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. 1986 Nov;60(2):626–634. doi: 10.1128/jvi.60.2.626-634.1986

Bovine papillomavirus type 1 3' early region transformation and plasmid maintenance functions.

M S Rabson, C Yee, Y C Yang, P M Howley
PMCID: PMC288935  PMID: 3021996

Abstract

We examined bovine papillomavirus type 1 (BPV-1) DNAs mutated in the E2 open reading frame (ORF) to determine their ability (i) to transform C127 cells and (ii) to remain extrachromosomal in transfected cells. Results obtained with deletion mutants and insertion mutants containing a linker with translational termination codons in all possible reading frames indicated that an E2 ORF gene product(s) is necessary for efficient transformation, as well as viral plasmid replication and maintenance in the context of the full BPV-1 genome. Complementation assays in which mutant BPV-1 DNAs were transfected into cell lines expressing some viral functions from integrated BPV-1 cDNAs demonstrated that the E2 ORF product, when provided in trans, could allow BPV-1 E2 mutants to remain extrachromosomal. The E2 function could also augment transformation of some, but not all, BPV-1 E2 mutants, allowing identification of another region of BPV-1 involved in cellular transformation. It is likely that the role of the BPV-1 E2 product(s) in transformation and plasmid maintenance is indirect. A BPV-1 mutant altered in the E5 ORF is transformation defective and unable to replicate as a stable plasmid in C127 cells.

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Selected References

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

  1. Amtmann E., Sauer G. Bovine papilloma virus transcription: polyadenylated RNA species and assessment of the direction of transcription. J Virol. 1982 Jul;43(1):59–66. doi: 10.1128/jvi.43.1.59-66.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Androphy E. J., Schiller J. T., Lowy D. R. Identification of the protein encoded by the E6 transforming gene of bovine papillomavirus. Science. 1985 Oct 25;230(4724):442–445. doi: 10.1126/science.2996134. [DOI] [PubMed] [Google Scholar]
  3. Campo M. S., Spandidos D. A., Lang J., Wilkie N. M. Transcriptional control signals in the genome of bovine papillomavirus type 1. Nature. 1983 May 5;303(5912):77–80. doi: 10.1038/303077a0. [DOI] [PubMed] [Google Scholar]
  4. Colbère-Garapin F., Horodniceanu F., Kourilsky P., Garapin A. C. A new dominant hybrid selective marker for higher eukaryotic cells. J Mol Biol. 1981 Jul 25;150(1):1–14. doi: 10.1016/0022-2836(81)90321-1. [DOI] [PubMed] [Google Scholar]
  5. DiMaio D. Nonsense mutation in open reading frame E2 of bovine papillomavirus DNA. J Virol. 1986 Feb;57(2):475–480. doi: 10.1128/jvi.57.2.475-480.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dvoretzky I., Shober R., Chattopadhyay S. K., Lowy D. R. A quantitative in vitro focus assay for bovine papilloma virus. Virology. 1980 Jun;103(2):369–375. doi: 10.1016/0042-6822(80)90195-6. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Gorman C. M., Howard B. H., Reeves R. Expression of recombinant plasmids in mammalian cells is enhanced by sodium butyrate. Nucleic Acids Res. 1983 Nov 11;11(21):7631–7648. doi: 10.1093/nar/11.21.7631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Groff D. E., Lancaster W. D. Genetic analysis of the 3' early region transformation and replication functions of bovine papillomavirus type 1. Virology. 1986 Apr 15;150(1):221–230. doi: 10.1016/0042-6822(86)90281-3. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Howley P. M., Schenborn E. T., Lund E., Byrne J. C., Dahlberg J. E. The bovine papillomavirus distal "enhancer" is not cis essential for transformation or for plasmid maintenance. Mol Cell Biol. 1985 Nov;5(11):3310–3315. doi: 10.1128/mcb.5.11.3310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lancaster W. D., Olson C. Animal papillomaviruses. Microbiol Rev. 1982 Jun;46(2):191–207. doi: 10.1128/mr.46.2.191-207.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Law M. F., Byrne J. C., Howley P. M. A stable bovine papillomavirus hybrid plasmid that expresses a dominant selective trait. Mol Cell Biol. 1983 Nov;3(11):2110–2115. doi: 10.1128/mcb.3.11.2110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Lusky M., Berg L., Weiher H., Botchan M. Bovine papilloma virus contains an activator of gene expression at the distal end of the early transcription unit. Mol Cell Biol. 1983 Jun;3(6):1108–1122. doi: 10.1128/mcb.3.6.1108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lusky M., Botchan M. R. Characterization of the bovine papilloma virus plasmid maintenance sequences. Cell. 1984 Feb;36(2):391–401. doi: 10.1016/0092-8674(84)90232-0. [DOI] [PubMed] [Google Scholar]
  18. Lusky M., Botchan M. R. Genetic analysis of bovine papillomavirus type 1 trans-acting replication factors. J Virol. 1985 Mar;53(3):955–965. doi: 10.1128/jvi.53.3.955-965.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nakabayashi Y., Chattopadhyay S. K., Lowy D. R. The transforming function of bovine papillomavirus DNA. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5832–5836. doi: 10.1073/pnas.80.19.5832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sarver N., Byrne J. C., Howley P. M. Transformation and replication in mouse cells of a bovine papillomavirus--pML2 plasmid vector that can be rescued in bacteria. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7147–7151. doi: 10.1073/pnas.79.23.7147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sarver N., Rabson M. S., Yang Y. C., Byrne J. C., Howley P. M. Localization and analysis of bovine papillomavirus type 1 transforming functions. J Virol. 1984 Nov;52(2):377–388. doi: 10.1128/jvi.52.2.377-388.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schiller J. T., Vass W. C., Lowy D. R. Identification of a second transforming region in bovine papillomavirus DNA. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7880–7884. doi: 10.1073/pnas.81.24.7880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schiller J. T., Vass W. C., Vousden K. H., Lowy D. R. E5 open reading frame of bovine papillomavirus type 1 encodes a transforming gene. J Virol. 1986 Jan;57(1):1–6. doi: 10.1128/jvi.57.1.1-6.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schlegel R., Wade-Glass M., Rabson M. S., Yang Y. C. The E5 transforming gene of bovine papillomavirus encodes a small, hydrophobic polypeptide. Science. 1986 Jul 25;233(4762):464–467. doi: 10.1126/science.3014660. [DOI] [PubMed] [Google Scholar]
  25. Spalholz B. A., Yang Y. C., Howley P. M. Transactivation of a bovine papilloma virus transcriptional regulatory element by the E2 gene product. Cell. 1985 Aug;42(1):183–191. doi: 10.1016/s0092-8674(85)80114-8. [DOI] [PubMed] [Google Scholar]
  26. Stenlund A., Zabielski J., Ahola H., Moreno-Lopez J., Pettersson U. Messenger RNAs from the transforming region of bovine papilloma virus type I. J Mol Biol. 1985 Apr 20;182(4):541–554. doi: 10.1016/0022-2836(85)90240-2. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Yang Y. C., Spalholz B. A., Rabson M. S., Howley P. M. Dissociation of transforming and trans-activation functions for bovine papillomavirus type 1. Nature. 1985 Dec 12;318(6046):575–577. doi: 10.1038/318575a0. [DOI] [PubMed] [Google Scholar]

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