Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1986 Nov;60(2):635–644. doi: 10.1128/jvi.60.2.635-644.1986

Characterization of a low-molecular-weight virus-associated (VA) RNA encoded by simian adenovirus type 7 which functionally can substitute for adenovirus type 5 VA RNAI.

S Larsson, C Svensson, G Akusjärvi
PMCID: PMC288936  PMID: 3773054

Abstract

Human adenoviruses (Ads), like Ad type 2 (Ad2) and Ad5, encode a low-molecular-weight RNA (designated virus-associated [VA] RNAI) which is required for the efficient translation of viral mRNAs late after infection. We cloned and characterized a VA RNA gene from simian adenovirus type 7 (SA7) which appears to have biological activity analogous to that of Ad2 VA RNAI. Thus, SA7 VA RNA stimulates protein synthesis in a transient expression assay and can also functionally substitute for VA RNAI during lytic growth of human Ad5. The SA7 genome encodes only one VA RNA species, in contrast to human Ad2, which encodes two distinct species. This RNA is transcribed by RNA polymerase III in the rightward direction from a gene located at about coordinate 30 on the viral genome, like its Ad2 counterparts. SA7 VA RNA shows only a limited primary sequence homology with the Ad2 VA RNAs (approximately 55%); the flanking sequences, in fact, are better conserved than the VA RNA gene itself. The predicted secondary structure of SA7 VA RNA is, however, very similar to that of Ad2 VA RNAI, inferring that the double-stranded nature rather than the primary sequence of VA RNA is important for its biological activity.

Full text

PDF
635

Images in this article

636Image
on p.636
636Image
on p.636
639Image
on p.639
640Image
on p.640

Selected References

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

  1. Akusjärvi G., Mathews M. B., Andersson P., Vennström B., Pettersson U. Structure of genes for virus-associated RNAI and RNAII of adenovirus type 2. Proc Natl Acad Sci U S A. 1980 May;77(5):2424–2428. doi: 10.1073/pnas.77.5.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akusjärvi G., Persson H. Controls of RNA splicing and termination in the major late adenovirus transcription unit. Nature. 1981 Jul 30;292(5822):420–426. doi: 10.1038/292420a0. [DOI] [PubMed] [Google Scholar]
  3. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  4. Bhat R. A., Domer P. H., Thimmappaya B. Structural requirements of adenovirus VAI RNA for its translation enhancement function. Mol Cell Biol. 1985 Jan;5(1):187–196. doi: 10.1128/mcb.5.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bhat R. A., Metz B., Thimmappaya B. Organization of the noncontiguous promoter components of adenovirus VAI RNA gene is strikingly similar to that of eucaryotic tRNA genes. Mol Cell Biol. 1983 Nov;3(11):1996–2005. doi: 10.1128/mcb.3.11.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bhat R. A., Thimmappaya B. Adenovirus mutants with DNA sequence perturbations in the intragenic promoter of VAI RNA gene allow the enhanced transcription of VAII RNA gene in HeLa cells. Nucleic Acids Res. 1984 Oct 11;12(19):7377–7388. doi: 10.1093/nar/12.19.7377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bogenhagen D. F., Brown D. D. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell. 1981 Apr;24(1):261–270. doi: 10.1016/0092-8674(81)90522-5. [DOI] [PubMed] [Google Scholar]
  8. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fowlkes D. M., Shenk T. Transcriptional control regions of the adenovirus VAI RNA gene. Cell. 1980 Nov;22(2 Pt 2):405–413. doi: 10.1016/0092-8674(80)90351-7. [DOI] [PubMed] [Google Scholar]
  10. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  12. Guilfoyle R., Weinmann R. Control region for adenovirus VA RNA transcription. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3378–3382. doi: 10.1073/pnas.78.6.3378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  14. Kimelman D., Miller J. S., Porter D., Roberts B. E. E1a regions of the human adenoviruses and of the highly oncogenic simian adenovirus 7 are closely related. J Virol. 1985 Feb;53(2):399–409. doi: 10.1128/jvi.53.2.399-409.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Larsson S., Bellett A., Akusjärvi G. VA RNAs from avian and human adenoviruses: dramatic differences in length, sequence, and gene location. J Virol. 1986 May;58(2):600–609. doi: 10.1128/jvi.58.2.600-609.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lengyel P. Enzymology of interferon action--a short survey. Methods Enzymol. 1981;79(Pt B):135–148. [PubMed] [Google Scholar]
  17. Lewis J. B., Fahnestock M. L., Hardy M. M., Anderson C. W. Presence in infected cells of nonvirion proteins encoded by adenovirus messenger RNAs of the major late transcription regions L0 and L1. Virology. 1985 Jun;143(2):452–466. doi: 10.1016/0042-6822(85)90385-x. [DOI] [PubMed] [Google Scholar]
  18. Linné T., Jörnvall H., Philipson L. Purification and characterization of the phosphorylated DNA-binding protein from adenovirus-type-2-infected cells. Eur J Biochem. 1977 Jun 15;76(2):481–490. doi: 10.1111/j.1432-1033.1977.tb11618.x. [DOI] [PubMed] [Google Scholar]
  19. Mathews M. B. Genes for VA-RNA in adenovirus 2. Cell. 1975 Oct;6(2):223–229. doi: 10.1016/0092-8674(75)90013-6. [DOI] [PubMed] [Google Scholar]
  20. Mathews M. B., Grodzicker T. Virus-associated RNAs of naturally occurring strains and variants of group C adenoviruses. J Virol. 1981 Jun;38(3):849–862. doi: 10.1128/jvi.38.3.849-862.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mathews M. B., Pettersson U. The low molecular weight of RNAs of adenovirus 2-infected cells. J Mol Biol. 1978 Feb 25;119(2):293–328. doi: 10.1016/0022-2836(78)90439-4. [DOI] [PubMed] [Google Scholar]
  22. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  23. Miller J. S., Ricciardi R. P., Roberts B. E., Paterson B. M., Mathews M. B. Arrangement of messenger RNAs and protein coding sequences in the major late transcription unit of adenovirus 2. J Mol Biol. 1980 Oct 5;142(4):455–488. doi: 10.1016/0022-2836(80)90258-2. [DOI] [PubMed] [Google Scholar]
  24. Monstein H. J., Philipson L. The conformation of adenovirus VAI-RNA in solution. Nucleic Acids Res. 1981 Sep 11;9(17):4239–4250. doi: 10.1093/nar/9.17.4239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. O'Malley R. P., Mariano T. M., Siekierka J., Mathews M. B. A mechanism for the control of protein synthesis by adenovirus VA RNAI. Cell. 1986 Feb 14;44(3):391–400. doi: 10.1016/0092-8674(86)90460-5. [DOI] [PubMed] [Google Scholar]
  26. PHILIPSON L. Adenovirus assay by the fluorescent cell-counting procedure. Virology. 1961 Nov;15:263–268. doi: 10.1016/0042-6822(61)90357-9. [DOI] [PubMed] [Google Scholar]
  27. Pettersson U., Philipson L., Höglund S. Structural proteins of adenoviruses. I. Purification and characterization of the adenovirus type 2 hexon antigen. Virology. 1967 Dec;33(4):575–590. doi: 10.1016/0042-6822(67)90057-8. [DOI] [PubMed] [Google Scholar]
  28. Pettersson U., Sambrook J. Amount of viral DNA in the genome of cells transformed by adenovirus type 2. J Mol Biol. 1973 Jan;73(1):125–130. doi: 10.1016/0022-2836(73)90164-2. [DOI] [PubMed] [Google Scholar]
  29. Reich P. R., Forget B. G., Weissman S. M. RNA of low molecular weight in KB cells infected with adenovirus type 2. J Mol Biol. 1966 Jun;17(2):428–439. doi: 10.1016/s0022-2836(66)80153-5. [DOI] [PubMed] [Google Scholar]
  30. Reichel P. A., Merrick W. C., Siekierka J., Mathews M. B. Regulation of a protein synthesis initiation factor by adenovirus virus-associated RNA. Nature. 1985 Jan 17;313(5999):196–200. doi: 10.1038/313196a0. [DOI] [PubMed] [Google Scholar]
  31. Schneider R. J., Safer B., Munemitsu S. M., Samuel C. E., Shenk T. Adenovirus VAI RNA prevents phosphorylation of the eukaryotic initiation factor 2 alpha subunit subsequent to infection. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4321–4325. doi: 10.1073/pnas.82.13.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schneider R. J., Weinberger C., Shenk T. Adenovirus VAI RNA facilitates the initiation of translation in virus-infected cells. Cell. 1984 May;37(1):291–298. doi: 10.1016/0092-8674(84)90325-8. [DOI] [PubMed] [Google Scholar]
  33. Siekierka J., Mariano T. M., Reichel P. A., Mathews M. B. Translational control by adenovirus: lack of virus-associated RNAI during adenovirus infection results in phosphorylation of initiation factor eIF-2 and inhibition of protein synthesis. Proc Natl Acad Sci U S A. 1985 Apr;82(7):1959–1963. doi: 10.1073/pnas.82.7.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smart J. E., Stillman B. W. Adenovirus terminal protein precursor. Partial amino acid sequence and the site of covalent linkage to virus DNA. J Biol Chem. 1982 Nov 25;257(22):13499–13506. [PubMed] [Google Scholar]
  35. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  36. Svensson C., Akusjärvi G. Adenovirus VA RNAI mediates a translational stimulation which is not restricted to the viral mRNAs. EMBO J. 1985 Apr;4(4):957–964. doi: 10.1002/j.1460-2075.1985.tb03724.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Svensson C., Akusjärvi G. Adenovirus VA RNAI: a positive regulator of mRNA translation. Mol Cell Biol. 1984 Apr;4(4):736–742. doi: 10.1128/mcb.4.4.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Svensson C., Akusjärvi G. Defective RNA splicing in the absence of adenovirus-associated RNAI. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4690–4694. doi: 10.1073/pnas.83.13.4690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Svensson C., Pettersson U., Akusjärvi G. Splicing of adenovirus 2 early region 1A mRNAs is non-sequential. J Mol Biol. 1983 Apr 15;165(3):475–495. doi: 10.1016/s0022-2836(83)80214-9. [DOI] [PubMed] [Google Scholar]
  40. Söderlund H., Pettersson U., Vennström B., Philipson L., Mathews M. B. A new species of virus-coded low molecular weight RNA from cells infected with adenovirus type 2. Cell. 1976 Apr;7(4):585–593. doi: 10.1016/0092-8674(76)90209-9. [DOI] [PubMed] [Google Scholar]
  41. Thimmappaya B., Weinberger C., Schneider R. J., Shenk T. Adenovirus VAI RNA is required for efficient translation of viral mRNAs at late times after infection. Cell. 1982 Dec;31(3 Pt 2):543–551. doi: 10.1016/0092-8674(82)90310-5. [DOI] [PubMed] [Google Scholar]
  42. Tikchonenko T. I. Molecular biology of S16 (SA7) and some other simian adenoviruses. Curr Top Microbiol Immunol. 1984;110:169–189. doi: 10.1007/978-3-642-46494-2_6. [DOI] [PubMed] [Google Scholar]
  43. Tolun A., Aleström P., Pettersson U. Sequence of inverted terminal repetitions from different adenoviruses: demonstration of conserved sequences and homology between SA7 termini and SV40 DNA. Cell. 1979 Jul;17(3):705–713. doi: 10.1016/0092-8674(79)90277-0. [DOI] [PubMed] [Google Scholar]
  44. Traboni C., Ciliberto G., Cortese R. A novel method for site-directed mutagenesis: its application to an eukaryotic tRNAPro gene promoter. EMBO J. 1982;1(4):415–420. doi: 10.1002/j.1460-2075.1982.tb01184.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Weinmann R., Brendler T. G., Raskas H. J., Roeder R. G. Low molecular weight viral RNAs transcribed by RNA polymerase III during adenovirus 2 infection. Cell. 1976 Apr;7(4):557–566. doi: 10.1016/0092-8674(76)90206-3. [DOI] [PubMed] [Google Scholar]
  47. Weinmann R., Roeder R. G. Role of DNA-dependent RNA polymerase 3 in the transcription of the tRNA and 5S RNA genes. Proc Natl Acad Sci U S A. 1974 May;71(5):1790–1794. doi: 10.1073/pnas.71.5.1790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wigler M., Pellicer A., Silverstein S., Axel R. Biochemical transfer of single-copy eucaryotic genes using total cellular DNA as donor. Cell. 1978 Jul;14(3):725–731. doi: 10.1016/0092-8674(78)90254-4. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES