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. 1990 Dec;64(12):6196–6203. doi: 10.1128/jvi.64.12.6196-6203.1990

A novel mechanism for the initiation of Tacaribe arenavirus genome replication.

D Garcin 1, D Kolakofsky 1
PMCID: PMC248794  PMID: 2243392

Abstract

The ends of arenavirus genome and antigenome RNAs are highly conserved and where determined directly, always contain a 3' G (referred to as position +1). However, primers extended to the 5' ends of Tacaribe virus genomes and antigenomes extend to position -1. When genomes and antigenomes are annealed either inter or intramolecularly and treated with RNase A or T1, there appears to be a single unpaired G at the 5' ends of the hybrids. A single extra G is also found by cloning the 5' ends of S antigenomes, and studies with capping enzyme detect (p)ppG at the 5' ends of genome and antigenome chains. A model is proposed in which genome replication initiates with pppGpC to create the nontemplated extra G. In contrast, the nontemplated bases at the 5' ends of the N mRNAs, which extend to positions -1 to -5, were found to be capped and also heterogeneous in sequence.

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Selected References

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  1. Auperin D. D., Compans R. W., Bishop D. H. Nucleotide sequence conservation at the 3' termini of the virion RNA species of New World and Old World arenaviruses. Virology. 1982 Aug;121(1):200–203. doi: 10.1016/0042-6822(82)90130-1. [DOI] [PubMed] [Google Scholar]
  2. Auperin D. D., Romanowski V., Galinski M., Bishop D. H. Sequencing studies of pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA. J Virol. 1984 Dec;52(3):897–904. doi: 10.1128/jvi.52.3.897-904.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Auperin D. D., Sasso D. R., McCormick J. B. Nucleotide sequence of the glycoprotein gene and intergenic region of the Lassa virus S genome RNA. Virology. 1986 Oct 15;154(1):155–167. doi: 10.1016/0042-6822(86)90438-1. [DOI] [PubMed] [Google Scholar]
  4. Banerjee A. K. 5'-terminal cap structure in eucaryotic messenger ribonucleic acids. Microbiol Rev. 1980 Jun;44(2):175–205. doi: 10.1128/mr.44.2.175-205.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bishop D. H., Auperin D. D. Arenavirus gene structure and organization. Curr Top Microbiol Immunol. 1987;133:5–17. doi: 10.1007/978-3-642-71683-6_2. [DOI] [PubMed] [Google Scholar]
  6. Bishop D. H., Gay M. E., Matsuoko Y. Nonviral heterogeneous sequences are present at the 5' ends of one species of snowshoe hare bunyavirus S complementary RNA. Nucleic Acids Res. 1983 Sep 24;11(18):6409–6418. doi: 10.1093/nar/11.18.6409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bouloy M., Pardigon N., Vialat P., Gerbaud S., Girard M. Characterization of the 5' and 3' ends of viral messenger RNAs isolated from BHK21 cells infected with Germiston virus (Bunyavirus). Virology. 1990 Mar;175(1):50–58. doi: 10.1016/0042-6822(90)90185-t. [DOI] [PubMed] [Google Scholar]
  8. Chanda P. K., Banerjee A. K. Identification of promoter-proximal oligonucleotides and a unique dinucleotide, pppGpC, from in vitro transcription products of vesicular stomatitis virus. J Virol. 1981 Jul;39(1):93–103. doi: 10.1128/jvi.39.1.93-103.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Compans R. W., Bishop D. H. Biochemistry of arenaviruses. Curr Top Microbiol Immunol. 1985;114:153–175. doi: 10.1007/978-3-642-70227-3_4. [DOI] [PubMed] [Google Scholar]
  10. Elliott R. M. Molecular biology of the Bunyaviridae. J Gen Virol. 1990 Mar;71(Pt 3):501–522. doi: 10.1099/0022-1317-71-3-501. [DOI] [PubMed] [Google Scholar]
  11. Erdmann V. A., Huysmans E., Vandenberghe A., De Wachter R. Collection of published 5S and 5.8S ribosomal RNA sequences. Nucleic Acids Res. 1983 Jan 11;11(1):r105–r133. [PMC free article] [PubMed] [Google Scholar]
  12. Franze-Fernández M. T., Zetina C., Iapalucci S., Lucero M. A., Bouissou C., López R., Rey O., Daheli M., Cohen G. N., Zakin M. M. Molecular structure and early events in the replication of Tacaribe arenavirus S RNA. Virus Res. 1987 Jun;7(4):309–324. doi: 10.1016/0168-1702(87)90045-1. [DOI] [PubMed] [Google Scholar]
  13. Fuller-Pace F. V., Southern P. J. Detection of virus-specific RNA-dependent RNA polymerase activity in extracts from cells infected with lymphocytic choriomeningitis virus: in vitro synthesis of full-length viral RNA species. J Virol. 1989 May;63(5):1938–1944. doi: 10.1128/jvi.63.5.1938-1944.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hacker D., Raju R., Kolakofsky D. La Crosse virus nucleocapsid protein controls its own synthesis in mosquito cells by encapsidating its mRNA. J Virol. 1989 Dec;63(12):5166–5174. doi: 10.1128/jvi.63.12.5166-5174.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hacker D., Rochat S., Kolakofsky D. Anti-mRNAs in La Crosse bunyavirus-infected cells. J Virol. 1990 Oct;64(10):5051–5057. doi: 10.1128/jvi.64.10.5051-5057.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Krug R. M., Broni B. A., LaFiandra A. J., Morgan M. A., Shatkin A. J. Priming and inhibitory activities of RNAs for the influenza viral transcriptase do not require base pairing with the virion template RNA. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5874–5878. doi: 10.1073/pnas.77.10.5874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krug R. M. Priming of influenza viral RNA transcription by capped heterologous RNAs. Curr Top Microbiol Immunol. 1981;93:125–149. doi: 10.1007/978-3-642-68123-3_6. [DOI] [PubMed] [Google Scholar]
  18. Leung W. C., Ghosh H. P., Rawls W. E. Strandedness of Pichinde virus RNA. J Virol. 1977 Apr;22(1):235–237. doi: 10.1128/jvi.22.1.235-237.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loh E. Y., Elliott J. F., Cwirla S., Lanier L. L., Davis M. M. Polymerase chain reaction with single-sided specificity: analysis of T cell receptor delta chain. Science. 1989 Jan 13;243(4888):217–220. doi: 10.1126/science.2463672. [DOI] [PubMed] [Google Scholar]
  20. Moss B. Utilization of the guanylyltransferase and methyltransferases of vaccinia virus to modify and identify the 5'-terminals of heterologous RNA species. Biochem Biophys Res Commun. 1977 Jan 24;74(2):374–383. doi: 10.1016/0006-291x(77)90314-x. [DOI] [PubMed] [Google Scholar]
  21. Palmer E. L., Obijeski J. F., Webb P. A., Johnson K. M. The circular, segmented nucleocapsid of an arenavirus-Tacaribe virus. J Gen Virol. 1977 Sep;36(3):541–545. doi: 10.1099/0022-1317-36-3-541. [DOI] [PubMed] [Google Scholar]
  22. Patterson J. L., Holloway B., Kolakofsky D. La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonuclease. J Virol. 1984 Oct;52(1):215–222. doi: 10.1128/jvi.52.1.215-222.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Patterson J. L., Kolakofsky D. Characterization of La Crosse virus small-genome transcripts. J Virol. 1984 Mar;49(3):680–685. doi: 10.1128/jvi.49.3.680-685.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Raju R., Raju L., Hacker D., Garcin D., Compans R., Kolakofsky D. Nontemplated bases at the 5' ends of Tacaribe virus mRNAs. Virology. 1990 Jan;174(1):53–59. doi: 10.1016/0042-6822(90)90053-t. [DOI] [PubMed] [Google Scholar]
  25. Salvato M. S., Shimomaye E. M. The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology. 1989 Nov;173(1):1–10. doi: 10.1016/0042-6822(89)90216-x. [DOI] [PubMed] [Google Scholar]
  26. Schwer B., Visca P., Vos J. C., Stunnenberg H. G. Discontinuous transcription or RNA processing of vaccinia virus late messengers results in a 5' poly(A) leader. Cell. 1987 Jul 17;50(2):163–169. doi: 10.1016/0092-8674(87)90212-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shaw M. W., Lamb R. A. A specific sub-set of host-cell mRNAs prime influenza virus mRNA synthesis. Virus Res. 1984 Sep;1(6):455–467. doi: 10.1016/0168-1702(84)90003-0. [DOI] [PubMed] [Google Scholar]
  28. Venkatesan S., Gershowitz A., Moss B. Modification of the 5' end of mRNA. Association of RNA triphosphatase with the RNA guanylyltransferase-RNA (guanine-7-)methyltransferase complex from vaccinia virus. J Biol Chem. 1980 Feb 10;255(3):903–908. [PubMed] [Google Scholar]
  29. Vidal S., Curran J., Kolakofsky D. A stuttering model for paramyxovirus P mRNA editing. EMBO J. 1990 Jun;9(6):2017–2022. doi: 10.1002/j.1460-2075.1990.tb08330.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weber H., Weissmann C. The 3'-termini of bacteriophage Q-beta plus and minus strands. J Mol Biol. 1970 Jul 28;51(2):215–224. doi: 10.1016/0022-2836(70)90138-5. [DOI] [PubMed] [Google Scholar]

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