Functional dissection of eukaryotic initiation factor 4F: The 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes

Molecular and Cellular Biology

Volumn 16, Issue 12, 1996, Pages 6870-6878

  Pestova, Tatyana V ^a,b   Shatsky, Ivan N ^b   Hellen, Christopher U T ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INITIATION FACTOR; MESSENGER RNA; TRANSFER RNA; VIRUS RNA;

ARTICLE; BINDING SITE; ENCEPHALOMYOCARDITIS VIRUS; EUKARYOTE; NONHUMAN; PICORNAVIRUS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; RIBOSOME; RNA BINDING; TRANSLATION INITIATION; VIRUS INFECTION;

ENCEPHALOMYOCARDITIS VIRUS; EUKARYOTA; PICORNAVIRIDAE;

EID: 0029968997     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.12.6870     Document Type: Article

References (54)

1. Abramson, R. D., T. E. Dever, T. G. Lawson, B. K. Ray, R. E. Thach, and W. C. Merrick. 1987. The ATP-dependent interaction of eukaryotic initiation factors with mRNA. J. Biol. Chem. 262:3826-3832.
2. Allen, M. L., A. M. Metz, R. T. Timmer, R. E. Rhoads, and K. S. Browning. 1992. Isolation and sequence of the cDNAs encoding the subunits of the isozyme form of wheat protein synthesis initiation factor 4F. J. Biol. Chem. 267:23232-23236.
3. Anthony, D. D., and W. C. Merrick. 1992. Analysis of 40S and 80S complexes with mRNA as measured by sucrose density gradients and primer extension inhibition. J. Biol. Chem. 267:1554-1562.
4. Birney, E., S. Kumar, and A. R. Krainer. 1993. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21:5803-5816.
5. Bu, X., D. W. Haas, and C. H. Hagedorn. 1993. Novel phosphorylation sites of eukaryotic initiation factor 4F and evidence that phosphorylation stabilizes interactions of the p25 and p220 subunits. J. Biol. Chem. 268:4975-4978.
6. Duke, G. M., M. A. Hoffman, and A. C. Palmenberg. 1992. Sequence and structural elements that contribute to efficient encephalomyocarditis virus RNA translation. J. Virol. 66:1602-1609.
7. Etchison, D., S. C. Milburn, I. Edery, N. Sonenberg, and J. W. B. Hershey. 1982. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000 dalton polypeptide associated with eukaryotic initiation factor 3 and a cap-binding complex. J. Biol. Chem. 257:14806-14810.
8. Evstafieva, A. G., T. Y. Ugarova, B. K. Chernov, and I. N. Shalsky. 1991. A complex RNA sequence determines the internal initiation of encephalomyocarditis virus RNA translation. Nucleic Acids Res. 19:665-671.
9. Flynn, A., I. N. Shatsky, C. G. Proud, and A. Kaminski. 1994. The RNA-binding properties of protein synthesis initiation factor eIF-2. Biochim. Biophys. Acta 1219:293-301.
10. Goyer, C., M. Altmann, H. S. Lee, A. Blanc, M. Deshmukh, J. L. Woolford, H. Trachsel, and N. Sonenberg. 1993. TIF4631 and TIF4632: two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA-recognition motif-like sequence and carry out an essential function. Mol. Cell. Biol. 13:4860-4874.
11. Grifo, J. A., S. M. Tahara, M. A. Morgan, A. J. Shatkin, and W. C. Merrick. 1983. New initiation factor required for globin mRNA translation. J. Biol. Chem. 258:5804-5810.
12. Haghighat, A., S. Mader, A. Pause, and N. Sonenberg. 1995. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J. 14:5701-5709.
13. Hellen, C. U. T., and E. Wimmer, 1995. Translation of encephalomyocarditis virus RNA by internal ribosomal entry. Curr. Top. Microbiol. Immunol. 203: 31-64.
14. Hellen, C. U. T., G. W. Witherell, M. Schmidt, S. Shine, T. V. Pestova, A. Gil, and E. Wimmer. 1993. A cytoplasmic 57kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc. Natl. Acad. Sci. USA 90:7642-7646.
15. Hochüli, E., H. Döbeli, and A. Schachner. 1987. New chelate adsorbant selective for proteins and peptides containing neighbouring histidine residues. J. Chromatogr. 411:177-184.
16. Hughes, D. L., T. E. Dever, and W. C. Merrick. 1993. Further biochemical characterization of rabbit reticulocyte eIF-4B. Arch. Biochem. Biophys. 301: 311-319.
17. Jackson, R. J. 1996. A comparative view of initiation site selection mechanisms, p. 71-112. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
18. Jang, S. K., M. V. Davies, R. J. Kaufman, and E. Wimmer. 1989. Initiation of protein synthesis by internal entry of ribosomes into the 5′ nontranslated region of encephalomyocarditis virus RNA in vivo. J. Virol. 63:1651-1660.
19. Jang, S.-K., H.-G. Kräusslich, M. J. H. Nicklin, G. M. Duke, A. C. Palmenberg, and E. Wimmer. 1988. A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:2636-2643.
20. Jaramillo, M., T. E. Dever, W. C. Merrick, and N. Sonenberg. 1991. RNA unwinding in translation: assembly of helicase complex intermediates comprising eukaryotic initiation factors eIF-4F and eIF-4B. Mol. Cell. Biol. 11:5992-5997.
21. Jen, G., B. M. Detjen, and R. E. Thach. 1980. Shutoff of HeLa cell protein synthesis by encephalomyocarditis virus and poliovirus: a comparative study. J. Virol. 35:150-156.
22. Jen, G., and R. E. Thach. 1982. Inhibition of host translation in encephalomyocarditis virus-infected L cells: a novel mechanism. J. Virol. 43:250-261.
23. Joshi, B., R. Yan, and R. E. Rhoads. 1994. In vitro synthesis of human protein synthesis initiation factor 4γ and its localization on 43S and 48S initiation complexes. J. Biol. Chem. 269:2048-2055.
24. Kaminski, A., G. J. Belsham, and R. J. Jackson. 1994. Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site. EMBO J. 13:1673-1681.
25. Kaminski, A., M. T. Howell, and R. J. Jackson. 1990. Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism. EMBO J. 9:3753-3759.
26. Koonin, E. V. 1995. Multidomain organization of eukaryotic guanine nucleotide exchange translation initiation factor eIF-2B subunits revealed by analysis of conserved sequence motifs. Protein Sci. 4:1608-1617.
27. Lamphear, B. J., R. Kirchenweger, T. Skern, and R. E. Rhoads. 1995. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270:21975-21983.
28. Lamphear, B. J., R. Yan, F. Yang, D. Waters, H.-D. Liebig, H. Klump, E. Kuechler, T. Skern, and R. E. Rhoads. 1993. Mapping the cleavage site in protein synthesis initiation factor eIF-4γ of the 2A proteases from human coxsackievirus and rhinovirus. J. Biol. Chem. 268:19200-19203.
29. Lawson, T. G., K. A. Lee, M. M. Maimone, R. D. Abramson, T. E. Dever, W. C. Merrick, and R. E. Thach. 1989. Dissociation of double-stranded polynucleotide helical structures by eukaryotic initiation factors, as revealed by a novel assay. Biochemistry 28:4729-4734.
30. Lyakhov, D. L., H. Ilgenfritz, B. K. Chernov, S. M. Dragan, V. O. Rechinsky, D. K. Pokholok, V. L. Tunitskaya, and S. N. Kochetkov. 1992. Site-specific mutagenesis of the Lys-172 residue in phage T7 RNA polymerase: characterization of the transcriptional properties of mutant proteins. Mol. Biol. 26:679-687.
31. Mader, S., H. Lee, A. Pause, and N. Sonenberg. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4γ and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15:4990-4997.
32. Merrick, W. C. 1992. Mechanism and regulation of eukaryotic protein synthesis. Microbiol. Rev. 56:291-315.
33. Méthot, N., A. Pause, J. W. B. Hershey, and N. Sonenberg. 1994. The translation factor eIF-4B contains an RNA-binding region that is distinct and independent from its ribonucleoprotein consensus sequence. Mol. Cell. Biol. 14:2307-2316.
34. Méthot, N., G. Pickett, J. D. Keene, and N. Sonenberg. 1996. In vitro RNA selection identifies RNA ligands that specifically bind to eukaryotic translation initiation factor 4B: the role of the RNA recognition motif. RNA 2:38-50.
35. Meyer, K., A. Petersen, M. Niepmann, and E. Beck. 1995. Interaction of eukaryotic initiation factor 4B with a picornaviral internal translation initiation site. J. Virol. 69:2819-2824.
36. Milburn, S. C., J. W. B. Hershey, M. V. Davies, K. Kelleher, and R. J. Kaufman. 1990. Cloning and expression of eukaryotic initiation factor 4B cDNA: sequence determination identifies a common RNA recognition motif. EMBO J. 9:2783-2790.
37. Minich, W. B., M. L. Balasta, D. J. Goss, and R. E. Rhoads. 1994. Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation factor eIF-4E: increased cap affinity of the phosphorylated form. Proc. Natl. Acad. Sci. USA 91:7668-7672.
38. Naranda, T., W. B. Strong, J. Menaya, B. J. Fabbri, and J. W. B. Hershey. 1994. Two structural domains of initiation factor eIF-4B are involved in binding to RNA. J. Biol. Chem. 269:14465-14472.
39. Ohlmann, T., M. Rau, V. M. Pain, and S. J. Morley. 1996. The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J. 15:1371-1382.
40. Pause, A., G. J. Belsham, A.-C. Gingras, O. Donzé, T. A. Lin, J. C. Lawrence, and N. Sonenberg. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature (London) 371: 762-767.
41. Pause, A., N. Méthot, and N. Sonenberg. 1993. The HRIGRR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol. Cell. Biol. 13:6789-6798.
42. Pause, A., N. Méthot, Y. Svitkin, W. C. Merrick, and N. Sonenberg. 1994. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J. 13:1205-1215.
43. Pelletier, J., and N. Sonenberg. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence from poliovirus RNA. Nature (London) 334:320-325.
44. Pestova, T. V., C. U. T. Hellen, and E. Wimmer. 1991. Translation of polio-virus RNA: role of an essential cis-acting oligopyrimidine element within the 5′-nontranslated region and involvement of a cellular 57-kilodalton protein. J. Virol. 65:6194-6204.
45. Pestova, T. V., C. U. T. Hellen, and I. N. Shatsky. 1996. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol. 16:6859-6869.
46. Pilipenko, E. V., V. M. Blinov, B. K. Chernov, T. M. Dmitrieva, and V. I. Agol. 1989. Conservation of the secondary structure elements of the 5′-untranslated region of cardio- and aphthovirus RNAs. Nucleic Acids Res. 17:5701-5711.
47. Ray, B. K., T. G. Lawson, J. C. Kramer, M. H. Cladaras, J. A. Grifo, A. D. Abramson, W. C. Merrick, and R. E. Thach. 1985. ATP-dependent unwinding of messenger RNA structure by eukaryotic initiation factors. J. Biol. Chem. 260:7651-7658.
48. Rhoads, R. E. 1991. Initiation: mRNA and 60S subunit binding, p. 109-148. In H. Trachsel (ed.), Translation in eukaryotes. CRC Press, Boca Raton, Fla.
49. Rozen, F., I. Edery, K. Meerovitch, T. E. Dever, W. C. Merrick, and N. Sonenberg. 1990. Bidirectional RNA helicase activity of eukaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 10:1134-1144.
50. Staehelin, T., H. Trachsel, B. Erni, A. Boschetti, and M. H. Schreier. 1975. The mechanism of initiation of mammalian protein synthesis, p. 309-323. In Proceedings of the Tenth FEBS Meeting. Elsevier-North Holland, Amsterdam.
51. Stanley, W. M. 1974. Specific aminoacylation of the methionine-specific tRNA's of eukaryotes. Methods Enzymol. 29:530-547.
52. Wigle, D. T., and A. E. Smith. 1973. Specificity in initiation in a fractionated mammalian cell-free system. Nature (London) New Biol. 242:136-140.
53. Yan, R., W. Rychlik, D. Etchison, and R. E. Rhoads. 1992. Amino acid sequence of the human protein synthesis initiation factor cIF-4γ. J. Biol. Chem. 267:23226-23231.
54. Voder-Hill, J., A. Pause, N. Sonenberg, and W. C. Merrick. 1993. The p46 subunit of eukaryotic initiation factor (eIF)-4F exchanges with eIF-4A. J. Biol. Chem. 268:5566-5573.