1887

Journal of General Virology header logo

Volume 66, Issue 12

Two Initiation Sites for Foot-and-Mouth Disease Virus Polyprotein Free

Abstract

SUMMARY

Typically, the translation of eukaryotic mRNAs into protein is initiated at a single site. However, we have recently shown that not one but two primary products, P20a and P16, are translated from the 5′ end of the coding region of the genome of foot-and-mouth disease virus (FMDV). In this paper we show by partial protease digestion of these proteins that they differ only at their N termini, thus confirming the presence of two initiation sites for translation of FMDV RNA. Sequence analysis of two subtypes of the virus (A and A) confirms the presence of two initiator AUG codons in the expected position on the genome. By correlation with protein synthesis data from these subtypes it appears that the relative use of each initiation site is dependent on its surrounding nucleotide sequence. In addition, the ratio of the two proteins when synthesized differs markedly from that when they are synthesized , suggesting the presence of a control mechanism for synthesis of P20a which may be absent . We also show that the cleavage site between these two proteins and the structural protein precursor, P88, is located closer to the N terminus of the polyprotein than has previously been reported.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): FMDV , multiple initiation and translation
© Journal of General Virology 1985
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-66-12-2615
1985-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/66/12/JV0660122615.html?itemId=/content/journal/jgv/10.1099/0022-1317-66-12-2615&mimeType=html&fmt=ahah

References

  1. Beck E., Forss S., Strebel K., Cattaneo R., Feil G. 1983; Structure of the FMDV translation initiation site and of the structural proteins. Nucleic Acids Research 11:7873–7885
     [Google Scholar]
  2. Benton W. D., Davis R. W. 1977; Screening X gt recombinant clones by hybridization to single plaques in situ. Science 196:180
     [Google Scholar]
  3. Boothroyd J. C., Harris T. J. R., Rowlands D. J., LowE P. A. 1982; The nucleotide sequence of cDNA coding for the structural proteins of foot and mouth disease virus. Gene 17:153–161
     [Google Scholar]
  4. Burroughs J. N., Sangar D. V., Clarke B. E., Rowlands D. J., Billiau A., Collen D. 1984; Multiple proteases in foot and mouth disease replication. Journal of Virology 50:878–883
     [Google Scholar]
  5. Butterworth B. E., Hall L., Stoltfus C. M., Rueckert R. R. 1971; Virus specific protein synthesis in encephalomyocarditis virus-infected HeLa cells. Proceedings of the National Academy of Sciences, U. S. A 68:3083–3087
     [Google Scholar]
  6. Carroll A. R., Rowlands D. J., Clarke B. E. 1984; The complete nucleotide sequence of the RNA coding for the primary translation product of foot and mouth disease virus. Nucleic Acids Research 12:2461–2472
     [Google Scholar]
  7. Casadaban M. J., Cohen S. N. 1980; Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. Journal of Molecular Biology 138:179–207
     [Google Scholar]
  8. Celma M. L., Ehrenfeld E. 1975; Translation of poliovirus RNA in vitro: detection of two different initiation sites. Journal of Molecular Biology 98:761–780
     [Google Scholar]
  9. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. 1977; Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. Journal of Biological Chemistry 252:1102–1106
     [Google Scholar]
  10. Degener A. M., Pagnotti P., Facchini J., Perez-bercoff R. 1983; Genomic RNA of Mengovirus. VI. Translation of its two cistrons in lysates of interferon-treated cells. Journal of Virology 45:889–894
     [Google Scholar]
  11. Doel T. R., Sangar D. V., Rowlands D. J., Brown F. 1978; A re-appraisal of the biochemical map of foot-and-mouth disease virus RNA. Journal of General Virology 41:395–404
     [Google Scholar]
  12. Doolittle R. F. 1970; Pyrrolidonecarboxylyl peptidase. Methods in Enzymology 19:555–569
     [Google Scholar]
  13. Dorner A. J., Semler B. L., Jackson R. J., Hanecak R., DupreY E., Wimmer E. 1984; In vitro translation of poliovirus RNA. Utilization of internal initiation sites in reticulocyte lysate. Journal of Virology 50:507–514
     [Google Scholar]
  14. Forss S., Strebel K., Beck E., Schaller H. 1984; Nucleotide sequence and genome organization of foot and mouth disease virus. Nucleic Acids Research 12:6587–6601
     [Google Scholar]
  15. Gheysen D., Iserentant D., Derom C., Fiers W. 1982; Systematic alteration of the nucleotide sequence preceding the translation initiation codon and the effects on bacterial expression of the cloned SV40 small-t antigen gene. Gene 17:55–63
     [Google Scholar]
  16. Giorgi C., Kolakofsky D. 1984; F.ffect of poliovirus superinfection on Sendai virus protein synthesis. Journal of Virology 52:298–299
     [Google Scholar]
  17. Grubman M. J., Baxt B. 1982; Translation of foot and mouth disease virion RNA and processing of the primary cleavage products in a rabbit reticulocyte lysate. Virology 116:19–30
     [Google Scholar]
  18. Grubman M. J., Robertson B. H., Morgan D. O., Moore D. M., Dowbenko D. 1984; Biochemical map of polypeptides specified by foot and mouth disease virus. Journal of Virology 50:579–586
     [Google Scholar]
  19. Grunstein M., Hogness D. S. 1975; Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proceedings of the National Academy of Sciences, U. S. A 72:3961–3965
     [Google Scholar]
  20. Hall M. N., Gabay J., Debarbouille M., Schwartz M. 1982; A role for mRNA secondary structure in the control of translation initiation. Nature, London 295:616–618
     [Google Scholar]
  21. Hewlett M. J., Rose J. K., Baltimore D. 1976; 5′ Terminal structure of poliovirus polyribosomal RNA is pUp. Proceedings of the National Academy of Sciences, U. S. A 73:327–330
     [Google Scholar]
  22. Jacobson M. F., Baltimore D. 1968; Polypeptide cleavages in the formation of poliovirus proteins. Proceedings of the National Academy of Sciences, U. S. A 61:77–84
     [Google Scholar]
  23. Jacobson M. F., Asso J., Baltimore D. 1970; Further evidence on the formation of poliovirus proteins. Journal of Molecular Biology 49:657–669
     [Google Scholar]
  24. King A. M. Q., Newman J. W. I. 1980; Temperature sensitive mutants of foot and mouth disease virus with altered structural polypeptides. I. Identification by electrofocusing. Journal of Virology 34:59–66
     [Google Scholar]
  25. Kozak M. 1980; Evaluation of the ‘scanning model’ for initiation of protein synthesis in eukaryotes. Cell 22:7–8
     [Google Scholar]
  26. Kozak M. 1981; Mechanism of mRNA recognition by eukaryotic ribosomes during initiation of protein synthesis. Current Topics in Microbiology and Immunology 98:81–123
     [Google Scholar]
  27. Kozak M. 1983a; Translation of insulin-related polypeptides from messenger RNAs with tandemly reiterated copies of the ribosome binding site. Cell 34:971–978
     [Google Scholar]
  28. Kozak M. 1983b; Comparison of initiation of protein synthesis in prokaryotes, eukaryotes and organelles. Microbiological Reviews 47:1–45
     [Google Scholar]
  29. Kozak M. 1984; Selection of initiation sites by eukaryotic ribosomes: effect of inserting AUG triplets upstream from the coding sequences for preproinsulin. Nucleic Acids Research 12:3873–3893
     [Google Scholar]
  30. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227:680–685
     [Google Scholar]
  31. Lee Y. F., Nomoto A., Wimmer E. 1976; The genome of poliovirus is an exceptional mRNA. Progress in Nucleic Acids Research and Molecular Biology 19:89–96
     [Google Scholar]
  32. Lewin B. 1980 In Gene Expression vol 2: pp 679–683 New York: John Wiley & Sons;
     [Google Scholar]
  33. Liu C.-C., Simonsen C. C., Levinson A. D. 1984; Initiation of translation at internal AUG codons in mammalian cells. Nature, London 309:82–85
     [Google Scholar]
  34. Losson R., Fuchs R. P. P., Lacroute F. 1983; In vivo transcription of a eukaryotic regulatory gene. EMBO Journal 2:2179–2184
     [Google Scholar]
  35. Maxam A. M., Gilbert W. 1980; Sequencing end-labeled DNA with base-specific chemical cleavages. Methods in Enzymology 65:499–560
     [Google Scholar]
  36. Mertens P. P. C., Dobos P. 1982; Messenger RNA of infectious pancreatic necrosis virus is polycistronic. Nature, London 297:243–246
     [Google Scholar]
  37. Messing J., Vieira J. 1982; A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene 19:269–276
     [Google Scholar]
  38. Palmenberg A. C., Kirby E. M., Janda M. R., Drake N. L., Duke G. M., Potratz K. F., Collett M. S. 1984; The nucleotide and deduced amino acid sequences of the encephalomyocarditis viral polyprotein coding region. Nucleic Acids Research 12:2969–2985
     [Google Scholar]
  39. Perez-bercoff R., Kaempfer R. 1982; Genomic RN A of mengovirus. V. Recognition of common features by ribosomes and eukaryotic initiation factor 2. Journal of Virology 41:30–31
     [Google Scholar]
  40. Rekosh D. M. 1977; The molecular biology of picornaviruses. In The Molecular Biology of Animal Viruses vol 1: pp 63–110 Edited by Nayak D. P. New York: Marcel Dekker;
     [Google Scholar]
  41. Rowlands D. J., Harris T. J. R., Brown F. 1978; More precise location of the polycytidylic acid tract in foot and mouth disease virus RNA. Journal of Virology 26:335–343
     [Google Scholar]
  42. Rowlands D. J., Clarke B. E., Carroll A. R., Brown F., Nicholson B. H., Bittle J. L., HoughteN R. A., Lerner R. A. 1983; Chemical basis of antigenic variation in foot and mouth disease virus. Nature, London 306:694–697
     [Google Scholar]
  43. Rueckert R. R., Wimmer E. 1984; Systematic nomenclature of picornavirus proteins. Journal of Virology 50:957–959
     [Google Scholar]
  44. Sangar D. V., Black D. N., Rowlands D. J., Brown F. 1977; Biochemical mapping of the foot-and-mouth disease virus genome. Journal of General Virology 35:281–297
     [Google Scholar]
  45. Sangar D. V., Black D. N., Rowlands D. J., Harris T. J. R., Brown F. 1980; Location of the initiation site for protein synthesis on foot and mouth disease virus RNA by in vitro translation of defined fragments of the RNA. Journal of Virology 33:59–68
     [Google Scholar]
  46. 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]
  47. Skinner M. A., Ebner D., Siddell S. G. 1985; Coronavirus MHV-JHM mRNA has a sequence arrangement which potentially allows translation of a second, downstream open reading frame. Journal of General Virology 66:581–592
     [Google Scholar]
  48. Thireos G., Driscoll Penn M., Greer H. 1984; 5′ untranslated sequences are required for the translational control of a yeast regulatory gene. Proceedings of the National Academy of Sciences, U. S. A 81:5096–5100
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-66-12-2615
Loading
Two Initiation Sites for Foot-and-Mouth Disease Virus Polyprotein in vivo
J. Gen. Virol. 66, 2615 (1985); https://doi.org/10.1099/0022-1317-66-12-2615
/content/journal/jgv/10.1099/0022-1317-66-12-2615
/content/journal/jgv/10.1099/0022-1317-66-12-2615
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error