Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1989 Aug;63(8):3529–3534. doi: 10.1128/jvi.63.8.3529-3534.1989

Transcriptional termination between bovine papillomavirus type 1 (BPV-1) early and late polyadenylation sites blocks late transcription in BPV-1-transformed cells.

C C Baker 1, J S Noe 1
PMCID: PMC250933  PMID: 2545923

Abstract

Bovine papillomavirus type 1 (BPV-1) is a small DNA tumor virus which induces fibropapillomas in cattle and transforms rodent cells in culture. Transcripts are derived from a single strand of the circular viral genome, which has multiple promoters and two polyadenylation sites. In the transformed cell, the first (early) polyadenylation site is utilized exclusively and, therefore, only the early region is expressed. Transcription of the late genes, which requires use of the second (late) polyadenylation site, is seen only in the fully differentiated keratinocytes of the fibropapilloma. In this study, nascent RNA chain analysis of BPV-1-transformed C127 cells was used to demonstrate that at least 90% of the RNA polymerases which transcribe past the early polyadenylation site terminate transcription within the late region before reaching the late polyadenylation site. Therefore, transcription termination is at least partially responsible for the absence of late transcription in the BPV-1-transformed cell and is likely to be an important mechanism for regulation of papillomavirus late transcription during keratinocyte differentiation.

Full text

PDF
3529

Images in this article

3531Image
on p.3531

Selected References

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

  1. Baker C. C., Howley P. M. Differential promoter utilization by the bovine papillomavirus in transformed cells and productively infected wart tissues. EMBO J. 1987 Apr;6(4):1027–1035. doi: 10.1002/j.1460-2075.1987.tb04855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bentley D. L., Groudine M. A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature. 1986 Jun 12;321(6071):702–706. doi: 10.1038/321702a0. [DOI] [PubMed] [Google Scholar]
  3. Burnett S., Moreno-Lopez J., Pettersson U. A novel spontaneous mutation of the bovine papillomavirus-1 genome. Plasmid. 1988 Jul;20(1):61–74. doi: 10.1016/0147-619x(88)90008-x. [DOI] [PubMed] [Google Scholar]
  4. Chen E. Y., Howley P. M., Levinson A. D., Seeburg P. H. The primary structure and genetic organization of the bovine papillomavirus type 1 genome. Nature. 1982 Oct 7;299(5883):529–534. doi: 10.1038/299529a0. [DOI] [PubMed] [Google Scholar]
  5. Choe J., Vaillancourt P., Stenlund A., Botchan M. Bovine papillomavirus type 1 encodes two forms of a transcriptional repressor: structural and functional analysis of new viral cDNAs. J Virol. 1989 Apr;63(4):1743–1755. doi: 10.1128/jvi.63.4.1743-1755.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Citron B., Falck-Pedersen E., Salditt-Georgieff M., Darnell J. E., Jr Transcription termination occurs within a 1000 base pair region downstream from the poly(A) site of the mouse beta-globin (major) gene. Nucleic Acids Res. 1984 Nov 26;12(22):8723–8731. doi: 10.1093/nar/12.22.8723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Connelly S., Manley J. L. A functional mRNA polyadenylation signal is required for transcription termination by RNA polymerase II. Genes Dev. 1988 Apr;2(4):440–452. doi: 10.1101/gad.2.4.440. [DOI] [PubMed] [Google Scholar]
  8. Crum C. P., Nuovo G., Friedman D., Silverstein S. J. Accumulation of RNA homologous to human papillomavirus type 16 open reading frames in genital precancers. J Virol. 1988 Jan;62(1):84–90. doi: 10.1128/jvi.62.1.84-90.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Engel L. W., Heilman C. A., Howley P. M. Transcriptional organization of bovine papillomavirus type 1. J Virol. 1983 Sep;47(3):516–528. doi: 10.1128/jvi.47.3.516-528.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Falck-Pedersen E., Logan J., Shenk T., Darnell J. E., Jr Transcription termination within the E1A gene of adenovirus induced by insertion of the mouse beta-major globin terminator element. Cell. 1985 Apr;40(4):897–905. doi: 10.1016/0092-8674(85)90349-6. [DOI] [PubMed] [Google Scholar]
  11. Frayne E. G., Leys E. J., Crouse G. F., Hook A. G., Kellems R. E. Transcription of the mouse dihydrofolate reductase gene proceeds unabated through seven polyadenylation sites and terminates near a region of repeated DNA. Mol Cell Biol. 1984 Dec;4(12):2921–2924. doi: 10.1128/mcb.4.12.2921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Galli G., Guise J. W., McDevitt M. A., Tucker P. W., Nevins J. R. Relative position and strengths of poly(A) sites as well as transcription termination are critical to membrane versus secreted mu-chain expression during B-cell development. Genes Dev. 1987 Jul;1(5):471–481. doi: 10.1101/gad.1.5.471. [DOI] [PubMed] [Google Scholar]
  13. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  14. Grummt I., Rosenbauer H., Niedermeyer I., Maier U., Ohrlein A. A repeated 18 bp sequence motif in the mouse rDNA spacer mediates binding of a nuclear factor and transcription termination. Cell. 1986 Jun 20;45(6):837–846. doi: 10.1016/0092-8674(86)90558-1. [DOI] [PubMed] [Google Scholar]
  15. Guise J. W., Lim P. L., Yuan D., Tucker P. W. Alternative expression of secreted and membrane forms of immunoglobulin mu-chain is regulated by transcriptional termination in stable plasmacytoma transfectants. J Immunol. 1988 Jun 1;140(11):3988–3994. [PubMed] [Google Scholar]
  16. Hagenbüchle O., Wellauer P. K., Cribbs D. L., Schibler U. Termination of transcription in the mouse alpha-amylase gene Amy-2a occurs at multiple sites downstream of the polyadenylation site. Cell. 1984 Oct;38(3):737–744. doi: 10.1016/0092-8674(84)90269-1. [DOI] [PubMed] [Google Scholar]
  17. Heilman C. A., Engel L., Lowy D. R., Howley P. M. Virus-specific transcription in bovine papillomavirus-transformed mouse cells. Virology. 1982 May;119(1):22–34. doi: 10.1016/0042-6822(82)90061-7. [DOI] [PubMed] [Google Scholar]
  18. Iwamoto S., Eggerding F., Falck-Pederson E., Darnell J. E., Jr Transcription unit mapping in adenovirus: regions of termination. J Virol. 1986 Jul;59(1):112–119. doi: 10.1128/jvi.59.1.112-119.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kao S. Y., Calman A. F., Luciw P. A., Peterlin B. M. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature. 1987 Dec 3;330(6147):489–493. doi: 10.1038/330489a0. [DOI] [PubMed] [Google Scholar]
  20. Kleiner E., Dietrich W., Pfister H. Differential regulation of papilloma virus early gene expression in transformed fibroblasts and carcinoma cell lines. EMBO J. 1986 Aug;5(8):1945–1950. doi: 10.1002/j.1460-2075.1986.tb04448.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lanoix J., Acheson N. H. A rabbit beta-globin polyadenylation signal directs efficient termination of transcription of polyomavirus DNA. EMBO J. 1988 Aug;7(8):2515–2522. doi: 10.1002/j.1460-2075.1988.tb03099.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Law M. F., Lowy D. R., Dvoretzky I., Howley P. M. Mouse cells transformed by bovine papillomavirus contain only extrachromosomal viral DNA sequences. Proc Natl Acad Sci U S A. 1981 May;78(5):2727–2731. doi: 10.1073/pnas.78.5.2727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Logan J., Falck-Pedersen E., Darnell J. E., Jr, Shenk T. A poly(A) addition site and a downstream termination region are required for efficient cessation of transcription by RNA polymerase II in the mouse beta maj-globin gene. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8306–8310. doi: 10.1073/pnas.84.23.8306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lowy D. R., Dvoretzky I., Shober R., Law M. F., Engel L., Howley P. M. In vitro tumorigenic transformation by a defined sub-genomic fragment of bovine papilloma virus DNA. Nature. 1980 Sep 4;287(5777):72–74. doi: 10.1038/287072a0. [DOI] [PubMed] [Google Scholar]
  25. Maderious A., Chen-Kiang S. Pausing and premature termination of human RNA polymerase II during transcription of adenovirus in vivo and in vitro. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5931–5935. doi: 10.1073/pnas.81.19.5931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Manley J. L., Sharp P. A., Gefter M. L. Rna synthesis in isolated nuclei processing of adenovirus serotype 2 late messenger rna precursors. J Mol Biol. 1982 Aug 25;159(4):581–599. doi: 10.1016/0022-2836(82)90102-4. [DOI] [PubMed] [Google Scholar]
  27. Muesing M. A., Smith D. H., Capon D. J. Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell. 1987 Feb 27;48(4):691–701. doi: 10.1016/0092-8674(87)90247-9. [DOI] [PubMed] [Google Scholar]
  28. Nevins J. R., Wilson M. C. Regulation of adenovirus-2 gene expression at the level of transcriptional termination and RNA processing. Nature. 1981 Mar 12;290(5802):113–118. doi: 10.1038/290113a0. [DOI] [PubMed] [Google Scholar]
  29. Pribyl T. M., Martinson H. G. Transcription termination at the chicken beta H-globin gene. Mol Cell Biol. 1988 Dec;8(12):5369–5377. doi: 10.1128/mcb.8.12.5369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Salditt-Georgieff M., Harpold M., Chen-Kiang S., Darnell J. E., Jr The addition of 5' cap structures occurs early in hnRNA synthesis and prematurely terminated molecules are capped. Cell. 1980 Jan;19(1):69–78. doi: 10.1016/0092-8674(80)90389-x. [DOI] [PubMed] [Google Scholar]
  31. Sato K., Ito R., Baek K. H., Agarwal K. A specific DNA sequence controls termination of transcription in the gastrin gene. Mol Cell Biol. 1986 Apr;6(4):1032–1043. doi: 10.1128/mcb.6.4.1032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shaw A. R., Ziff E. B. Transcripts from the adenovirus-2 major late promoter yield a single early family of 3' coterminal mRNAs and five late families. Cell. 1980 Dec;22(3):905–916. doi: 10.1016/0092-8674(80)90568-1. [DOI] [PubMed] [Google Scholar]
  33. Yang Y. C., Okayama H., Howley P. M. Bovine papillomavirus contains multiple transforming genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1030–1034. doi: 10.1073/pnas.82.4.1030. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES