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. 1985 Jul;4(7):1819–1825. doi: 10.1002/j.1460-2075.1985.tb03856.x

The presence of bovine papillomavirus type 4 DNA is not required for the progression to, or the maintenance of, the malignant state in cancers of the alimentary canal in cattle.

M S Campo, M H Moar, M L Sartirana, I M Kennedy, W F Jarrett
PMCID: PMC554423  PMID: 2992946

Abstract

In the Western Highlands of Scotland there is a very high incidence of alimentary cancers in cattle. The carcinomas of the upper alimentary canal are found in association with virus-induced benign papillomas, and transformation of papillomas to carcinomas has been observed. Strong circumstantial evidence suggests that the progression to malignancy is due to the interplay between the virus, bovine papillomavirus type 4 (BPV-4), and carcinogen(s) present in bracken fern, which infests the marginal upland grazing grounds. The carcinomas are often accompanied by adenomas and adenocarcinomas of the lower bowels. To elucidate the role of the virus in the transformation process, we have analysed several malignancies of the alimentary canal, and have detected the viral genome in only one case of transforming papilloma of the oesophagus and one case of carcinoma of the tongue. We conclude that, although required for the induction of papillomas, the presence of the BPV-4 DNA is not necessary for the progression to, or the maintenance of, the transformed state.

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Selected References

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  1. Amtmann E., Müller H., Sauer G. Equine connective tissue tumors contain unintegrated bovine papilloma virus DNA. J Virol. 1980 Sep;35(3):962–964. doi: 10.1128/jvi.35.3.962-964.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boshart M., Gissmann L., Ikenberg H., Kleinheinz A., Scheurlen W., zur Hausen H. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984 May;3(5):1151–1157. doi: 10.1002/j.1460-2075.1984.tb01944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Campo M. S., Coggins L. W. Molecular cloning of bovine papillomavirus genomes and comparison of their sequence homologies by heteroduplex mapping. J Gen Virol. 1982 Dec;63(2):255–264. doi: 10.1099/0022-1317-63-2-255. [DOI] [PubMed] [Google Scholar]
  4. Campo M. S., Moar M. H., Laird H. M., Jarrett W. F. Molecular heterogeneity and lesion site specificity of cutaneous bovine papillomaviruses. Virology. 1981 Aug;113(1):323–335. doi: 10.1016/0042-6822(81)90159-8. [DOI] [PubMed] [Google Scholar]
  5. Campo M. S., Spandidos D. A. Molecularly cloned bovine papillomavirus DNA transforms mouse fibroblasts in vitro. J Gen Virol. 1983 Mar;64(Pt 3):549–557. doi: 10.1099/0022-1317-64-3-549. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Coggins L. W., Hettich I., Smith K. T., Slater A. A., Roe F. A., Pfister H., Campo M. S. The genomes of bovine papillomaviruses types 3 and 4 are colinear. J Gen Virol. 1983 Dec;64(Pt 12):2771–2776. doi: 10.1099/0022-1317-64-12-2771. [DOI] [PubMed] [Google Scholar]
  8. Dürst M., Gissmann L., Ikenberg H., zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812–3815. doi: 10.1073/pnas.80.12.3812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ellis R. W., DeFeo D., Maryak J. M., Young H. A., Shih T. Y., Chang E. H., Lowy D. R., Scolnick E. M. Dual evolutionary origin for the rat genetic sequences of Harvey murine sarcoma virus. J Virol. 1980 Nov;36(2):408–420. doi: 10.1128/jvi.36.2.408-420.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Farber E. The multistep nature of cancer development. Cancer Res. 1984 Oct;44(10):4217–4223. [PubMed] [Google Scholar]
  11. Georges E., Croissant O., Bonneaud N., Orth G. Physical state and transcription of the cottontail rabbit papillomavirus genome in warts and transplantable VX2 and VX7 carcinomas of domestic rabbits. J Virol. 1984 Aug;51(2):530–538. doi: 10.1128/jvi.51.2.530-538.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  14. Jarrett W. F., Campo M. S., Blaxter M. L., O'Neil B. W., Laird H. M., Moar M. H., Sartirana M. L. Alimentary fibropapilloma in cattle: a spontaneous tumor, nonpermissive for papillomavirus replication. J Natl Cancer Inst. 1984 Aug;73(2):499–504. doi: 10.1093/jnci/73.2.499. [DOI] [PubMed] [Google Scholar]
  15. Jarrett W. F., Campo M. S., O'Neil B. W., Laird H. M., Coggins L. W. A novel bovine papillomavirus (BPV-6) causing true epithelial papillomas of the mammary gland skin: a member of a proposed new BPV subgroup. Virology. 1984 Jul 30;136(2):255–264. doi: 10.1016/0042-6822(84)90162-4. [DOI] [PubMed] [Google Scholar]
  16. Jarrett W. F., McNeil P. E., Grimshaw W. T., Selman I. E., McIntyre W. I. High incidence area of cattle cancer with a possible interaction between an environmental carcinogen and a papilloma virus. Nature. 1978 Jul 20;274(5668):215–217. doi: 10.1038/274215a0. [DOI] [PubMed] [Google Scholar]
  17. Jarrett W. F., Murphy J., O'Neil B. W., Laird H. M. Virus-induced papillomas of the alimentary tract of cattle. Int J Cancer. 1978 Sep 15;22(3):323–328. doi: 10.1002/ijc.2910220316. [DOI] [PubMed] [Google Scholar]
  18. Kruijer W., Cooper J. A., Hunter T., Verma I. M. Platelet-derived growth factor induces rapid but transient expression of the c-fos gene and protein. Nature. 1984 Dec 20;312(5996):711–716. doi: 10.1038/312711a0. [DOI] [PubMed] [Google Scholar]
  19. Lancaster W. D. Apparent lack of integration of bovine papillomavirus DNA in virus-induced equine and bovine tumor cells and virus-transformed mouse cells. Virology. 1981 Jan 30;108(2):251–255. doi: 10.1016/0042-6822(81)90433-5. [DOI] [PubMed] [Google Scholar]
  20. Land H., Parada L. F., Weinberg R. A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature. 1983 Aug 18;304(5927):596–602. doi: 10.1038/304596a0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. McCance D. J., Walker P. G., Dyson J. L., Coleman D. V., Singer A. Presence of human papillomavirus DNA sequences in cervical intraepithelial neoplasia. Br Med J (Clin Res Ed) 1983 Sep 17;287(6395):784–788. doi: 10.1136/bmj.287.6395.784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moar M. H., Campo M. S., Laird H. M., Jarrett W. F. Unintegrated viral DNA sequences in a hamster tumor induced by bovine papilloma virus. J Virol. 1981 Sep;39(3):945–949. doi: 10.1128/jvi.39.3.945-949.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moar M. H., Campo M. S., Laird H., Jarrett W. F. Persistence of non-integrated viral DNA in bovine cells transformed in vitro by bovine papillomavirus type 2. Nature. 1981 Oct 29;293(5835):749–751. doi: 10.1038/293749a0. [DOI] [PubMed] [Google Scholar]
  25. Müller R., Bravo R., Burckhardt J., Curran T. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature. 1984 Dec 20;312(5996):716–720. doi: 10.1038/312716a0. [DOI] [PubMed] [Google Scholar]
  26. Ostrow R. S., Bender M., Niimura M., Seki T., Kawashima M., Pass F., Faras A. J. Human papillomavirus DNA in cutaneous primary and metastasized squamous cell carcinomas from patients with epidermodysplasia verruciformis. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1634–1638. doi: 10.1073/pnas.79.5.1634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Parada L. F., Tabin C. J., Shih C., Weinberg R. A. Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature. 1982 Jun 10;297(5866):474–478. doi: 10.1038/297474a0. [DOI] [PubMed] [Google Scholar]
  28. Pfister H. Biology and biochemistry of papillomaviruses. Rev Physiol Biochem Pharmacol. 1984;99:111–181. doi: 10.1007/BFb0027716. [DOI] [PubMed] [Google Scholar]
  29. Pfister H., Fink B., Thomas C. Extrachromosomal bovine papillomavirus type 1 DNA in hamster fibromas and fibrosarcomas. Virology. 1981 Dec;115(2):414–418. doi: 10.1016/0042-6822(81)90125-2. [DOI] [PubMed] [Google Scholar]
  30. Rassoulzadegan M., Cowie A., Carr A., Glaichenhaus N., Kamen R., Cuzin F. The roles of individual polyoma virus early proteins in oncogenic transformation. Nature. 1982 Dec 23;300(5894):713–718. doi: 10.1038/300713a0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Saveria Campo M., Moar M. H., Jarrett W. F., Laird H. M. A new papillomavirus associated with alimentary cancer in cattle. Nature. 1980 Jul 10;286(5769):180–182. doi: 10.1038/286180a0. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Spandidos D. A., Wilkie N. M. Malignant transformation of early passage rodent cells by a single mutated human oncogene. Nature. 1984 Aug 9;310(5977):469–475. doi: 10.1038/310469a0. [DOI] [PubMed] [Google Scholar]
  35. Ushijima J., Matsukawa K., Yuasa A., Okada M. Toxicities of bracken fern in guinea pigs. Nihon Juigaku Zasshi. 1983 Oct;45(5):593–602. doi: 10.1292/jvms1939.45.593. [DOI] [PubMed] [Google Scholar]
  36. Wettstein F. O., Stevens J. G. Variable-sized free episomes of Shope papilloma virus DNA are present in all non-virus-producing neoplasms and integrated episomes are detected in some. Proc Natl Acad Sci U S A. 1982 Feb;79(3):790–794. doi: 10.1073/pnas.79.3.790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wieslander L. A simple method to recover intact high molecular weight RNA and DNA after electrophoretic separation in low gelling temperature agarose gels. Anal Biochem. 1979 Oct 1;98(2):305–309. doi: 10.1016/0003-2697(79)90145-3. [DOI] [PubMed] [Google Scholar]

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