Vaccinia virus capping enzyme is a transcription initiation factor (original) (raw)

Abstract

It has previously been demonstrated that vaccinia virus capping enzyme is involved both in the formation of a 5' cap structure and in termination of early transcription. Here we show that capping enzyme has an additional activity which is required for transcription of intermediate genes. VITF-A and VITF-B have been defined as two activities which together with RNA polymerase are necessary and sufficient to transcribe intermediate genes in vitro. VITF-A and the viral capping enzyme are shown to copurify to near homogeneity. Direct evidence that capping enzyme is VITF-A was obtained by complementation of a reconstituted transcription system with viral capping enzyme expressed in Escherichia coli. Although capping enzyme is a cofactor in early transcription termination, intermediate transcription is not terminated in response to the early termination signal. Capping enzyme is shown to form a complex with RNA polymerase in the absence of VITF-B. This appears to be a prerequisite for the formation of a stable initiation complex.

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Selected References

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  1. Bateman E., Paule M. R. Regulation of eukaryotic ribosomal RNA transcription by RNA polymerase modification. Cell. 1986 Nov 7;47(3):445–450. doi: 10.1016/0092-8674(86)90601-x. [DOI] [PubMed] [Google Scholar]
  2. Broyles S. S., Yuen L., Shuman S., Moss B. Purification of a factor required for transcription of vaccinia virus early genes. J Biol Chem. 1988 Aug 5;263(22):10754–10760. [PubMed] [Google Scholar]
  3. Bunick D., Zandomeni R., Ackerman S., Weinmann R. Mechanism of RNA polymerase II--specific initiation of transcription in vitro: ATP requirement and uncapped runoff transcripts. Cell. 1982 Jul;29(3):877–886. doi: 10.1016/0092-8674(82)90449-4. [DOI] [PubMed] [Google Scholar]
  4. Coppola J. A., Field A. S., Luse D. S. Promoter-proximal pausing by RNA polymerase II in vitro: transcripts shorter than 20 nucleotides are not capped. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1251–1255. doi: 10.1073/pnas.80.5.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fire A., Samuels M., Sharp P. A. Interactions between RNA polymerase II, factors, and template leading to accurate transcription. J Biol Chem. 1984 Feb 25;259(4):2509–2516. [PubMed] [Google Scholar]
  6. Guo P. X., Moss B. Interaction and mutual stabilization of the two subunits of vaccinia virus mRNA capping enzyme coexpressed in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4023–4027. doi: 10.1073/pnas.87.11.4023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hernandez N., Weiner A. M. Formation of the 3' end of U1 snRNA requires compatible snRNA promoter elements. Cell. 1986 Oct 24;47(2):249–258. doi: 10.1016/0092-8674(86)90447-2. [DOI] [PubMed] [Google Scholar]
  8. Martin S. A., Paoletti E., Moss B. Purification of mRNA guanylyltransferase and mRNA (guanine-7-) methyltransferase from vaccinia virions. J Biol Chem. 1975 Dec 25;250(24):9322–9329. [PubMed] [Google Scholar]
  9. Morgan J. R., Cohen L. K., Roberts B. E. Identification of the DNA sequences encoding the large subunit of the mRNA-capping enzyme of vaccinia virus. J Virol. 1984 Oct;52(1):206–214. doi: 10.1128/jvi.52.1.206-214.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Moss B. Regulation of vaccinia virus transcription. Annu Rev Biochem. 1990;59:661–688. doi: 10.1146/annurev.bi.59.070190.003305. [DOI] [PubMed] [Google Scholar]
  11. Niles E. G., Lee-Chen G. J., Shuman S., Moss B., Broyles S. S. Vaccinia virus gene D12L encodes the small subunit of the viral mRNA capping enzyme. Virology. 1989 Oct;172(2):513–522. doi: 10.1016/0042-6822(89)90194-3. [DOI] [PubMed] [Google Scholar]
  12. Samuels M., Fire A., Sharp P. A. Dinucleotide priming of transcription mediated by RNA polymerase II. J Biol Chem. 1984 Feb 25;259(4):2517–2525. [PubMed] [Google Scholar]
  13. Samuels M., Fire A., Sharp P. A. Separation and characterization of factors mediating accurate transcription by RNA polymerase II. J Biol Chem. 1982 Dec 10;257(23):14419–14427. [PubMed] [Google Scholar]
  14. Sawadogo M., Roeder R. G. Factors involved in specific transcription by human RNA polymerase II: analysis by a rapid and quantitative in vitro assay. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4394–4398. doi: 10.1073/pnas.82.13.4394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schmitt J. F., Stunnenberg H. G. Sequence and transcriptional analysis of the vaccinia virus HindIII I fragment. J Virol. 1988 Jun;62(6):1889–1897. doi: 10.1128/jvi.62.6.1889-1897.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schnapp A., Pfleiderer C., Rosenbauer H., Grummt I. A growth-dependent transcription initiation factor (TIF-IA) interacting with RNA polymerase I regulates mouse ribosomal RNA synthesis. EMBO J. 1990 Sep;9(9):2857–2863. doi: 10.1002/j.1460-2075.1990.tb07475.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Shuman S., Broyles S. S., Moss B. Purification and characterization of a transcription termination factor from vaccinia virions. J Biol Chem. 1987 Sep 5;262(25):12372–12380. [PubMed] [Google Scholar]
  18. Shuman S., Hurwitz J. Mechanism of mRNA capping by vaccinia virus guanylyltransferase: characterization of an enzyme--guanylate intermediate. Proc Natl Acad Sci U S A. 1981 Jan;78(1):187–191. doi: 10.1073/pnas.78.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shuman S., Moss B. Factor-dependent transcription termination by vaccinia virus RNA polymerase. Evidence that the cis-acting termination signal is in nascent RNA. J Biol Chem. 1988 May 5;263(13):6220–6225. [PubMed] [Google Scholar]
  20. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  21. Vos J. C., Sasker M., Stunnenberg H. G. Promoter melting by a stage-specific vaccinia virus transcription factor is independent of the presence of RNA polymerase. Cell. 1991 Apr 5;65(1):105–113. doi: 10.1016/0092-8674(91)90412-r. [DOI] [PubMed] [Google Scholar]
  22. Vos J. C., Stunnenberg H. G. Derepression of a novel class of vaccinia virus genes upon DNA replication. EMBO J. 1988 Nov;7(11):3487–3492. doi: 10.1002/j.1460-2075.1988.tb03224.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. de Vegvar H. E., Lund E., Dahlberg J. E. 3' end formation of U1 snRNA precursors is coupled to transcription from snRNA promoters. Cell. 1986 Oct 24;47(2):259–266. doi: 10.1016/0092-8674(86)90448-4. [DOI] [PubMed] [Google Scholar]