1887

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Volume 92, Issue 5

Influence of the 5′-proximal elements of the 5′-untranslated region of classical swine fever virus on translation and replication Free

Abstract

The 5′-terminal sequence spanning nt 1–29 of the 5′-untranslated region of classical swine fever virus (CSFV) forms a 5′-proximal stem–loop structure known as domain Ia. Deletions and replacement mutations were performed to examine the role of this domain. Deletion of the 5′-proximal nucleotides and disruption of the stem–loop structure greatly increased internal ribosome entry site-mediated translation but abolished the replication of the replicons. Internal deletions resulting in a change in the size of the loop of domain Ia, and even removal of the entire domain, did not substantially change the translation activity, but reduced the replication of CSFV replicons provided the replicons contained the extreme 5′-GUAU terminal sequence. Internal replacements leading to a change in the nucleotide sequence of the loop did not alter the translation and replication activities of the CSFV RNA replicon, and did not influence the rescue of viruses and growth characteristics of new viruses. These results may be important for our understanding of the regulation of translation, replication and encapsidation in CSFV and other positive-sense RNA viruses.

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© 2011 SGM
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2011-05-01
2024-04-18
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References

  1. Baird S. D., Turcotte M., Korneluk R. G., Holcik M. 2006; Searching for IRES. RNA 12:1755–1785 [View Article][PubMed]
     [Google Scholar]
  2. Barton D. J., Morasco B. J., Flanegan J. B. 1999; Translating ribosomes inhibit poliovirus negative-strand RNA synthesis. J Virol 73:10104–10112[PubMed]
     [Google Scholar]
  3. Becher P., Thiel H.-J. 2002; Genus Pestivirus (Flaviviridae). In The Springer Index of Viruses pp. 327–331 Edited by Tidona C. A., Darai G. Heidelberg, Germany: Springer-Verlag; [View Article]
     [Google Scholar]
  4. Becher P., Orlich M., Thiel H.-J. 2000; Mutations in the 5′ nontranslated region of bovine viral diarrhea virus result in altered growth characteristics. J Virol 74:7884–7894 [View Article][PubMed]
     [Google Scholar]
  5. Chon S. K., Perez D. R., Donis R. O. 1998; Genetic analysis of the internal ribosome entry segment of bovine viral diarrhea virus. Virology 251:370–382 [View Article][PubMed]
     [Google Scholar]
  6. Cuthbert J. A. 1994; Hepatitis C: progress and problems. Clin Microbiol Rev 7:505–532[PubMed]
     [Google Scholar]
  7. Fletcher S. P., Jackson R. J. 2002; Pestivirus internal ribosome entry site (IRES) structure and function: elements in the 5′ untranslated region important for IRES function. J Virol 76:5024–5033 [View Article][PubMed]
     [Google Scholar]
  8. Fletcher S. P., Ali I. K., Kaminski A., Digard P., Jackson R. J. 2002; The influence of viral coding sequences on pestivirus IRES activity reveals further parallels with translation initiation in prokaryotes. RNA 8:1558–1571[PubMed]
     [Google Scholar]
  9. Friebe P., Bartenschlager R. 2009; Role of RNA structures in genome terminal sequences of the hepatitis C virus for replication and assembly. J Virol 83:11989–11995 [View Article][PubMed]
     [Google Scholar]
  10. Gamarnik A. V., Andino R. 1998; Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev 12:2293–2304 [View Article][PubMed]
     [Google Scholar]
  11. Gong Y., Trowbridge R., Macnaughton T. B., Westaway E. G., Shannon A. D., Gowans E. J. 1996; Characterization of RNA synthesis during a one-step growth curve and of the replication mechanism of bovine viral diarrhoea virus. J Gen Virol 77:2729–2736 [View Article][PubMed]
     [Google Scholar]
  12. He Y., Yan W., Coito C., Li Y., Gale M. Jr, Katze M. G. 2003; The regulation of hepatitis C virus (HCV) internal ribosome-entry site-mediated translation by HCV replicons and nonstructural proteins. J Gen Virol 84:535–543 [View Article][PubMed]
     [Google Scholar]
  13. Heinz F. X., Collett M. S., Purcell R. H., Gould E. A., Howard C. R., Houghton M., Moormann R. J. M., Rice C. M., Thiel H.-J. 2000; Family Flaviviridae. In Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses pp. 859–878 Edited by Fauquet C. M., van Regenmortel M. H. V., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J. et al. San Diego, CA: Academic Press;
     [Google Scholar]
  14. Honda M., Beard M. R., Ping L.-H., Lemon S. M. 1999; A phylogenetically conserved stem–loop structure at the 5′ border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J Virol 73:1165–1174[PubMed]
     [Google Scholar]
  15. Huang Q., Zhang C., Wang J., Wang N., Fu L. 1998; Molecular cloning and nucleotide sequence of classical swine fever virus strain Shimen. Wuhan Univ J Nat Sci 3:504–508 [View Article]
     [Google Scholar]
  16. Isken O., Grassmann C. W., Sarisky R. T., Kann M., Zhang S., Grosse F., Kao P. N., Behrens S. E. 2003; Members of the NF90/NFAR protein group are involved in the life cycle of a positive-strand RNA virus. EMBO J 22:5655–5665 [View Article][PubMed]
     [Google Scholar]
  17. Isken O., Grassmann C. W., Yu H., Behrens S. E. 2004; Complex signals in the genomic 3′ nontranslated region of bovine viral diarrhea virus coordinate translation and replication of the viral RNA. RNA 10:1637–1652 [View Article][PubMed]
     [Google Scholar]
  18. Junker-Niepmann M., Bartenschlager R., Schaller H. 1990; A short cis-acting sequence is required for hepatitis B virus pregenome encapsidation and sufficient for packaging of foreign RNA. EMBO J 9:3389–3396[PubMed]
     [Google Scholar]
  19. Kolupaeva V. G., Pestova T. V., Hellen C. U. T. 2000; Ribosomal binding to the internal ribosomal entry site of classical swine fever virus. RNA 6:1791–1807 [View Article][PubMed]
     [Google Scholar]
  20. Lu J., Zhang J., Wang X., Jiang H., Liu C., Hu Y. 2006; In vitro and in vivo identification of structural and sequence elements in the 5′ untranslated region of Ectropis obliqua picorna-like virus required for internal initiation. J Gen Virol 87:3667–3677 [View Article][PubMed]
     [Google Scholar]
  21. Luo G., Xin S., Cai Z. 2003; Role of the 5′-proximal stem–loop structure of the 5′ untranslated region in replication and translation of hepatitis C virus RNA. J Virol 77:3312–3318 [View Article][PubMed]
     [Google Scholar]
  22. Moennig V., Plagemann P. G. W. 1992; The pestiviruses. Adv Virus Res 41:53–98 [View Article][PubMed]
     [Google Scholar]
  23. Pankraz A., Thiel H. J., Becher P. 2005; Essential and nonessential elements in the 3′ nontranslated region of bovine viral diarrhea virus. J Virol 79:9119–9127 [View Article][PubMed]
     [Google Scholar]
  24. Reed L. J., Muench H. 1938; A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–497
     [Google Scholar]
  25. Rice C. M. 1996; Flaviviridae: the viruses and their replication. 1996. In Fields Virology pp. 931–959 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia, PA: Raven Press;
     [Google Scholar]
  26. Rijnbrand R., Bredenbeek P., van der Straaten T., Whetter L., Inchauspé G., Lemon S., Spaan W. 1995; Almost the entire 5′ non-translated region of hepatitis C virus is required for cap-independent translation. FEBS Lett 365:115–119 [View Article][PubMed]
     [Google Scholar]
  27. Rijnbrand R., van der Straaten T., van Rijn P. A., Spaan W. J. M., Bredenbeek P. J. 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[PubMed]
     [Google Scholar]
  28. Sheng C., Xiao M., Geng X., Liu J., Wang Y., Gu F. 2007; Characterization of interaction of classical swine fever virus NS3 helicase with 3′ untranslated region. Virus Res 129:43–53 [View Article][PubMed]
     [Google Scholar]
  29. Sheng C., Zhu Z., Yu J., Wan L., Wang Y., Chen J., Gu F., Xiao M. 2010; Characterization of NS3, NS5A and NS5B of classical swine fever virus through mutation and complementation analysis. Vet Microbiol 140:72–80 [View Article][PubMed]
     [Google Scholar]
  30. Steffens S., Thiel H. J., Behrens S. E. 1999; The RNA-dependent RNA polymerases of different members of the family Flaviviridae exhibit similar properties in vitro. J Gen Virol 80:2583–2590[PubMed]
     [Google Scholar]
  31. Wang Y., Xiao M., Chen J., Zhang W., Luo J., Bao K., Nie M., Chen J., Li B. 2007; Mutational analysis of the GDD sequence motif of classical swine fever virus RNA-dependent RNA polymerases. Virus Genes 34:63–65 [View Article][PubMed]
     [Google Scholar]
  32. Wu H., Zhang C., Zheng C., Wang J., Pan Z., Li L., Cao S., Yi G. 2003; Construction of cytopathic PK-15 cell model of classical swine fever virus. Chin Sci Bull 48:887–891 [View Article]
     [Google Scholar]
  33. Xiao M., Zhang C. Y., Pan Z. S., Wu H. X., Guo J. Q. 2002; Classical swine fever virus NS5B–GFP fusion protein possesses an RNA-dependent RNA polymerase activity. Arch Virol 147:1779–1787 [View Article][PubMed]
     [Google Scholar]
  34. Xiao M., Gao J., Wang W., Wang Y., Chen J., Chen J., Li B. 2004a; Specific interaction between the classical swine fever virus NS5B protein and the viral genome. Eur J Biochem 271:3888–3896 [View Article][PubMed]
     [Google Scholar]
  35. Xiao M., Gao J., Wang Y., Wang X., Lu W., Zhen Y., Chen J., Li B. 2004b; Influence of a 12-nt insertion present in the 3′ untranslated region of classical swine fever virus HCLV strain genome on RNA synthesis. Virus Res 102:191–198 [View Article][PubMed]
     [Google Scholar]
  36. Xiao M., Li H., Wang Y., Wang X., Wang W., Peng J., Chen J., Li B. 2006; Characterization of the N-terminal domain of classical swine fever virus RNA-dependent RNA polymerase. J Gen Virol 87:347–356 [View Article][PubMed]
     [Google Scholar]
  37. Xiao M., Wang Y., Zhu Z., Yu J., Wan L., Chen J. 2009; Influence of NS5A protein of classical swine fever virus (CSFV) on CSFV internal ribosome entry site-dependent translation. J Gen Virol 90:2923–2928 [View Article][PubMed]
     [Google Scholar]
  38. Yu H., Grassmann C. W., Behrens S. E. 1999; Sequence and structural elements at the 3′ terminus of bovine viral diarrhea virus genomic RNA: functional role during RNA replication. J Virol 73:3638–3648[PubMed]
     [Google Scholar]
  39. Yu H., Isken O., Grassmann C. W., Behrens S. E. 2000; A stem–loop motif formed by the immediate 5′ terminus of the bovine viral diarrhea virus genome modulates translation as well as replication of the viral RNA. J Virol 74:5825–5835 [View Article][PubMed]
     [Google Scholar]
  40. Zhao J.-J., Cheng D., Li N., Sun Y., Shi Z., Zhu Q.-H., Tu C., Tong G.-Z., Qiu H.-J. 2008; Evaluation of a multiplex real-time RT-PCR for quantitative and differential detection of wild-type viruses and C-strain vaccine of Classical swine fever virus. Vet Microbiol 126:1–10 [View Article][PubMed]
     [Google Scholar]
  41. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [View Article][PubMed]
     [Google Scholar]
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Influence of the 5′-proximal elements of the 5′-untranslated region of classical swine fever virus on translation and replication
J. Gen. Virol. 92, 1087 (2011); https://doi.org/10.1099/vir.0.027870-0
/content/journal/jgv/10.1099/vir.0.027870-0
/content/journal/jgv/10.1099/vir.0.027870-0
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