1887

Abstract

Positive-stranded RNA viruses include important human, animal and plant pathogens. Their genomes are able to fold into complex structures stabilized by base pairing between individual nucleotides, many of which are highly conserved and have essential functions during virus replication. With new studies and technological advances the diversity of roles, mechanisms and interactions in which such structured viral RNA functions is becoming increasingly clear. It is also evident that many RNA structures do not function as discrete elements but through mechanisms involving multiple, long-range and often dynamic RNARNA interactions. Through a range of examples and recent advances, this review illustrates the diverse roles and mechanisms of structured viral RNA during the replication of positive-stranded RNA viruses infecting humans and animals.

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2015-07-01
2019-12-15
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References

  1. Alvarez D. E., De Lella Ezcurra A. L., Fucito S., Gamarnik A. V.. 2005; a. Role of RNA structures present at the 3UTR of dengue virus on translation, RNA synthesis, and viral replication. . Virology 339:, 200– 212. [CrossRef] [PubMed]
    [Google Scholar]
  2. Alvarez D. E., Lodeiro M. F., Luduea S. J., Pietrasanta L. I., Gamarnik A. V.. 2005; b. Long-range RNA-RNA interactions circularize the dengue virus genome. . J Virol 79:, 6631– 6643. [CrossRef] [PubMed]
    [Google Scholar]
  3. Atkinson N. J., Witteveldt J., Evans D. J., Simmonds P.. 2014; . The influence of CpG and UpA dinucleotide frequencies on RNA virus replication and characterization of the innate cellular pathways underlying virus attenuation and enhanced replication. . Nucleic Acids Res 42:, 4527– 4545. [CrossRef] [PubMed]
    [Google Scholar]
  4. Burrill C. P., Westesson O., Schulte M. B., Strings V. R., Segal M., Andino R.. 2013; . Global RNA structure analysis of poliovirus identifies a conserved RNA structure involved in viral replication and infectivity. . J Virol 87:, 11670– 11683. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chapman E. G., Costantino D. A., Rabe J. L., Moon S. L., Wilusz J., Nix J. C., Kieft J. S.. 2014; . The structural basis of pathogenic subgenomic flavivirus RNA sfRNA production. . Science 344:, 307– 310. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chase A. J., Daijogo S., Semler B. L.. 2014; . Inhibition of poliovirus-induced cleavage of cellular protein PCBP2 reduces the levels of viral RNA replication. . J Virol 88:, 3192– 3201. [CrossRef] [PubMed]
    [Google Scholar]
  7. Diviney S., Tuplin A., Struthers M., Armstrong V., Elliott R. M., Simmonds P., Evans D. J.. 2008; . A hepatitis C virus cis-acting replication element forms a long-range RNA-RNA interaction with upstream RNA sequences in NS5B. . J Virol 82:, 9008– 9022. [CrossRef] [PubMed]
    [Google Scholar]
  8. Fayzulin R., Frolov I.. 2004; . Changes of the secondary structure of the 5 end of the Sindbis virus genome inhibit virus growth in mosquito cells and lead to accumulation of adaptive mutations. . J Virol 78:, 4953– 4964. [CrossRef] [PubMed]
    [Google Scholar]
  9. Filomatori C. V., Lodeiro M. F., Alvarez D. E., Samsa M. M., Pietrasanta L., Gamarnik A. V.. 2006; . A 5 RNA element promotes dengue virus RNA synthesis on a circular genome. . Genes Dev 20:, 2238– 2249. [CrossRef] [PubMed]
    [Google Scholar]
  10. Filomatori C. V., Iglesias N. G., Villordo S. M., Alvarez D. E., Gamarnik A. V.. 2011; . RNA sequences and structures required for the recruitment and activity of the dengue virus polymerase. . J Biol Chem 286:, 6929– 6939. [CrossRef] [PubMed]
    [Google Scholar]
  11. Firth A. E., Wills N. M., Gesteland R. F., Atkins J. F.. 2011; . Stimulation of stop codon readthrough frequent presence of an extended 3 RNA structural element. . Nucleic Acids Res 39:, 6679– 6691. [CrossRef] [PubMed]
    [Google Scholar]
  12. Friebe P., Boudet J., Simorre J. P., Bartenschlager R.. 2005; . Kissing-loop interaction in the 3 end of the hepatitis C virus genome essential for RNA replication. . J Virol 79:, 380– 392. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gebhard L. G., Filomatori C. V., Gamarnik A. V.. 2011; . Functional RNA elements in the dengue virus genome. . Viruses 3:, 1739– 1756. [CrossRef] [PubMed]
    [Google Scholar]
  14. Giedroc D. P., Cornish P. V.. 2009; . Frameshifting RNA pseudoknots structure and mechanism. . Virus Res 139:, 193– 208. [CrossRef] [PubMed]
    [Google Scholar]
  15. Gorchakov R., Hardy R., Rice C. M., Frolov I.. 2004; . Selection of functional 5 cis-acting elements promoting efficient sindbis virus genome replication. . J Virol 78:, 61– 75. [CrossRef] [PubMed]
    [Google Scholar]
  16. Groat-Carmona A. M., Orozco S., Friebe P., Payne A., Kramer L., Harris E.. 2012; . A novel coding-region RNA element modulates infectious dengue virus particle production in both mammalian and mosquito cells and regulates viral replication in Aedes aegypti mosquitoes. . Virology 432:, 511– 526. [CrossRef] [PubMed]
    [Google Scholar]
  17. Han J. Q., Townsend H. L., Jha B. K., Paranjape J. M., Silverman R. H., Barton D. J.. 2007; . A phylogenetically conserved RNA structure in the poliovirus open reading frame inhibits the antiviral endoribonuclease RNase L. . J Virol 81:, 5561– 5572. [CrossRef] [PubMed]
    [Google Scholar]
  18. Harvey S. C., Zeng Y., Heitsch C. E.. 2013; . The icosahedral RNA virus as a grotto organizing the genome into stalagmites and stalactites. . J Biol Phys 39:, 163– 172. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hyde J. L., Gardner C. L., Kimura T., White J. P., Liu G., Trobaugh D. W., Huang C., Tonelli M., Paessler S. et al. 2014; . A viral RNA structural element alters host recognition of nonself RNA. . Science 343:, 783– 787. [CrossRef] [PubMed]
    [Google Scholar]
  20. Jan E., Sarnow P.. 2002; . Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. . J Mol Biol 324:, 889– 902. [CrossRef] [PubMed]
    [Google Scholar]
  21. Keel A. Y., Jha B. K., Kieft J. S.. 2012; . Structural architecture of an RNA that competitively inhibits RNase L. . RNA 18:, 88– 99. [CrossRef] [PubMed]
    [Google Scholar]
  22. Khromykh A. A., Meka H., Guyatt K. J., Westaway E. G.. 2001; . Essential role of cyclization sequences in flavivirus RNA replication. . J Virol 75:, 6719– 6728. [CrossRef] [PubMed]
    [Google Scholar]
  23. Lee H., Shin H., Wimmer E., Paul A. V.. 2004; . cis-acting RNA signals in the NS5B C-terminal coding sequence of the hepatitis C virus genome. . J Virol 78:, 10865– 10877. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lo M. K., Tilgner M., Bernard K. A., Shi P. Y.. 2003; . Functional analysis of mosquito-borne flavivirus conserved sequence elements within 3 untranslated region of West Nile virus by use of a reporting replicon that differentiates between viral translation and RNA replication. . J Virol 77:, 10004– 10014. [CrossRef] [PubMed]
    [Google Scholar]
  25. Lpez de Quinto S., Siz M., de la Morena D., Sobrino F., Martnez-Salas E.. 2002; . IRES-driven translation is stimulated separately by the FMDV 3-NCR and polyA sequences. . Nucleic Acids Res 30:, 4398– 4405. [CrossRef] [PubMed]
    [Google Scholar]
  26. Manzano M., Reichert E. D., Polo S., Falgout B., Kasprzak W., Shapiro B. A., Padmanabhan R.. 2011; . Identification of cis-acting elements in the 3-untranslated region of the dengue virus type 2 RNA that modulate translation and replication. . J Biol Chem 286:, 22521– 22534. [CrossRef] [PubMed]
    [Google Scholar]
  27. Merino E. J., Wilkinson K. A., Coughlan J. L., Weeks K. M.. 2005; . RNA structure analysis at single nucleotide resolution by selective 2-hydroxyl acylation and primer extension SHAPE. . J Am Chem Soc 127:, 4223– 4231. [CrossRef] [PubMed]
    [Google Scholar]
  28. Oakland T. E., Haselton K. J., Randall G.. 2013; . EWSR1 binds the hepatitis C virus cis-acting replication element and is required for efficient viral replication. . J Virol 87:, 6625– 6634. [CrossRef] [PubMed]
    [Google Scholar]
  29. Ogram S. A., Flanegan J. B.. 2011; . Non-template functions of viral RNA in picornavirus replication. . Curr Opin Virol 1:, 339– 346. [CrossRef] [PubMed]
    [Google Scholar]
  30. Olsthoorn, R. van Duin, J. 2011. Bacteriophages with ssRNA eLS.
  31. Pathak K. B., Pogany J., Nagy P. D.. 2011; . Non-template functions of the viral RNA in plant RNA virus replication. . Curr Opin Virol 1:, 332– 338. [CrossRef] [PubMed]
    [Google Scholar]
  32. Plant E. P., Dinman J. D.. 2008; . The role of programmed-1 ribosomal frameshifting in coronavirus propagation. . Front Biosci 13:, 4873– 4881. [CrossRef] [PubMed]
    [Google Scholar]
  33. Polacek C., Friebe P., Harris E.. 2009; . PolyA-binding protein binds to the non-polyadenylated 3 untranslated region of dengue virus and modulates translation efficiency. . J Gen Virol 90:, 687– 692. [CrossRef] [PubMed]
    [Google Scholar]
  34. Romero-Lpez C., Berzal-Herranz A.. 2012; . The functional RNA domain 5BSL3.2 within the NS5B coding sequence influences hepatitis C virus IRES-mediated translation. . Cell Mol Life Sci 69:, 103– 113. [CrossRef] [PubMed]
    [Google Scholar]
  35. Schnettler E., Sterken M. G., Leung J. Y., Metz S. W., Geertsema C., Goldbach R. W., Vlak J. M., Kohl A., Khromykh A. A., Pijlman G. P.. 2012; . Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and Mammalian cells. . J Virol 86:, 13486– 13500. [CrossRef] [PubMed]
    [Google Scholar]
  36. Serrano P., Pulido M. R., Siz M., Martnez-Salas E.. 2006; . The 3 end of the foot-and-mouth disease virus genome establishes two distinct long-range RNA-RNA interactions with the 5 end region. . J Gen Virol 87:, 3013– 3022. [CrossRef] [PubMed]
    [Google Scholar]
  37. Simmonds P., Tuplin A., Evans D. J.. 2004; . Detection of genome-scale ordered RNA structure GORS in genomes of positive-stranded RNA viruses Implications for virus evolution and host persistence. . RNA 10:, 1337– 1351. [CrossRef] [PubMed]
    [Google Scholar]
  38. Song Y., Liu Y., Ward C. B., Mueller S., Futcher B., Skiena S., Paul A. V., Wimmer E.. 2012; . Identification of two functionally redundant RNA elements in the coding sequence of poliovirus using computer-generated design. . Proc Natl Acad Sci U S A 109:, 14301– 14307. [CrossRef] [PubMed]
    [Google Scholar]
  39. Strauss E. G., Rice C. M., Strauss J. H.. 1983; . Sequence coding for the alphavirus nonstructural proteins is interrupted by an opal termination codon. . Proc Natl Acad Sci U S A 80:, 5271– 5275. [CrossRef] [PubMed]
    [Google Scholar]
  40. Tuplin A., Struthers M., Simmonds P., Evans D. J.. 2012; . A twist in the tail SHAPE mapping of long-range interactions and structural rearrangements of RNA elements involved in HCV replication. . Nucleic Acids Res 40:, 6908– 6921. [CrossRef] [PubMed]
    [Google Scholar]
  41. Villordo S. M., Gamarnik A. V.. 2009; . Genome cyclization as strategy for flavivirus RNA replication. . Virus Res 139:, 230– 239. [CrossRef] [PubMed]
    [Google Scholar]
  42. Villordo S. M., Gamarnik A. V.. 2013; . Differential RNA sequence requirement for dengue virus replication in mosquito and mammalian cells. . J Virol 87:, 9365– 9372. [CrossRef] [PubMed]
    [Google Scholar]
  43. Villordo S. M., Alvarez D. E., Gamarnik A. V.. 2010; . A balance between circular and linear forms of the dengue virus genome is crucial for viral replication. . RNA 16:, 2325– 2335. [CrossRef] [PubMed]
    [Google Scholar]
  44. Wilkinson K. A., Merino E. J., Weeks K. M.. 2006; . Selective 2-hydroxyl acylation analyzed by primer extension SHAPE quantitative RNA structure analysis at single nucleotide resolution. . Nat Protoc 1:, 1610– 1616. [CrossRef] [PubMed]
    [Google Scholar]
  45. Witteveldt J., Blundell R., Maarleveld J. J., McFadden N., Evans D. J., Simmonds P.. 2014; . The influence of viral RNA secondary structure on interactions with innate host cell defences. . Nucleic Acids Res 42:, 3314– 3329. [CrossRef] [PubMed]
    [Google Scholar]
  46. You S., Stump D. D., Branch A. D., Rice C. M.. 2004; . A cis-acting replication element in the sequence encoding the NS5B RNA-dependent RNA polymerase is required for hepatitis C virus RNA replication. . J Virol 78:, 1352– 1366. [CrossRef] [PubMed]
    [Google Scholar]
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