Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1979 Jul;76(7):3111–3115. doi: 10.1073/pnas.76.7.3111

Binding of ribosomes to 5'-terminal leader sequences of eukaryotic messenger RNAs.

W Filipowicz, A L Haenni
PMCID: PMC383773  PMID: 290990

Abstract

Tobacco mosaic virus and turnip yellow mosaic virus genome RNAs, which have long (greater than or equal to 69 nucleotides) 5'-terminal leader sequences preceding the AUG initiation codon, can form disome initiation complexes when incubated with a wheat germ extract and sparsomycin. In tobacco mosaic virus RNA, whereas one ribosome in such complexes presumably occupies the AUG-containing initiation site, the other is located within the RNA leader sequence. The results favor a model of eukaryotic initiation in which ribosomes first bind to the 5' end of the mRNA independently of AUG, then advance to the AUG initiation codon, where protein synthesis ensues.

Full text

PDF
3111

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams S. L., Safer B., Anderson W. F., Merrick W. C. Eukaryotic initiation complex formation. Evidence for two distinct pathways. J Biol Chem. 1975 Dec 10;250(23):9083–9089. [PubMed] [Google Scholar]
  2. Baralle F. E., Brownlee G. G. AUG is the only recognisable signal sequence in the 5' non-coding regions of eukaryotic mRNA. Nature. 1978 Jul 6;274(5666):84–87. doi: 10.1038/274084a0. [DOI] [PubMed] [Google Scholar]
  3. Both G. W., Furuichi Y., Muthukrishnan S., Shatkin A. J. Effect of 5'-terminal structure and base composition on polyribonucleotide binding to ribosomes. J Mol Biol. 1976 Jul 5;104(3):637–658. doi: 10.1016/0022-2836(76)90126-1. [DOI] [PubMed] [Google Scholar]
  4. Briand J. P., Keith G., Guilley H. Nucleotide sequence at the 5' extremity of turnip yellow mosaic virus genome RNA. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3168–3172. doi: 10.1073/pnas.75.7.3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brooker J., Marcus A. Ribosome binding of capped satellite tobacco necrosis virus RNA. FEBS Lett. 1977 Nov 1;83(1):118–124. doi: 10.1016/0014-5793(77)80654-6. [DOI] [PubMed] [Google Scholar]
  6. Bénicourt C., Péré J. P., Haenni A. L. Translation of TYMV RNA into high molecular weight proteins. FEBS Lett. 1978 Feb 15;86(2):268–272. doi: 10.1016/0014-5793(78)80577-8. [DOI] [PubMed] [Google Scholar]
  7. Dasgupta R., Shih D. S., Saris C., Kaesberg P. Nucleotide sequence of a viral RNA fragment that binds to eukaryotic ribosomes. Nature. 1975 Aug 21;256(5519):624–628. doi: 10.1038/256624a0. [DOI] [PubMed] [Google Scholar]
  8. Filipowicz W. Functions of the 5,-terminal m7G cap in eukaryotic mRNA. FEBS Lett. 1978 Dec 1;96(1):1–11. doi: 10.1016/0014-5793(78)81049-7. [DOI] [PubMed] [Google Scholar]
  9. Guilley H., Briand J. P. Nucleotide sequence of turnip yellow mosaic virus coat protein mRNA. Cell. 1978 Sep;15(1):113–122. doi: 10.1016/0092-8674(78)90087-9. [DOI] [PubMed] [Google Scholar]
  10. Hagenbüchle O., Santer M., Steitz J. A., Mans R. J. Conservation of the primary structure at the 3' end of 18S rRNA from eucaryotic cells. Cell. 1978 Mar;13(3):551–563. doi: 10.1016/0092-8674(78)90328-8. [DOI] [PubMed] [Google Scholar]
  11. Hunter A. R., Jackson R. J., Hunt T. The role of complexes between the 40-S ribosomal subunit and Met-tRNA-Met-f in the initiation of protein synthesis in the wheat-germ system. Eur J Biochem. 1977 May 2;75(1):159–170. doi: 10.1111/j.1432-1033.1977.tb11513.x. [DOI] [PubMed] [Google Scholar]
  12. Hunter T. R., Hunt T., Knowland J., Zimmern D. Messenger RNA for the coat protein of tobacco mosaic virus. Nature. 1976 Apr 29;260(5554):759–764. doi: 10.1038/260759a0. [DOI] [PubMed] [Google Scholar]
  13. Jonard G., Richards K., Mohier E., Gerlinger P. Nucleotide sequence at the 5' extremity of tobacco-mosaic-virus RNA. 2. The coding region (nucleotides 69-236). Eur J Biochem. 1978 Mar 15;84(2):521–531. doi: 10.1111/j.1432-1033.1978.tb12195.x. [DOI] [PubMed] [Google Scholar]
  14. Kozak M. How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell. 1978 Dec;15(4):1109–1123. doi: 10.1016/0092-8674(78)90039-9. [DOI] [PubMed] [Google Scholar]
  15. Kozak M. Nucleotide sequences of 5'-terminal ribosome-protected initiation regions from two reovirus messages. Nature. 1977 Sep 29;269(5627):391–394. doi: 10.1038/269390a0. [DOI] [PubMed] [Google Scholar]
  16. Kozak M., Shatkin A. J. Characterization of ribosome-protected fragments from reovirus messenger RNA. J Biol Chem. 1976 Jul 25;251(14):4259–4266. [PubMed] [Google Scholar]
  17. Kozak M., Shatkin A. J. Identification of features in 5' terminal fragments from reovirus mRNA which are important for ribosome binding. Cell. 1978 Jan;13(1):201–212. doi: 10.1016/0092-8674(78)90150-2. [DOI] [PubMed] [Google Scholar]
  18. Kozak M., Shatkin A. J. Migration of 40 S ribosomal subunits on messenger RNA in the presence of edeine. J Biol Chem. 1978 Sep 25;253(18):6568–6577. [PubMed] [Google Scholar]
  19. Kozak M., Shatkin A. J. Sequences of two 5'-terminal ribosome-protected fragments from reovirus messenger RNAs. J Mol Biol. 1977 May 5;112(1):75–96. doi: 10.1016/s0022-2836(77)80157-5. [DOI] [PubMed] [Google Scholar]
  20. Lagerkvist U. "Two out of three": an alternative method for codon reading. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1759–1762. doi: 10.1073/pnas.75.4.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Moss B. Utilization of the guanylyltransferase and methyltransferases of vaccinia virus to modify and identify the 5'-terminals of heterologous RNA species. Biochem Biophys Res Commun. 1977 Jan 24;74(2):374–383. doi: 10.1016/0006-291x(77)90314-x. [DOI] [PubMed] [Google Scholar]
  22. Nombela C., Nombela N. A., Ochoa S., Safer B., Anderson W. F., Merrick W. C. Polypeptide chain initiation in eukaryotes: mechanism of formation of initiation complex. Proc Natl Acad Sci U S A. 1976 Feb;73(2):298–301. doi: 10.1073/pnas.73.2.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pelham H. R. Leaky UAG termination codon in tobacco mosaic virus RNA. Nature. 1978 Mar 30;272(5652):469–471. doi: 10.1038/272469a0. [DOI] [PubMed] [Google Scholar]
  24. Revel M., Groner Y. Post-transcriptional and translational controls of gene expression in eukaryotes. Annu Rev Biochem. 1978;47:1079–1126. doi: 10.1146/annurev.bi.47.070178.005243. [DOI] [PubMed] [Google Scholar]
  25. Richards K., Guilley H., Jonard G., Hirth L. Nucleotide sequence at the 5' extremity of tobacco-mosaic-virus RNA. 1. The noncoding region (nucleotides 1-68). Eur J Biochem. 1978 Mar 15;84(2):513–519. doi: 10.1111/j.1432-1033.1978.tb12194.x. [DOI] [PubMed] [Google Scholar]
  26. Rose J. K. Complete sequences of the ribosome recognition sites in vesicular stomatitis virus mRNAs: recognition by the 40S and 80S complexes. Cell. 1978 Jun;14(2):345–353. doi: 10.1016/0092-8674(78)90120-4. [DOI] [PubMed] [Google Scholar]
  27. Sonenberg N., Shatkin A. J., Ricciardi R. P., Rubin M., Goodman R. M. Analysis of terminal structures of RNA from potato virus X. Nucleic Acids Res. 1978 Jul;5(7):2501–2512. doi: 10.1093/nar/5.7.2501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Steitz J. A., Jakes K. How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4734–4738. doi: 10.1073/pnas.72.12.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weber L. A., Hickey E. D., Nuss D. L., Baglioni C. 5'-Terminal 7-methylguanosine and mRNA function: influence of potassium concentration on translation in vitro. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3254–3258. doi: 10.1073/pnas.74.8.3254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weissbach H., Ochoa S. Soluble factors required for eukaryotic protein synthesis. Annu Rev Biochem. 1976;45:191–216. doi: 10.1146/annurev.bi.45.070176.001203. [DOI] [PubMed] [Google Scholar]
  31. Wodnar-Filipowicz A., Szczesna E., Zan-Kowalczewska M., Muthukrishnan S., Szybiak U., Legocki A. B., Filipowicz W. 5'-Terminal 7-methylguanosine and mRNA function. The effect of enzymatic decapping and of cap analogs on translation of tobacco-mosaic-virus RNA and globin mRNA in vitro. Eur J Biochem. 1978 Dec 1;92(1):69–80. doi: 10.1111/j.1432-1033.1978.tb12724.x. [DOI] [PubMed] [Google Scholar]
  32. Zan-Kowalczewska M., Bretner M., Sierakowska H., Szczesna E., Filipowicz W., Shatkin A. J. Removal of 5'-terminal m7G from eukaryotic mRNAs by potato nucleotide pyrophosphatase and its effect on translation. Nucleic Acids Res. 1977 Sep;4(9):3065–3081. doi: 10.1093/nar/4.9.3065. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES