Effects of sequence elements in the potato virus X RNA 5′ non-translated -leader on its translation enhancing activity Free

Abstract

The 5′ non-translated -leader sequence of potato virus X RNA consists of two regions: the sequence (41 nucleotides with no G) and the sequence (42 nucleotides upstream from AUG). The -leader has been shown to enhance strongly the expression of adjacent genes in chimeric mRNAs. This phenomenon has been postulated to be due to the unpaired conformation of the 5′-terminal 30 nucleotides and/or to the presence within the region of the CCACC pentanucleotide complementary to the 3′-terminal conserved structure of 18S rRNA. Different derivatives of -leader have been constructed for use in determining the contribution of separate elements of the sequence to translational enhancement. It was found that deletion of the sequence large fragment which was supposed to be unfolded did not reduce the Δ-leader enhancement activity. Moreover, translational enhancement was greater for this derivative. Deletion of the sequence resulted in a considerable increase in activity of the -leader showing that the region was dispensable for translation. Disruption or ‘masking’ of CCACC led to inactivation of the -leader as a translational enhancer. Thus, we identified the CCACC pentanucleotide as the primary motif responsible for the translation enhancing ability of -leader.

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1993-12-01
2024-03-29
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References

  1. Adams S. E., Jones R. A., Coutts R. H. A. 1987; A comparison between the capsid proteins and the products of in vitro translation of three strains of potato virus X. Journal of General Virology 68:3207–3210
    [Google Scholar]
  2. Berben-Bloemhevel G., Kasperaitis M. A. M., van Haugten H., Thomas A. A. M., van Steeg H., Voorma H. O. 1992; Interaction of initiation factors with the cap structure of chimeric mRNA containing the 5′-untranslated regions of Semliki Forest virus RNA is related to translational efficiency. European Journal of Biochemistry 208:578–581
    [Google Scholar]
  3. Carrington J. C., Freed D. D. 1990; Cap-independent enhancement of translation by a plant potyvirus 5′-nontranslated region. Journal of Virology 64:1590–1597
    [Google Scholar]
  4. Gallie D. R., Walbot V. 1992; Identification of the motifs within the tobacco mosaic virus 5′-leader responsible for enhancing translation. Nucleic Acids Research 20:4631–1638
    [Google Scholar]
  5. Gallie D. R., Sleat D. E., Watts J. W., Turner P. C., Wilson T. M. A. 1987a; The 5′-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Research 15:3257–3273
    [Google Scholar]
  6. Gallie D. R., Sleat D. E., Watts J. W., Turner P. C., Wilson T. M. A. 1987b; A comparison of eukaryotic viral 5′-leader sequence as enhancers of mRNAs expression in vivo. Nucleic Acids Research 15:8693–8711
    [Google Scholar]
  7. Gallie D. R., Sleat D. E., Watts J. W., Turner P. C., Wilson T. M. A. 1988; Mutational analysis of the tobacco mosaic virus 5′-leader for altered ability to enhance translation. Nucleic Acids Research 16:883–893
    [Google Scholar]
  8. Hagenbuchle O., Santer M., Steitz J. A. 1978; Conservation of the primary structure at the 3′-end of 18S rRNA from eukaryotic cells. Cell 13:551–563
    [Google Scholar]
  9. Huisman M. J., Linthorst H. J. M., Bol J. F., Cornelissen B. J. C. 1988; The complete nucleotide sequence of potato virus X and its homologies at the amino acid level with various plus-stranded RNA viruses. Journal of General Virology 69:1789–1798
    [Google Scholar]
  10. Jobling S. A., Gehrke L. 1987; Enhanced translation of chimeric messenger RNAs containing a plant virus untranslated leader sequence. Nature, London 325:622–625
    [Google Scholar]
  11. Koenig R., Lesemann D. E. 1978; Potexvirus group. CMI/AAB Descriptions of Plant Viruses no. 200
    [Google Scholar]
  12. Kozak M. 1981; Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Research 9:5233–5252
    [Google Scholar]
  13. Kozak M. 1990; Determinants of translational efficiency in mRNAs from higher eukaryotes. In Post-Transcriptional Control of Gene Expression NATO ISI Series vol H49 pp 227–236 Edited by McCarthy J. E. G., Tuite M. F. Berlin: Springer Verlag;
    [Google Scholar]
  14. Kozak M. 1991; Structural features in eukaryotic mRNAs that modulate the initiation of translation. Journal of Biological Chemistry 266:19867–19870
    [Google Scholar]
  15. Morozov S. Yu., Gorbulev V. G., Novikov V. K., Agranovsky A. A., Kozlov Y. V., Atabekov J. G., Bayev A. A. 1981; The primary structure of the 5′- and 3′-terminal regions of the RNA of potato virus X. Dokladi Akademia Nauk SSSR 259:723–725 (in Russian)
    [Google Scholar]
  16. Morozov S. Yu., Miroshnichenko N. A., Zelenina D. A., Fedorkin O. N., Solovyev A. G., Lukasheva L. I., Atabekov J. G. 1990; Expression of RNA transcripts of potato virus X full-length and subgenomic cDNAs. Biochimie 12:677–684
    [Google Scholar]
  17. Morozov S. Yu., Miroshnichenko N. A., Solovyev A. G., Fedorkin O. N., Zelenina D. A., Lukasheva L. I., Karasev A. V., Dolja V. V., Atabekov J. G. 1991; Expression strategy of the potato virus X triple gene block. Journal of General Virology 72:2039–2042
    [Google Scholar]
  18. Nicolaisen M., Johansen E., Poulsen G. B., Borkardt B. 1992; The 5′-untranslated region from pea seedborne mosaic potyvirus RNA as a translational enhancer in pea and tobacco protoplasts. FEBS Letters 303:169–172
    [Google Scholar]
  19. Pilipenko E. V., Gmyl A. P., Maslova S. V., Svitkin Yu. V., Sinyakov A. N., Agol V. I. 1992; Prokaryotic-like cis-elements in the cap-independent internal initiation of translation on picorna-virus RNA. Cell 68:119–131
    [Google Scholar]
  20. Pooggin M. M., Skryabin K. G. 1992; The 5′-untranslated leader sequence of potato virus X RNA enhances the expression of heterologous gene in vivo. Molecular and General Genetics 234:329–331
    [Google Scholar]
  21. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, U,. S,. A 74:5463–5467
    [Google Scholar]
  22. Sargan D. R., Gregory S. P., Butterworth P. H. W. 1982; A possible novel interaction between the 3′-end of 18S ribosomal RNA and the 5′-leader sequence of many eukaryotic messenger RNAs. FEBS Letters 147:133–136
    [Google Scholar]
  23. Skryabin K. G., Morozov S. Yu., Kraev A. S., Rozanov M. N., Chernov B. K., Lukasheva L. I., Atabekov J. G. 1988; Conserved and variable elements in RNA genomes of potexviruses. FEBS Letters 240:33–40
    [Google Scholar]
  24. Sleat D. E., Wilson T. M. A. 1992; Plant virus genomes as sources of novel functions for genetic manipulations. In Genetic Engineering with Plant Viruses pp 55–114 Edited by Wilson T. M. A., Davies J. W. Boca Raton: CRC Press;
    [Google Scholar]
  25. Sleat D. E., Gallie D. R., Jefferson R. A., Bevan M. W., Turner P. C., Wilson T. M. A. 1987; Characterization of the 5′-leader sequence of tobacco mosaic virus RNA as a general enhancer of translation in vitro. Gene 60:217–225
    [Google Scholar]
  26. Sleat D. E., Hull R., Turner P. C., Wilson T. M. A. 1988; Studies on the mechanism of translation enhancement by the 5′-leader sequence of tobacco mosaic virus RNA. European Journal of Biochemistry 175:75–86
    [Google Scholar]
  27. Smirnyagina E. V., Morozov S. Yu., Rodionova N. P., Miroshnichenko N. A., Solovyev A. G., Fedorkin O. N., Atabekov J. G. 1991; Translational efficiency and competitive ability of mRNAs with 5′-untranslated αβ-leader of potato virus X RNA. Biochimie 73:998–1011
    [Google Scholar]
  28. Sonenberg N., Shatkin A. J., Ricciardi R. P., Rubin M., Goodman R. M. 1978; Analysis of terminal structures of RNA from potato virus X. Nucleic Acids Research 5:2501–2512
    [Google Scholar]
  29. Thanaraj T. A., Pandit M. W. 1990; Translation-initiation promoting site on transcripts of highly expressed genes from Saccharomyces cerevisiae and the role of hairpin stems to position the site near the initiation codon. Journal of Biomolecular Structure and Dynamics 1:1279–1289
    [Google Scholar]
  30. Tomashevskaya O. L., Solovyev A. G., Karpova O. V., Fedorkin O. N., Morozov S. Yu., Rodionova N. P., Atabekov J. G. 1992; The contribution of separate structural elements of the nontranslational sequence of potato virus X RNA in translational enhancement. Dokladi Akademia Nauk SSSR 324:697–700
    [Google Scholar]
  31. Wilson T. M. A., Saunders K., Dowson-Dag M. J., Sleat D. E., Trachel H., Mundry K. W. 1990; Effects of the 5′-leader sequence of tobacco mosaic virus RNA, or derivatives thereof, on foreign mRNA and native viral gene expression. In Post-Transcriptional Control of Gene Expression NATO ISI Series vol H49 pp 262–275 Edited by McCarthy J. E. G., Tuite M. F. Berlin: Springer Verlag;
    [Google Scholar]
  32. Wodnar-Filipowicz A., Skreczowski L. J., Filipowicz W. 1980; Translation of potato virus X RNA into high molecular weight proteins. FEBS Letters 109:151–155
    [Google Scholar]
  33. Wu S., Rinehart C. A., Kaesberg P. 1987; Sequence and organization of southern bean mosaic virus genomic RNA. Virology 161:73–80
    [Google Scholar]
  34. Yamaguchi K., Hidaka S., Miura K. 1982; Relationship between structure of the 5′-noncoding region of viral mRNA and efficiency in the initiation step of protein synthesis in an eukaryotic system. Proceedings of the National Academy of Sciences, U,. S,. A 79:1012–1016
    [Google Scholar]
  35. Yokoe S., Tanaka M., Hibasami H., Nagai J., Nakashima K. 1983; Cross-linking of tobacco mosaic virus RNA and capped poly-ribonucleotides to 18S rRNA in wheat germ ribosome-mRNA complexes. Journal of Biochemistry (Tokyo) 94:1803–1808
    [Google Scholar]
  36. Zelenina D. A., Kulaeva O. I., Smirnyagina E. V., Solovyev A. G., Miroshnichenko N. A., Fedorkin O. N., Rodionova N. P., Morozov S. Yu., Atabekov J. G. 1992; Translation enhancing properties of the 5′-leader of potato virus genomic RNA. FEBS Letters 296:267–270
    [Google Scholar]
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