Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1983 Oct;80(19):5827–5831. doi: 10.1073/pnas.80.19.5827

A host protein (La) binds to a unique species of minus-sense leader RNA during replication of vesicular stomatitis virus.

J Wilusz, M G Kurilla, J D Keene
PMCID: PMC390168  PMID: 6310594

Abstract

Baby hamster kidney cells infected with the minus-strand RNA virus vesicular stomatitis virus (VSV) were found to contain three small viral leader RNA species of the minus sense. The longest minus-strand leader RNA was 54 nucleotides long and was complexed with the host cell La protein that was immunoprecipitated by antisera from patients with systemic lupus erythematosus. The La protein is normally found associated with RNA polymerase III transcripts in their unprocessed form. Shorter minus-strand leader RNA species of 45-48 nucleotides were more abundant but were not associated with the La protein. Unlike the plus-strand leader RNA of VSV, the minus-strand leader RNAs were not detected in the nucleus in any form. The minus-strand leader RNAs accumulated gradually throughout the infection and could not be found in association with the viral nucleocapsid protein. The sequence required for La protein binding on the 54-nucleotide-long minus-strand leader is similar to that at the 3' end of the La protein binding-plus-strand leader RNA and, thus, we propose a role for the La protein in the replication of VSV.

Full text

PDF
5831

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ball L. A., White C. N. Coupled transcription and translation in mammalian and avian cell-free systems. Virology. 1978 Feb;84(2):479–495. doi: 10.1016/0042-6822(78)90264-7. [DOI] [PubMed] [Google Scholar]
  2. Banerjee A. D., Abraham G., Colonno R. J. Vesicular stomatitis virus: mode of transcription. J Gen Virol. 1977 Jan;34(1):1–8. doi: 10.1099/0022-1317-34-1-1. [DOI] [PubMed] [Google Scholar]
  3. Blumberg B. M., Giorgi C., Kolakofsky D. N protein of vesicular stomatitis virus selectively encapsidates leader RNA in vitro. Cell. 1983 Feb;32(2):559–567. doi: 10.1016/0092-8674(83)90475-0. [DOI] [PubMed] [Google Scholar]
  4. Emerson S. U., Dierks P. M., Parsons J. T. In vitro synthesis of a unique RNA species by a T particle of vesicular stomatitis virus. J Virol. 1977 Sep;23(3):708–716. doi: 10.1128/jvi.23.3.708-716.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hashimoto C., Steitz J. A. Sequential association of nucleolar 7-2 RNA with two different autoantigens. J Biol Chem. 1983 Feb 10;258(3):1379–1382. [PubMed] [Google Scholar]
  6. Hendrick J. P., Wolin S. L., Rinke J., Lerner M. R., Steitz J. A. Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells. Mol Cell Biol. 1981 Dec;1(12):1138–1149. doi: 10.1128/mcb.1.12.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Keene J. D., Chien I. M., Lazzarini R. A. Vesicular stomatitis virus defective interfering particle containing a muted internal leader RNA gene. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2090–2094. doi: 10.1073/pnas.78.4.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Keene J. D., Schubert M., Lazzarini R. A., Rosenberg M. Nucleotide sequence homology at the 3' termini of RNA from vesicular stomatitis virus and its defective interfering particles. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3225–3229. doi: 10.1073/pnas.75.7.3225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kurilla M. G., Piwnica-Worms H., Keene J. D. Rapid and transient localization of the leader RNA of vesicular stomatitis virus in the nuclei of infected cells. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5240–5244. doi: 10.1073/pnas.79.17.5240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Leppert M., Kolakofsky D. Effect of defective interfering particles on plus- and minus- strand leader RNAs in vesicular stomatitis virus-infected cells. J Virol. 1980 Sep;35(3):704–709. doi: 10.1128/jvi.35.3.704-709.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Leppert M., Rittenhouse L., Perrault J., Summers D. F., Kolakofsky D. Plus and minus strand leader RNAs in negative strand virus-infected cells. Cell. 1979 Nov;18(3):735–747. doi: 10.1016/0092-8674(79)90127-2. [DOI] [PubMed] [Google Scholar]
  12. Lerner M. R., Andrews N. C., Miller G., Steitz J. A. Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 1981 Feb;78(2):805–809. doi: 10.1073/pnas.78.2.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McGowan J. J., Emerson S. U., Wagner R. R. The plus-strand leader RNA of VSV inhibits DNA-dependent transcription of adenovirus and SV40 genes in a soluble whole-cell extract. Cell. 1982 Feb;28(2):325–333. doi: 10.1016/0092-8674(82)90350-6. [DOI] [PubMed] [Google Scholar]
  14. McGowan J. J., Wagner R. R. Inhibition of cellular DNA synthesis by vesicular stomatitis virus. J Virol. 1981 Apr;38(1):356–367. doi: 10.1128/jvi.38.1.356-367.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Piwnica-Worms H., Keene J. D. Sequential synthesis of small capped RNA transcripts in vitro by vesicular stomatitis virus. Virology. 1983 Feb;125(1):206–218. doi: 10.1016/0042-6822(83)90074-0. [DOI] [PubMed] [Google Scholar]
  16. Pringle C. R. The tdCE and hrCE phenotypes: host range mutants of vesicular stomatitis virus in which polymerase function is affected. Cell. 1978 Oct;15(2):597–606. doi: 10.1016/0092-8674(78)90028-4. [DOI] [PubMed] [Google Scholar]
  17. Rinke J., Steitz J. A. Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La lupus antibodies. Cell. 1982 May;29(1):149–159. doi: 10.1016/0092-8674(82)90099-x. [DOI] [PubMed] [Google Scholar]
  18. Rosa M. D., Gottlieb E., Lerner M. R., Steitz J. A. Striking similarities are exhibited by two small Epstein-Barr virus-encoded ribonucleic acids and the adenovirus-associated ribonucleic acids VAI and VAII. Mol Cell Biol. 1981 Sep;1(9):785–796. doi: 10.1128/mcb.1.9.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schubert M., Keene J. D., Herman R. C., Lazzarini R. A. Site on the vesicular stomatitis virus genome specifying polyadenylation and the end of the L gene mRNA. J Virol. 1980 May;34(2):550–559. doi: 10.1128/jvi.34.2.550-559.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Simonsen C. C., Batt-Humphries S., Summers D. F. RNA synthesis of vesicular stomatitis virus-infected cells: in vivo regulation of replication. J Virol. 1979 Jul;31(1):124–132. doi: 10.1128/jvi.31.1.124-132.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Soria M., Little S. P., Huang A. S. Characterization of vesicular stomatitis virus nucleocapsids. I. Complementary 40 S RNA molecules in nucleocapsids. Virology. 1974 Sep;61(1):270–280. doi: 10.1016/0042-6822(74)90261-x. [DOI] [PubMed] [Google Scholar]
  22. Szilágyi J. F., Pringle C. R. Virion trascriptase activity differences in host range mutants of vesicular stomatitis virus. J Virol. 1975 Oct;16(4):927–936. doi: 10.1128/jvi.16.4.927-936.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Weinberg R. A., Penman S. Small molecular weight monodisperse nuclear RNA. J Mol Biol. 1968 Dec;38(3):289–304. doi: 10.1016/0022-2836(68)90387-2. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES