A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initation of hepatitis C and classical swine fever virus RNAs

Genes and Development

Volumn 12, Issue 1, 1998, Pages 67-83

  Pestova, Tatyana V ^a,b   Shatsky, Ivan N ^b   Fletcher, Simon P ^c   Jackson, Richard J ^c   Hellen, Christopher U T ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Hepatitis C virus; MRNA; Protein synthesis; Ribosome; Translation initiation

Indexed keywords

ANIMAL CELL; ANTICODON; ARTICLE; BASE PAIRING; CODON; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; HEPATITIS C; NONHUMAN; PESTIVIRUS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; RABBIT; RIBOSOME SUBUNIT; TRANSLATION INITIATION;

ANIMALIA; CLASSICAL SWINE FEVER VIRUS; EUKARYOTA; HEPATITIS C VIRUS; ORYCTOLAGUS CUNICULUS; PESTIVIRUS; PROKARYOTA; SUS SCROFA;

EID: 0031905698     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.1.67     Document Type: Article

References (45)

1. 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.
2. Baker, A.-M. and D.E. Draper. 1995. Messenger RNA recognition by fragments of ribosomal protein S4. J. Biol. Chem. 270: 22939-22945.
3. Benne, R. and J.W.B. Hershey. 1978. The mechanism of action of protein synthesis initiation factors from rabbit reticulocytes. J. Biol. Chem. 253: 3078-3087.
4. Benne, R., M.L. Brown-Luedi, and J.W.B. Hershey. 1978. Purification and characterization of protein synthesis initiation factors eIF-1, eIF-4C, eIF-4D, and eIF-5 from rabbit reticulocytes. J. Biol. Chem. 253: 3070-3077.
5. Blum, S., M. Mueller, S.R. Schmid, P. Linder, and H. Trachsel. 1989. Translation in Saccharomyces cerevisiae: Initiation factor 4A-dependent cell-free system. Proc. Natl. Acad. Sci. 86: 6043-6046.
6. Borman, A. and R.J. Jackson. 1992. Initiation of translation of human rhinovirus RNA: Mapping the internal ribosome entry site. Virology 188: 685-696.
7. Brown, E.A., H. Zhang, L.-H. Ping, and S.M. Lemon. 1992. Secondary structure of the 5′ nontranslated regions of hepatitis C virus and pestivirus genomic RNAs. Nucleic Acids Res. 20: 5041-5045.
8. Chan, Y.-L., V. Paz, J. Olvera, and I.G. Wool. 1993. The primary structure of rat ribosomal protein S9. Biochem. Biophys. Res. Comm. 193: 106-112.
9. Dasso, M.C., S.C. Milburn, J.W.B. Hershey, and R.J. Jackson. 1990. Selection of the 5′-proximal translation initiation site is influenced by mRNA and eIF-2 concentrations. Eur. J. Biochem. 187: 361-371.
10. Evstafieva, A.G., T.Y. Ugarova, B.K. Chernov, and I.N. Shatsky. 1991. A complex RNA sequence determines the internal initiation of encephalomyocarditis virus RNA translation. Nucleic Acids Res. 19: 665-671.
11. Grifo, J.A., S.M. Tahara, M.A. Morgan, A.J. Shatkin, and W.C. Merrick. 1983. New initiation factor activity required for globin mRNA translation. J. Biol. Chem. 258: 5804-5810.
12. Gualerzi, C.O. and C.L. Pon. 1990. Initiation of mRNA translation in prokaryotes. Biochemistry 29: 1684-1689.
13. Hartz, D., D.S. McPheeters, R. Traut, and L. Gold. 1988. Extension inhibition analysis of translation initiation complexes. Methods Enzymol. 164: 419-425.
14. Hartz, D., D.S. McPheeters, L. Green, and L. Gold. 1991. Detection of Escherichia coli ribosome binding at translation initiation sites in the absence of tRNA. J. Mol. Biol. 218: 99-105.
15. Honda, M., E.A. Brown, and S.M. Lemon. 1996. Stability of a stem-loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA. RNA 2: 955-968.
16. Jackson, R.J. and A. Kaminski. 1995. Internal initiation of translation in eukaryotes: The picornavirus paradigm and beyond. RNA 1: 985-1000.
17. 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.
18. Kolupaeva, V.G., C.U.T. Hellen, and I.N. Shatsky. 1996. Structural analysis of the interaction of the pyrimidine tract-binding protein with the internal ribosomal entry site of encephalomyocarditis virus and foot-and-mouth disease virus RNAs. RNA 2: 1199-1212.
19. Kozak, M. 1987. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol. Cell. Biol. 7: 3438-3445.
20. 14-methionylpuromycin. Biochem. Biophys. Res. Comm. 25: 233-238.
21. Lu, H.-H. and E. Wimmer. 1996. Poliovirus chimeras replicating under the translational control of genetic elements of hepatitis C virus reveal unusual properties of the internal ribosomal entry site of hepatitis C virus. Proc. Natl. Acad. Sci. 93: 1412-1417.
22. Lütsch, G., H. Bielka, G. Enzmann, and F. Noll. 1983. Electron microscopic investigations on the location of rat liver ribosomal proteins S3a, 5, S6, S7, and S9 by means of antibody labeling. Biomed. Biochim. Acta 42: 705-723.
23. McCarthy, J.E.G. and R. Brimacombe. 1994. Prokaryotic translation: The interactive pathway leading to initiation. Trends Genet. 10: 402-407.
24. Merrick, W.C. 1979. Purification of protein synthesis initiation factors from rabbit reticulocytes. Methods Enzymol. 60: 101-108.
25. _. 1992. Mechanism and regulation of eukaryotic protein synthesis. Microbiol. Rev. 56: 291-315.
26. Meyers, G., T. Rumenapf, and H.-J. Thiel. 1989. Molecular cloning and nucleotide sequence of the genome of hog cholera virus. Virology 171: 555-567.
27. Mundus, D.A., K.N. Bulygin, V.I. Yamkovoy, A.A. Malygin, M.N. Repkova, L.V. Vratskikh, A.G. Venijaminova, S.N. Vladimirov, and G.G. Karpova. 1993. Structural placement of the codon-anticodon interaction area in human placenta ribosomes. Affinity labeling of the 40S subunits by derivatives of oligoribo-nucleotides containing the AUG codon. Biochim. Biophys. Acta 1173: 273-282.
28. 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.
29. Pestova, T.V., C.U.T. Hellen, and E. Wimmer. 1991. Translation of poliovirus RNA: Role of an essential cis-acting oligopyrimidine element within the 5′-nontranslated region and involvement of a cellular 57-kilodaton protein. J. Virol. 65: 6194-6204.
30. Pestova, T.V., C.U.T. Hellen, and E. Wimmer. 1994. A conserved AUG triplet in the 5′ non translated region of poliovirus can function as an initiation codon in vitro and in vivo. Virology 204: 729-737.
31. Pestova, T.V., C.U.T. Hellen, and I.N. Shatsky. 1996a. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol. 16: 6859-6869.
32. Pestova, T.V, I.N. Shatsky, and C.U.T. Hellen. 1996b. 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. Mol. Cell. Biol. 16: 6870-6878.
33. Pilipenko, E.V., A.P. Gmyl, S.V. Maslova, Y.V. Svitkin, A.N. Sinyakov, and V.I. Agol. 1992. Prokaryotic-like cis elements in the cap-independent internal initiation of translation on picornavirus RNA. Cell 68: 119-131.
34. Pilipenko, E.V., A.P. Gmyl, S.V. Maslova, G.A. Belov, A.N. Sinyakov, M. Huang, T.D.K. Brown, and V.I. Agol. 1994. Starting window, a distinct element in the cap-independent internal initiation of translation on picornaviral RNA. J. Mol. Biol. 241: 398-414.
35. Poole, T.L., C. Wang, R.A. Popp, L.N.D. Potgieter, A. Siddiqui, and M.S. Collett. 1995. Pestivirus translation initiation occurs by internal ribosome entry. Virology 206: 750-754.
36. Reynolds, J.E., A. Kaminski, H.J. Kettinen, K. Grace, B.E. Clarke, A.R. Carroll, D.J. Rowlands, and R.J. Jackson. 1995. Unique features of internal initiation of hepatitis C virus RNA translation. EMBO J. 14: 6010-6020.
37. Reynolds, J.E., A. Kaminski, A.R. Carroll, B.E. Clarke, D.J. Rowlands, and R.J. Jackson. 1996. Internal initiation of translation of hepatitis C virus RNA: The ribosome entry site is at the authentic initiation codon. RNA 2: 867-878.
38. Rijnbrand, R., P.J. Bredenbeek, T. van der Straaten, L. Whetter, G. Inchauspé, S. Lemon, and W. Spaan. 1995. Almost the entire 5′ non-translated region of hepatitis C virus is required for cap-independent translation. FEBS Letts. 365: 115-119.
39. Rijnbrand, R., T.E.M. Abbink, P.C.J. Haasnoot, W.J.M. Spaan, and P.J. Bredenbeek. 1996. The influence of AUG codons in the hepatitis C virus 5′ nontranslated region on translation and mapping of the translation initiation window. Virology 226: 47-56.
40. Rijnbrand, R., T. van der Straaten, P.A. van Rijn, W.J.M. Spaan, and P.J. Bredenbeek. 1997. Internal entry of ribosomes is directed by the 5′ noncoding region of classical swine fever virus and is dependent on the presence of an RNA pseudoknot upstream of the initiation codon. J. Virol. 71: 451-457.
41. Sonenberg, N. 1996. mRNA 5′ cap-binding protein eIF4E and control of cell growth. In Translation control (ed. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 271-294. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Sundkvist, I.C. and T. Staehelin. 1975. Structure and function of free 40S ribosome subunits: Characterization of initiation factors. J. Mol. Biol. 99: 401-418.
43. Trachsel, H., B. Erni, M.H. Schreier, and T. Staehelin. 1977. Initiation of mammalian protein synthesis. II. The assembly of the initiation complex with purified initiation factors. J. Mol. Biol. 116: 755-767.
44. Tsukiyama-Kohara, K., N. Iizuka, M. Kohara, and A. Nomoto. 1992. Internal ribosomal entry site within hepatitis C virus RNA. J. Virol. 66: 1476-1483.
45. Wang, C., S.Y. Le, N. Ali, and A. Siddiqui. 1995. An RNA pseudoknot is an essential structural element of the internal ribosome entry site located within the hepatitis C virus 5′ noncoding region. RNA 1: 526-537.