Recognition of mRNA cap structures by viral and cellular proteins

Journal of General Virology

Volumn 86, Issue 5, 2005, Pages 1239-1249

  Fechter, Pierre ^a   Brownlee, George G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

7 METHYLGUANINE; AROMATIC AMINO ACID; CAP BINDING PROTEIN; CAPPED RNA; CELL PROTEIN; INITIATION FACTOR 4E; MESSENGER RNA; PHOSPHODIESTERASE I; RNA POLYMERASE; VIRUS PROTEIN; VIRUS RNA;

CELL NUCLEUS; COMPARATIVE STUDY; COMPLEX FORMATION; CONVERGENT EVOLUTION; CYTOPLASM; DATA ANALYSIS; EUKARYOTE; INFLUENZA VIRUS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN FUNCTION; PROTEIN MOTIF; REGULATORY MECHANISM; REVIEW; RNA BINDING; RNA DEGRADATION; RNA STRUCTURE; RNA TRANSLATION; RNA TRANSPORT; STRUCTURE ANALYSIS; VACCINIA VIRUS;

PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEINS; RNA CAP-BINDING PROTEINS; RNA CAPS; RNA, MESSENGER; VIRAL PROTEINS;

EUKARYOTA; INFLUENZA VIRUS; VACCINIA; VACCINIA VIRUS;

EID: 18144398494     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80755-0     Document Type: Review

References (87)

1. Blaas, D., Patzelt, E. & Kuechler, E. (1982). Identification of the cap binding protein of influenza virus. Nucleic Acids Res 10, 4803-4812.
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.
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.
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.
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.
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.
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.
8. 7GpppG binding to the nuclear cap-binding protein complex. Nat Struct Biol 9, 912-917.
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.
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.
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.
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.
13. Cianci, C., Tiley, L. & Krystal, M. (1995). Differential activation of the influenza virus polymerase via template RNA-binding. J Virol 69, 3995-3999.
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.
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.
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.
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.
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.
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.
21. Flick R., Neumann, G., Hoffmann, E., Neumeier, E. & Hobom, G. (1996). Promoter elements in the influenza vRNA terminal structure. RNA 2, 1046-1057.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
35. Hu, G., Oguro, A., Li, C., Gershon, P. D. & Ouiocho, 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.
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.
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.
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.
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.
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.
41. Kimball, S. R. (2001). Regulation of translation initiation by amino acids in eukaryotic cells. Prog Mol Subcell Biol 26, 155-184.
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.
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.
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.
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.
47. Lewis, J. D. & Izaurralde, E. (1997). The role of cap structure in RNA processing and nuclear export. Eur J Biochem 247, 461-469.
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.
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.
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.
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.
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.
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.
54. 7GDP and interaction with 4E-binding protein. Nat Struct Biol 4, 717-724.
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.
56. 7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J 21, 5548-5557.
57. McKendrick, L., Pain, V. M. & Morley, S. J. (1999). Translation initiation factor 4E. Int J Biochem Cell Biol 31, 31-35.
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.
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.
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.
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.
63. Portela, A., Zurcher, T., Nieto, A. & Ortín, J. (1999). Replication of orthomyxoviruses. Adv Virus Res 54, 319-348.
64. Proud, C. G. (2002). Regulation of mammalian translation factors by nutrients. Eur J Biochem 269, 5338-5349.
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.
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.
67. Raught, B. & Gingras, A. C. (1999). eIF4E activity is regulated at multiple levels. Int J Biochem Cell Biol 31, 43-57.
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.
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.
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.
71. 2 is the endonuclease which cleaves host cell messenger RNA and functions only as the trimeric enzyme. Virology 208, 38-47.
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.
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.
74. Smith, G. L., Vanderplasschen, A. & Law, M. (2002). The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83, 2915-2931.
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.
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.
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.
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.
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.
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.
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.
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.
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.
84. Wilson, F. K. & Cerione, R. A. (2000). Signal transduction and posttranscriptional gene expression. Biol Chem 381, 357-365.
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.
86. Wu, X. & Guarino, L. A. (2003). Autographica californica nucleopolyhedrovirus orf69 encodes an RNA cap (nucleoside-2′-O)methyltransferase. J Virol 77, 3430-3440.
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.