Factors Regulating Template Switch in Vitro by Viral RNA-dependent RNA Polymerases: Implications for RNA-RNA Recombination

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2001 Apr 20

PMID 11309487

Citations 55

Authors

M J Kim

C Kao

Affiliations

Soon will be listed here.

Abstract

Copy-choice RNA recombination occurs during viral RNA synthesis when the viral transcription complex switches templates. We demonstrate that RNA-dependent RNA polymerase from bovine viral diarrhea virus and the replicases from three plant-infecting RNA viruses can produce easily detectable recombination products in vitro by switching templates during elongative RNA synthesis. Template sequence and/or structure, and NTP availability affected the frequency of template switch by the transcription complex. Our results provide biochemical support for copy-choice recombination and establish assays for mechanistic analyses of intermolecular RNA recombination in vitro.

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References

ANDERSON J, Teufel 2nd R, Yin P, Hu W . Correlated template-switching events during minus-strand DNA synthesis: a mechanism for high negative interference during retroviral recombination. J Virol. 1998; 72(2):1186-94. PMC: 124595. DOI: 10.1128/JVI.72.2.1186-1194.1998. View

Nagy P, Bujarski J . Silencing homologous RNA recombination hot spots with GC-rich sequences in brome mosaic virus. J Virol. 1998; 72(2):1122-30. PMC: 124586. DOI: 10.1128/JVI.72.2.1122-1130.1998. View

Mooney R, Artsimovitch I, Landick R . Information processing by RNA polymerase: recognition of regulatory signals during RNA chain elongation. J Bacteriol. 1998; 180(13):3265-75. PMC: 107278. DOI: 10.1128/JB.180.13.3265-3275.1998. View

Murthy V, Meijer W, Blanco L, Salas M . DNA polymerase template switching at specific sites on the phi29 genome causes the in vivo accumulation of subgenomic phi29 DNA molecules. Mol Microbiol. 1998; 29(3):787-98. DOI: 10.1046/j.1365-2958.1998.00972.x. View

Figlerowicz M, Nagy P, Tang N, Kao C, Bujarski J . Mutations in the N terminus of the brome mosaic virus polymerase affect genetic RNA-RNA recombination. J Virol. 1998; 72(11):9192-200. PMC: 110338. DOI: 10.1128/JVI.72.11.9192-9200.1998. View

Zhong W, Gutshall L, Del Vecchio A . Identification and characterization of an RNA-dependent RNA polymerase activity within the nonstructural protein 5B region of bovine viral diarrhea virus. J Virol. 1998; 72(11):9365-9. PMC: 110362. DOI: 10.1128/JVI.72.11.9365-9369.1998. View

Adkins S, Kao C . Subgenomic RNA promoters dictate the mode of recognition by bromoviral RNA-dependent RNA polymerases. Virology. 1999; 252(1):1-8. DOI: 10.1006/viro.1998.9449. View

Arnold J, Cameron C . Poliovirus RNA-dependent RNA polymerase (3Dpol) is sufficient for template switching in vitro. J Biol Chem. 1999; 274(5):2706-16. DOI: 10.1074/jbc.274.5.2706. View

Kao C, Del Vecchio A, Zhong W . De novo initiation of RNA synthesis by a recombinant flaviviridae RNA-dependent RNA polymerase. Virology. 1999; 253(1):1-7. DOI: 10.1006/viro.1998.9517. View

10.

Nagy P, Ogiela C, Bujarski J . Mapping sequences active in homologous RNA recombination in brome mosaic virus: prediction of recombination hot spots. Virology. 1999; 254(1):92-104. DOI: 10.1006/viro.1998.9545. View

11.

Lohmann V, Overton H, Bartenschlager R . Selective stimulation of hepatitis C virus and pestivirus NS5B RNA polymerase activity by GTP. J Biol Chem. 1999; 274(16):10807-15. DOI: 10.1074/jbc.274.16.10807. View

12.

Nagy P, Pogany J, Simon A . RNA elements required for RNA recombination function as replication enhancers in vitro and in vivo in a plus-strand RNA virus. EMBO J. 1999; 18(20):5653-65. PMC: 1171632. DOI: 10.1093/emboj/18.20.5653. View

13.

Jarvis T, Kirkegaard K . The polymerase in its labyrinth: mechanisms and implications of RNA recombination. Trends Genet. 1991; 7(6):186-91. PMC: 7134375. DOI: 10.1016/0168-9525(91)90434-r. View

14.

You S, Padmanabhan R . A novel in vitro replication system for Dengue virus. Initiation of RNA synthesis at the 3'-end of exogenous viral RNA templates requires 5'- and 3'-terminal complementary sequence motifs of the viral RNA. J Biol Chem. 1999; 274(47):33714-22. DOI: 10.1074/jbc.274.47.33714. View

15.

Kim C, Kao C, Tinoco Jr I . RNA motifs that determine specificity between a viral replicase and its promoter. Nat Struct Biol. 2000; 7(5):415-23. DOI: 10.1038/75202. View

16.

Cheng Y, Gott J . Transcription and RNA editing in a soluble in vitro system from Physarum mitochondria. Nucleic Acids Res. 2000; 28(19):3695-701. PMC: 110774. DOI: 10.1093/nar/28.19.3695. View

17.

Kim M, Zhong W, Hong Z, Kao C . Template nucleotide moieties required for de novo initiation of RNA synthesis by a recombinant viral RNA-dependent RNA polymerase. J Virol. 2000; 74(22):10312-22. PMC: 110905. DOI: 10.1128/jvi.74.22.10312-10322.2000. View

18.

Sivakumaran K, Bao Y, Roossinck M, Kao C . Recognition of the core RNA promoter for minus-strand RNA synthesis by the replicases of Brome mosaic virus and Cucumber mosaic virus. J Virol. 2000; 74(22):10323-31. PMC: 110906. DOI: 10.1128/jvi.74.22.10323-10331.2000. View

19.

Kao C, Yang X, Kline A, Wang Q, Barket D, Heinz B . Template requirements for RNA synthesis by a recombinant hepatitis C virus RNA-dependent RNA polymerase. J Virol. 2000; 74(23):11121-8. PMC: 113194. DOI: 10.1128/jvi.74.23.11121-11128.2000. View

20.

Young D, Tuschall D, Flanegan J . Poliovirus RNA-dependent RNA polymerase and host cell protein synthesize product RNA twice the size of poliovirion RNA in vitro. J Virol. 1985; 54(2):256-64. PMC: 254792. DOI: 10.1128/JVI.54.2.256-264.1985. View