Characterization of a novel 5′ subgenomic RNA3a derived from RNA3 of brome mosaic bromovirus

Journal of Virology

Volumn 80, Issue 24, 2006, Pages 12357-12366

  Wierzchoslawski, Rafal ^a   Urbanowicz, Anna ^b   Dzianott, Aleksandra ^a   Figlerowicz, Marek ^b   Bujarski, Jozef J ^a,b,c  

^a NORTHERN ILLINOIS UNIVERSITY   (United States)

^b INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; MESSENGER RNA; SINDBIS VIRUS NONSTRUCTURAL PROTEIN 4; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; BROME MOSAIC BROMOVIRUS; BROMOVIRUS; GENE DELETION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; RNA SEQUENCE; RNA SYNTHESIS; VIRION; VIRUS REPLICATION;

BASE PAIRING; BASE SEQUENCE; BROMOVIRUS; CLONING, MOLECULAR; DNA PRIMERS; GENE COMPONENTS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; OLIGODEOXYRIBONUCLEOTIDES; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

BROME MOSAIC VIRUS; BROMOVIRUS; BROMUS; RNA VIRUSES;

EID: 33845463807     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01207-06     Document Type: Article

References (72)

1. Ahlquist, P., R. Dasgupta, and P. Kaesberg. 1984. Nucleotide sequence of the Brome mosaic virus genome and its implications for viral replication. J. Mol. Biol. 172:369-383.
2. Ayllon, M. A., S. Gowda, T. Satyanarayana, and W. O. Dawson. 2004. cis-acting elements at opposite ends of the Citrus tristeza virus genome differ in initiation and termination of subgenomic RNAs. Virology 322:41-50.
3. Baumstark, T., and P. Ahlquist. 2001. The Brome mosaic virus RNA3 intergenic replication enhancer folds to mimic a tRNA TpsiC-stem loop and is modified in vivo. RNA 7:1652-1670.
4. Beelman, C., and R. Parker. 1995. Degradation of mRNA in eukaryotes. Cell 81:179-183.
5. Bruyere, A., M. Wantroba, S. Flasinski, A. Dzianott, and J. J. Bujarski. 2000. Frequent homologous recombination events between molecules of one RNA component in a multipartite RNA virus. J. Virol. 74:4214-4219.
6. Cascone, P. J., C. D. Carpenter, X. H. Li, and A. E. Simon. 1990. Recombination between satellite RNAs of turnip crinkle virus. EMBO J. 9:1709-1715.
7. Cascone, P. J., T. F. Haydar, and A. E. Simon. 1993. Sequences and structures required for recombination between virus-associated RNAs. Science 260:801-805.
8. Chen, J., A. Noueiry, and P. Ahlquist. 2001. Brome mosaic virus protein 1a recruits viral RNA2 to RNA replication through a 5′ proximal RNA2 signal. J. Virol. 75:3207-3219.
9. Chetverin, A. B., D. S. Kopein, H. V. Chetverina, A. A. Demidenko, and V. I. Ugerov. 2005. Viral RNA-directed RNA polymerases use diverse mechanisms to promote recombination between RNA molecules. J. Biol. Chem. 280:8748-8755.
10. Choi, I. R., M. Ostrovsky, G. Zhang, and K. A. White. 2001. Regulatory activity of distal and core RNA elements in tombusvirus subgenomic mRNA2 transcription. J. Biol. Chem. 276:41761-41768.
11. Choi, S.-K., M. Hema, K. Gopinath, J. Santos, and C. Kao. 2004. Replicase-binding sites on plus- and minus-strand Brome mosaic virus RNAs and their roles in RNA replication in plant cells. J. Virol. 78:13420-13429.
12. Choi, Y. G., and A. L. Rao. 2003. Packaging of Brome mosaic virus RNA3 is mediated through a bipartite signal. J. Virol. 77:9750-9757.
13. Dasgupta, R., and P. Kaesberg. 1982. Complete nucleotide sequences of the coat protein messenger RNAs of Brome mosaic virus and cowpea chlorotic mottle virus. Nucleic Acids Res. 10:703-713.
14. Deng, L., and S. Shuman. 1997. Elongation properties of vaccinia virus RNA polymerase: pausing, slippage, 3′ end addition, and termination site choice. Biochemistry 36:15892-15899.
15. Dzianott, A., and J. J. Bujarski. 2004. Infection and RNA recombination of Brome mosaic virus in Arabidopsis thaliana. Virology 318:482-492.
16. Dzianott, A., N. Rauffer-Bruyere, and J. J. Bujarski. 2001. Studies on functional interaction between Brome mosaic virus replicase proteins during RNA recombination, using combined mutants in vivo and in vitro. Virology 289:137-149.
17. Eckerle, L. D., and L. A. Ball. 2002. Replication of the RNA segments of a bipartite viral genome is coordinated by a transactivating subgenomic RNA. Virology 296:165-176.
18. French, R., and P. Ahlquist. 1988. Characterization and engineering of sequences controlling in vivo synthesis of Brome mosaic virus subgenomic RNA. J. Virol. 62:2411-2420.
19. Galiakparov, N., D. E. Goszczynski, X. Che, O. Batuman, M. Bar-Joseph, and M. Mawassi. 2003. Two classes of subgenomic RNA of grapevine virus A produced by internal controller elements. Virology 312:434-448.
20. Gowda, S., M. A. Ayllon, T. Satyanarayana, M. Bar-Joseph, and W. O. Dawson. 2003. Transcription strategy in a Closterovirus: a novel 5′-proximal controller element of Citrus tristeza virus produces 5′- and 3′-terminal subgenomic RNAs and differs from 3′ open reading frame controller elements. J. Virol. 77:340-352.
21. Gray, N. K., and M. W. Hentze. 1994. Regulation of protein synthesis by mRNA structure. Mol. Biol. Rep. 195:195-200.
22. Grdzelishvili, V. Z., H. Garcia-Ruiz, T. Watanabe, and P. Ahlquist. 2005. Mutual interference between genomic RNA replication and subgenomic mRNA transcription in Brome mosaic virus. J. Virol. 79:1438-1451.
23. Guo, L., E. M. Ellen, and W. A. Miller. 2001. Base-pairing between untranslated regions facilitates translation of uncapped, nonpoly(A)denylated viral RNA. Mol. Cell 7:1103-1109.
24. Hasnoot, P. C., P. C. Olsthoorn, and J. F. Bol. 2002. The Brome mosaic virus subgenomic promoter hairpin is structurally similar to the iron-responsive element and functionally equivalent to the minus-strand core promoter stem-loop C. RNA 8:110-112.
25. Hausmann, S., J. P. Jacques, and D. Kolakofsky. 1996. Paramyxovirus RNA editing and the requirement for hexamer genome length. RNA 2:1033-1045.
26. Howard, S. T., C. A. Ray, D. D. Patel, J. B. Antczak, and D. J Pickup. 1999. A 43-nucleotide RNA cis-acting element governs the site-specific formation of the 3′ end of a poxvirus late mRNA. Virology 255:190-204.
27. Jackson, A. O., and B. A. Larkins. 1976. Influence of ionic strength, pH, and chelation of divalent metals on isolation of polyribosomes from tobacco leaves. Plant Physiol. 57:5-10.
28. Janda, M., and P. Ahlquist. 1998. Brome mosaic virus RNA replication protein Ia dramatically increases in vivo stability but not translation of viral genomic RNA3. Proc. Natl. Acad. Sci. USA 95:2227-2232.
29. Janda, M., R. French, and P. Ahlquist. 1987. High efficiency T7 polymerase synthesis of infectious RNA from cloned Brome mosaic virus cDNA and effects of 5′ extensions on the transcripts infectivity. Virology 158:259-262.
30. Jaspars, E. M. 1998. A core promoter hairpin is essential for subgenomic RNA synthesis in alfalfa mosaic alfamovirus and is conserved in other Bromoviridae. Virus Genes 17:233-422.
31. Joshi, P. J., T. W. North, and V. R. Prasad. 2005. Aptamers directed to HIV-1 reverse transcriptase display greater efficacy over small hairpin RNAs targeted to viral RNA in blocking HIV-1 replication. Mol. Ther. 11:677-686.
32. Kao, C. C. 2002. Lessons learned from the core RNA promoters of Brome mosaic virus and cucumber mosaic virus. Mol. Plant Pathol. 3:53-59.
33. Kao, C. C., P. Singh, and D. J. Ecker. 2001. De novo initiation of viral RNA-dependent RNA synthesis. Virology 287:251-260.
34. Kim, K. H., and C. L. Hemenway. 1999. Long-distance RNA-RNA interactions and conserved sequence elements affect potato virus X plus-strand RNA accumulation. RNA 5:636-645.
35. Kroner, P., D. Richards, P. Traynor, and P. Ahlquist. 1989. Defined mutations in a small region of the Brome mosaic virus 2 gene cause diverse temperature-sensitive RNA replication phenotypes. J. Virol. 63:5302-5309.
36. Maia, I. G., K. Seron, A. L. Haenni, and F. Bernardi. 1996. Gene expression from viral RNA genomes. Plant Mol. Biol. 32:367-391.
37. Meyer, S., C. Temme, and E. Wahle. 2004. Messenger RNA turnover in eukaryotes: pathways and enzymes. Crit. Rev. Biochem. Mol. Biol. 39:197-216.
38. Miller, W. A., T. W. Dreher, and T. C. Hall. 1985. Synthesis of Brome mosaic virus subgenomic RNA in vitro by internal initiation on (-)-sense genomic RNA. Nature 313:68-70.
39. Miller, W. A., S. Liu, and R. Becket. 2002. Barley yellow dwarf virus: Luteoviridae or Tombusviridae? Mol. Plant Path. 3:177-183.
40. Nagy, P. D., and J. J. Bujarski. 1992. Genetic recombination in Brome mosaic virus: effect of sequence and replication of RNA on accumulation of recombinants. J. Virol. 66:6824-6828.
41. Nagy, P. D., and J. J. Bujarski. 1996. Homologous RNA recombination in Brome mosaic virus: AU-rich sequences decrease the accuracy of crossovers. J. Virol. 70:415-426.
42. Nagy, P. D., and J. J. Bujarski. 1997. Engineering of homologous recombination hotspots with AU-rich sequences in Brome mosaic virus. J. Virol. 71:3799-3810.
43. Nagy, P. D., and A. E. Simon. 1998. In vitro characterization of late steps of RNA recombination in turnip crinkle virus. II. The role of the priming stem and flanking sequences. Virology 249:393-405.
44. Nagy, P. D., and A. E. Simon. 1998. In vitro characterization of late steps of RNA recombination in turnip crinkle virus. I. Role of motif1-hairpin structure. Virology 249:379-392.
45. Noueiry, A. O., J. Diez, S. P. Falk, J. Chen, and P. Ahlquist. 2003. Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for Brome mosaic virus genomic RNA translation. Mol. Cell. Biol. 23:4094-4106.
46. Pasternak, A. O., E. van den Born, W. J. Spaan, and E. J. Snijder. 2001. Sequence requirements for RNA strand transfer during nidovirus discontinuous subgenomic RNA synthesis. EMBO J. 20:7220-7228.
47. Pathak, V. K., and W. S. Hu. 1997. "Might as well jump!" template switching bt retroviral reverse transcriptase, defective genome formation, and recombination. Semin. Virol. 8:141-159.
48. Pellisier, T., C. Bosquet-Antonelli, L. Lavie, and J. M. Deragon. 2004. Synthesis and processing of tRNA-related SINE transcripts in Arabidopsis thaliana. Nucleic Acids Res. 32:3957-3966.
49. Pierangeli, A., M. Bucci, M. Forzan, P. Pagnotti, M. Equestre, and R. Perez Bercoff. 1999. 'Primer alignment-and-extension': a novel mechanism of viral RNA recombination responsible for the rescue of inactivated poliovirus cDNA clones. J. Gen. Virol. 80:1889-1897.
50. Read, R. L., and C. J. Norbury. 2002. Roles for cytoplasmic polyadenylationin cell cycle regulation. J. Cell. Biochem. 87:258-265.
51. Schmitz, I., and A. L. Rao. 1998. Deletions in the conserved amino-terminal basic arm of cucumber mosaic virus coat protein disrupt virion assembly but do not abolish infectivity and cell-to-cell movement. Virology 248:323-331.
52. Schwartz, M., J. Chen, M. Janda, M. Sullivan, J. den Boon, and P. Ahlquist. 2002. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 9:505-514.
53. Shapka, N., and P. D. Nagy. 2004. The AU-rich RNA recombination hot spot sequence of Brome mosaic virus is functional in tombusviruses: implications for the mechanism of RNA recombination. J. Virol. 78:2288-2300.
54. Sit, T. L., A. A. Vaewhongs, and S. A. Lommel. 1998. RNA-mediated transactivation of transcription from a viral RNA. Science 281:829-832.
55. Smirnygina, E., Y. H. Hsu, N. Chua, and P. Ahlquist. 1994. Second-site mutations in the Brome mosaic virus RNA3 intercistronic region partially suppress a defect in coat protein mRNA transcription. Virology 198:427-436.
56. Stawicki, S. S., and C. C. Kao. 1999. Spatial perturbations within an RNA promoter specifically recognized by a viral RNA-dependent RNA polymerase (RdRP) reveal that RdRp can adjust its promoter binding sites. J. Virol. 73:198-204.
57. Sullivan, M. L., and P. Ahlquist. 1999. A Brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. J. Virol. 73:2622-2632.
58. Suzuki, M., T. Hibi, and C. Masuta. 2003. RNA recombination between cucumoviruses: possible role of predicted stem-loop structures and an internal subgenomic promoter-like motif. Virology 306:77-86.
59. Tanguay, R. L., and D. R. Gallie. 1996. The effect of the length of the 3′-untranslated region on expression in plants. FEBS Lett. 394:285-288.
60. Urbanowicz, A., M. Alejska, P. Formanowicz, J. Blazewicz, M. Figlerowicz, and J. J. Bujarski. 2005. Homologous crossovers among molecules of Brome mosaic bromovirus RNA1 or RNA2 segments in vivo. J. Virol. 79:5732-5742.
61. van den Born, E., C. C. Posthuma, A. P. Gultyaev, and E. J. Nijder. 2005. Discontinuous subgenomic RNA synthesis in arteriviruses is guided by an RNA hairpin structure located in the genomic leader region. J. Virol. 79:6312-6324.
62. van Marle, G., L. C. van Dinten, W. J. Spaan, W. Luytjes, and E. J. Snijder. 1999. Characterization of an equine arteritis virus replicase mutant defective in subgenomic mRNA synthesis. J. Virol. 73:5274-5281.
63. van Vliet, A, L. W., S. L. Smits, P. J. M. Rottier, and R. J. de Groot. 2002. Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO J. 21:6571-6580.
64. Vives, M. C., L. Galipienso, L. Navarro, P. Moreno, and J. Guerri. 2002. Characterization of two kinds of subgenomic RNAs produced by citrus leaf blotch virus. Virology 295:328-336.
65. von Hippel, P. H. 1998. An integrated model of the transcription complex in elongation, termination, and editing. Science 281:660-665.
66. Wielgosz, M. M., and H. V. Huang. 1997. A novel viral RNA species in Sindbis virus-infected cells. J. Virol. 71:9108-9117.
67. Wierzchoslawski, R., and J. J. Bujarski. 2006. An efficient in vitro system of homologous recombination in Brome mosaic bromovirus. J. Virol. 80:6182-6187.
68. Wierzchoslawski, R., A. Dzianott, and J. J. Bujarski. 2004. Dissecting the requirement for subgenomic promoter sequences by RNA recombination of Brome mosaic virus in vivo: evidence for functional separation of transcription and recombination. J. Virol. 78:8552-8564.
69. Wierzchoslawski, R., A. Dzianott, S. Kunimalayan, and J. J. Bujarski. 2003. A transcriptionally active subgenomic promoter supports homologous crossovers in a plus-strand RNA virus. J. Virol. 77:6769-6776.
70. Zanier, K., I. Luyten, C. Crombie, B. Müller, D. Schümperli, J. P. Linge, M. Nilges, and M. Sattlercell. 2002. Cycle regulation of human histone H1 mRNA. RNA 8:29-46.
71. Zhang, C. X., P. J. Cascone, and A. E. Simon. 1991. Recombination between satellite and genomic RNAs of turnip crinkle virus. Virology 184:791-794.
72. Ziebuhr, J. 2005. The coronavirus replicase. Curr. Top. Microbiol. Immunol. 287:57-94.