RNA sequence determinants of a coupled termination-reinitiation strategy for downstream open reading frame translation in Helminthosporium victoriae virus 190S and other victoriviruses (family Totiviridae)

Journal of Virology

Volumn 85, Issue 14, 2011, Pages 7343-7352

  Li, Hua ^a   Havens, Wendy M ^a   Nibert, Max L ^b   Ghabrial, Said A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED RNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; COUPLED TERMINATION REINITIATION; HELMINTHOSPORIUM VICTORIAE VIRUS; NONHUMAN; NUCLEOTIDE REPEAT; OPEN READING FRAME; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSLATION; SEQUENCE HOMOLOGY; SIGNAL DETECTION; STOP CODON; STRUCTURE ANALYSIS; TETRANUCLEOTIDE REPEAT; TOTIVIRIDAE; TRANSCRIPTION INITIATION; TRINUCLEOTIDE REPEAT; VIRUS TRANSCRIPTION;

BASE SEQUENCE; BLOTTING, WESTERN; CODON, TERMINATOR; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; TERMINATOR REGIONS, GENETIC; TOTIVIRIDAE;

HELMINTHOSPORIUM VICTORIAE VIRUS 190S; MIRIDAE; TOTIVIRIDAE;

EID: 79960383893     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00364-11     Document Type: Article

References (51)

1. Ahmadian, G., J. S. Randhawa, and A. J. Easton. 2000. Expression of the ORF-2 protein of the human respiratory syncytial virus M2 gene is initiated by a ribosomal termination-dependent reinitiation mechanism. EMBO J. 19:2681-2689.
2. Amrani, N., R. Ganesan, S. Kervestin, D. A. Mangus, S. Ghosh, and A. Jacobson. 2004. A faux 3'UTR promotes mRNA decay. Nature 432:112-118.
3. Ballance, D. J. 1986. Sequences important for gene expression in filamentous fungi. Yeast 2:229-236.
4. Castón, J. R., et al. 2006. Three-dimensional structure and stoichiometry of Helmintosporium victoriae 190S totivirus. Virology 347:323-332.
5. Child, S. J., M. K. Miller, and A. P. Geballe. 1999. Translational control by an upstream open reading frame in the HER-2/neu transcript. J. Biol. Chem. 274:24335-24341.
6. Dinman, J. D., T. Icho, and R. B. Wickner. 1991. A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc. Natl. Acad. Sci. U. S. A. 88:174-178.
7. Dinman, J. D., and R. B. Wickner. 1992. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J. Virol. 66:3669-3676.
8. Dreher, T. W., and W. A. Miller. 2006. Translational control in positive strand RNA plant viruses. Virology 344:185-197.
9. Fujimura, T., J. C. Ribas, A. M. Makhov, and R. B. Wickner. 1992. Pol of gag-pol fusion protein required for encapsidation of viral RNA of yeast L-A virus. Nature 359:746-749.
10. Ghabrial, S. A. 2008. Totiviruses, p. 163-174. In B. W. J. Mahy and M. H. V. Van Regenmortel (ed.), Encyclopedia of virology, 3rd ed. Elsevier, Oxford, United Kingdom.
11. Ghabrial, S. A., J. A. Bibb, K. H. Price, W. M. Havens, and J. A. Lesnaw. 1987. The capsid polypeptides of the 190S virus of Helminthosporium victoriae. J. Gen. Virol. 68:1791-1800.
12. Ghabrial, S. A., and W. M. Havens. 1989. Conservative transcription of Helminthosporium victoriae 190S virus double-stranded RNA in vitro. J. Gen. Virol. 70:1025-1035.
13. Ghabrial, S. A., and W. M. Havens. 1992. The Helminthosporium victoriae 190S mycovirus has two forms distinguishable by capsid protein composition and phosphorylation state. Virology 188:657-665.
14. Ghabrial, S. A., and M. L. Nibert. 2009. Victorivirus, a new genus of fungal viruses in the family Totiviridae. Arch. Virol. 154:373-379.
15. Gould, P. S., and A. J. Easton. 2005. Coupled translation of the respiratory syncytial virus M2 open reading frames requires upstream sequences. J. Biol. Chem. 280:21972-21980.
16. Gould, P. S., and A. J. Easton. 2007. Coupled translation of the second open reading frame of M2 mRNA is sequence dependent and differs significantly within the subfamily Pneumovirinae. J. Virol. 81:8488-8496.
17. Guo, L. H., L. Sun, S. Chiba, H. Araki, and N. Suzuki. 2009. Coupled termination/reinitiation for translation of the downstream open reading frame B of the prototypic hypovirus CHV1-EP713. Nucleic Acids Res. 37: 3645-3659.
18. Hellen, C. U., and P. Sarnow. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15:1593-1612.
19. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
20. Horton, R. M., Z. L. Cai, S. N. Ho, and L. R. Pease. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528-535.
21. Horvath, C. M., M. A. Williams, and R. A. Lamb. 1990. Eukaryotic coupled translation of tandem cistrons: identification of the influenza B virus BM2 polypeptide. EMBO J. 9:2639-2647.
22. Huang, C. H., C. L. Lu, and H. T. Chiu. 2005. A heuristic approach for detecting RNA H-type pseudoknots. Bioinformatics 21:3501-3508.
23. Huang, S., and S. A. Ghabrial. 1996. Organization and expression of the double-stranded RNA genome of Helminthosporium victoriae 190S virus, a totivirus infecting a plant pathogenic filamentous fungus. Proc. Natl. Acad. Sci. U. S. A. 93:12541-12546.
24. Huang, S., A. I. Soldevila, B. A. Webb, and S. A. Ghabrial. 1997. Expression, assembly, and proteolytic processing of Helminthosporium victoriae 190S totivirus capsid protein in insect cells. Virology 234:130-137.
25. Icho, T., and R. B. Wickner. 1989. The double-stranded RNA genome ofyeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames. J. Biol. Chem. 264:6716-6723.
26. Kozak, M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
27. Kozak, M. 2001. Constraints on reinitiation of translation in mammals. Nucleic Acids Res. 29:5226-5232.
28. Kozak, M. 2002. Pushing the limits of the scanning mechanism for initiation of translation. Gene 299:1-34.
29. Liu, H. W., Y. D. Chu, and J. H. Tai. 1998. Characterization of Trichomonas vaginalis virus proteins in the pathogenic protozoan T. vaginalis. Arch. Virol. 143:963-970.
30. Luttermann, C., and G. Meyers. 2007. A bipartite sequence motif induces translation reinitiation in feline calicivirus RNA. J. Biol. Chem. 282:7056-7065.
31. Luttermann, C., and G. Meyers. 2009. The importance of interand intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA. Genes Dev. 23:331-344.
32. Matassova, N. B., A. G. Venjaminova, and G. G. Karpova. 1998. Nucleotides of 18S rRNA surrounding mRNA at the decoding site of translating human ribosome as revealed from the cross-linking data. Biochim. Biophys. Acta 1397:231-239.
33. Meyers, G. 2003. Translation of the minor capsid protein of a calicivirus is initiated by a novel termination-dependent reinitiation mechanism. J. Biol. Chem. 278:34051-34060.
34. Meyers, G. 2007. Characterization of the sequence element directing translation reinitiation in RNA of the calicivirus rabbit hemorrhagic disease virus. J. Virol. 81:9623-9632.
35. Park, C. M., J. D. Lopinski, J. Masuda, T. H. Tzeng, and J. A. Bruenn. 1996. A second double-stranded RNA virus from yeast. Virology 216:451-454.
36. Pisarev, A. V., C. U. Hellen, and T. V. Pestova. 2007. Recycling of eukaryotic posttermination ribosomal complexes. Cell 131:286-299.
37. Pisarev, A. V., et al. 2010. The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell 37:196-210.
38. Plant, E. P., et al. 2003. The 9-Å solution: how mRNA pseudoknots promote efficient programmed -1 ribosomal frameshifting. RNA 9:168-174.
39. Powell, M. L., T. D. Brown, and I. Brierley. 2008. Translational terminationre-initiation in viral systems. Biochem. Soc. Trans. 36:717-722.
40. Powell, M. L., S. Napthine, R. J. Jackson, I. Brierley, and T. D. Brown. 2008. Characterization of the termination-reinitiation strategy employed in the expression of influenza B virus BM2 protein. RNA 14:2394-2406.
41. Pöyry, T. A., A. Kaminski, E. J. Connell, C. S. Fraser, and R. J. Jackson. 2007. The mechanism of an exceptional case of reinitiation after translation of a long ORF reveals why such events do not generally occur in mammalian mRNA translation. Genes Dev. 21:3149-3162.
42. Reeder, J., P. Steffen, and R. Giegerich. 2007. pknotsRG: RNA pseudoknot folding including near-optimal structures and sliding windows. Nucleic Acids Res. 35:W320-W324.
43. Ryabova, L. A., and T. Hohn. 2000. Ribosome shunting in the cauliflower mosaic virus 35S RNA leader is a special case of reinitiation of translation functioning in plant and animal systems. Genes Dev. 14:817-829.
44. Schoch, C. L., et al. 2006. A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 98:1041-1052.
45. Soldevila, A. I., and S. A. Ghabrial. 2000. Expression of the totivirus Helminthosporium victoriae 190S virus RNA-dependent RNA polymerase from its downstream open reading frame in dicistronic constructs. J. Virol. 74: 997-1003.
46. Soldevila, A. I., and S. A. Ghabrial. 2001. A novel alcohol oxidase/RNAbinding protein with affinity for mycovirus double-stranded RNA from the filamentous fungus Helminthosporium (Cochliobolus) victoriae: molecular and functional characterization. J. Biol. Chem. 276:4652-4661.
47. Sperschneider, J., A. Datta, and M. J. Wise. 2011. Heuristic RNA pseudoknot prediction including intramolecular kissing hairpins. RNA 17:27-38.
48. Stuart, K. D., R. Weeks, L. Guilbride, and P. J. Myler. 1992. Molecular organization of Leishmania RNA virus 1. Proc. Natl. Acad. Sci. U. S. A. 89:8596-8600.
49. Wang, A. L., H. M. Yang, K. A. Shen, and C. C. Wang. 1993. Giardiavirus double-stranded RNA genome encodes a capsid polypeptide and a gag-pollike fusion protein by a translation frameshift. Proc. Natl. Acad. Sci. U. S. A. 90:8595-8599.
50. Yoder, O. C. 1988. Cochliobolus heterostrophus, cause of Southern corn leaf blight. Adv. Plant Pathol. 6:93-112.
51. Zhao, T., W. M. Havens, and S. A. Ghabrial. 2006. Disease phenotype of virus-infected Helminthosporium victoriae is independent of overexpression of the cellular alcohol oxidase/RNA-binding protein Hv-p68. Phytopathology 96:326-332.