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. 1986 May;58(2):600–609. doi: 10.1128/jvi.58.2.600-609.1986

VA RNAs from avian and human adenoviruses: dramatic differences in length, sequence, and gene location.

S Larsson, A Bellett, G Akusjärvi
PMCID: PMC252950  PMID: 3009871

Abstract

Human adenoviruses encode low-molecular-weight RNAs, so-called VA RNAs, which are transcribed by RNA polymerase III. These RNAs are required for an efficient translation of viral mRNAs late after infection. The genes for the VA RNAs in the genome of CELO virus were mapped and characterized. The results showed a number of surprising differences between CELO virus and human adenovirus type 2 (Ad2). Thus, the CELO virus genome encoded only one VA RNA species, in contrast to human Ad2, which encoded two distinct species. The VA RNA from CELO virus was much shorter than the Ad2 VA RNAs (90 nucleotides compared with 160 nucleotides), and there existed no detectable primary sequence homology between them. The predicted secondary structure of CELO virus VA RNA was, however, similar to that of the Ad2 VA RNAs, implying that the folding rather than the primary sequence was the important feature for biological activity. CELO VA RNA also stimulated translation in a transient expression assay, as did the Ad2 counterparts, albeit with a much lower efficiency. The location of the gene for CELO VA RNA also differed from all previously characterized serotypes, suggesting that the genome organization of avian and human adenoviruses are different. Finally, termination of CELO VA RNA transcription occurred in a TTATT sequence which is unique as a stop signal for RNA polymerase III transcription.

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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. Aleström P., Stenlund A., Li P., Bellett A., Pettersson U. Sequence homology between avian and human adenoviruses. J Virol. 1982 Apr;42(1):306–310. doi: 10.1128/jvi.42.1.306-310.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aleström P., Stenlund A., Li P., Pettersson U. A common sequence in the inverted terminal repetitions of human and avian adenoviruses. Gene. 1982 May;18(2):193–197. doi: 10.1016/0378-1119(82)90117-2. [DOI] [PubMed] [Google Scholar]
  4. Bellett A. J., Younghusband H. B. Replication of the DNA of chick embryo lethal orphan virus. J Mol Biol. 1972 Dec 30;72(3):691–709. doi: 10.1016/0022-2836(72)90185-4. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. 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]
  9. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  10. Cozzarelli N. R., Gerrard S. P., Schlissel M., Brown D. D., Bogenhagen D. F. Purified RNA polymerase III accurately and efficiently terminates transcription of 5S RNA genes. Cell. 1983 Oct;34(3):829–835. doi: 10.1016/0092-8674(83)90540-8. [DOI] [PubMed] [Google Scholar]
  11. Denisova T. S., Sitnikov B. S., Gibadulin R. A. Izuchenie fragmentatsii DNK ptich'ego adenovirusa CELO s pomoshch'iu spetsificheskikh endonukleaz R. HpaI, R. EcoRI, R. HindIII. Mol Biol (Mosk) 1979 Sep-Oct;13(5):1021–1034. [PubMed] [Google Scholar]
  12. Föhring B., Geis A., Koomey M., Raska K., Jr Adenovirus type 12 VA RNA. I. Synthesis in productive infection and gene mapping. Virology. 1979 Jun;95(2):295–302. doi: 10.1016/0042-6822(79)90485-9. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. Kaufman R. J. Identification of the components necessary for adenovirus translational control and their utilization in cDNA expression vectors. Proc Natl Acad Sci U S A. 1985 Feb;82(3):689–693. doi: 10.1073/pnas.82.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Laver W. G., Younghusband H. B., Wrigley N. G. Purification and properties of chick embryo lethal orphan virus (an avian adenovirus). Virology. 1971 Sep;45(3):598–614. doi: 10.1016/0042-6822(71)90175-9. [DOI] [PubMed] [Google Scholar]
  18. Li P., Bellett A. J., Parish C. R. A comparison of the terminal protein and hexon polypeptides of avian and human adenoviruses. J Gen Virol. 1983 Jun;64(Pt 6):1375–1379. doi: 10.1099/0022-1317-64-6-1375. [DOI] [PubMed] [Google Scholar]
  19. Li P., Bellett A. J., Parish C. R. DNA-binding proteins of chick embryo lethal orphan virus: lack of complementation between early proteins of avian and human adenoviruses. J Gen Virol. 1984 Oct;65(Pt 10):1817–1825. doi: 10.1099/0022-1317-65-10-1817. [DOI] [PubMed] [Google Scholar]
  20. Li P., Bellett A. J., Parish C. R. Structural organization and polypeptide composition of the avian adenovirus core. J Virol. 1984 Nov;52(2):638–649. doi: 10.1128/jvi.52.2.638-649.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Li P., Bellett A. J., Parish C. R. The structural proteins of chick embryo lethal orphan virus (fowl adenovirus type 1). J Gen Virol. 1984 Oct;65(Pt 10):1803–1815. doi: 10.1099/0022-1317-65-10-1803. [DOI] [PubMed] [Google Scholar]
  22. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. 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]
  26. 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]
  27. May J. T., Welsh J. K., Asch B. B., McCormick K. J. Chicken embyro lethal orphan (CELO) virus DNA present in hamster cell lines derived from CELO-induced hepatomas. Intervirology. 1978;9(5):321–324. doi: 10.1159/000148951. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Pettersson U., Philipson L. Location of sequences on the adenovirus genome coding for the 5.5S RNA. Cell. 1975 Sep;6(1):1–4. doi: 10.1016/0092-8674(75)90066-5. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  34. Robinson A. J., Younghusband H. B., Bellett A. J. A circula DNA-protein complex from adenoviruses. Virology. 1973 Nov;56(1):54–69. doi: 10.1016/0042-6822(73)90287-0. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. 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]
  38. 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]
  39. 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]
  40. 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]
  41. 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]
  42. 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]
  43. 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]
  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]
  49. Younghusband H. B., Bellett A. J. Denaturation pattern of the deoxyribonucleic acid from chicken embryo lethal orphan virus. J Virol. 1972 Oct;10(4):855–857. doi: 10.1128/jvi.10.4.855-857.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]

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