef]
    [Google Scholar]
  72. Shi, L., Galarza, J. M. & Summers, D. F. ( 1996; ). Recombinant-baculovirus-expressed PB2 subunit of the influenza A virus RNA polymerase binds cap groups as an isolated subunit. Virus Res 42, 1–9.[CrossRef]
    [Google Scholar]
  73. Shuman, S. & Lima, C. D. ( 2004; ). The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases. Curr Opin Struct Biol 14, 757–764.[CrossRef]
    [Google Scholar]
  74. Smith, G. L., Vanderplasschen, A. & Law, M. ( 2002; ). The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83, 2915–2931.
    [Google Scholar]
  75. Sonenberg, N. & Gingras, A. C. ( 1998; ). The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr Opin Cell Biol 10, 268–275.[CrossRef]
    [Google Scholar]
  76. Stolarski, R., Sitek, A., Stepinski, J., Jankowska, M., Oksman, P., Temeriusz, A., Darzynkiewicz, E., Lonnberg, H. & Shugar, D. ( 1996; ). 1H-NMR studies on association of mRNA cap-analogues with tryptophan-containing peptides. Biochim Biophys Acta 1293, 97–105.[CrossRef]
    [Google Scholar]
  77. Tomoo, K., Shen, X., Okabe, K. & 9 other authors ( 2003; ). Structural features of human initiation factor 4E, studied by X-ray crystal analyses and molecular dynamics simulations. J Mol Biol 328, 365–383.[CrossRef]
    [Google Scholar]
  78. Ueda, H., Iyo, H., Doi, M., Inoue, M. & Ishida, T. ( 1991; ). Cooperative stacking and hydrogen bond pairing interactions of fragment peptide in cap binding protein with mRNA cap structure. Biochim Biophys Acta 1075, 181–186.[CrossRef]
    [Google Scholar]
  79. Ulmanen, I., Broni, B. A. & Krug, R. M. ( 1981; ). Role of two of the influenza virus core P proteins in recognizing cap 1 structures (m7GpppNm) on RNAs and in initiating viral RNA transcription. Proc Natl Acad Sci U S A 78, 7355–7359.[CrossRef]
    [Google Scholar]
  80. von der Haar, T., Ball, P. D. & McCarthy, J. E. ( 2000; ). Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5′-cap by domains of eIF4G. J Biol Chem 275, 30551–30555.[CrossRef]
    [Google Scholar]
  81. von der Haar, T., Gross, J. D., Wagner, G. & McCarthy, J. E. ( 2004; ). The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat Struct Mol Biol 11, 503–511.[CrossRef]
    [Google Scholar]
  82. Vreede, F. T., Jung, T. E. & Brownlee, G. G. ( 2004; ). Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J Virol 78, 9568–9572.[CrossRef]
    [Google Scholar]
  83. Wei, C. C., Balasta, M. L., Ren, J. & Goss, D. J. ( 1998; ). Wheat germ poly(A) binding protein enhances the binding affinity of eukaryotic initiation factor 4F and (iso)4F for cap analogues. Biochemistry 37, 1910–1916.[CrossRef]
    [Google Scholar]
  84. Wilson, F. K. & Cerione, R. A. ( 2000; ). Signal transduction and post-transcriptional gene expression. Biol Chem 381, 357–365.
    [Google Scholar]
  85. Wilson, K. F., Fortes, P., Singh, U. S., Ohno, M., Mattaj, I. W. & Cerione, R. A. ( 1999; ). The nuclear cap-binding complex is a novel target of growth factor receptor-coupled signal transduction. J Biol Chem 274, 4166–4173.[CrossRef]
    [Google Scholar]
  86. Wu, X. & Guarino, L. A. ( 2003; ). Autographica californica nucleopolyhedrovirus orf69 encodes an RNA cap (nucleoside-2′-O)methyltransferase. J Virol 77, 3430–3440.[CrossRef]
    [Google Scholar]
  87. Zuberek, J., Wyslouch-Cieszynska, A., Niedzwiecka, A. & 9 other authors ( 2003; ). Phosphorylation of eIF4E attenuates its interaction with mRNA 5′ cap analogs by electrostatic repulsion: intein-mediated protein ligation strategy to obtain phosphorylated protein. RNA 9, 52–61.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80755-0
Loading
/content/journal/jgv/10.1099/vir.0.80755-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error