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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1979 Oct;76(10):4822–4826. doi: 10.1073/pnas.76.10.4822

Integration of bovine leukemia virus DNA in the bovine genome.

R Kettmann, M Meunier-Rotival, J Cortadas, G Cuny, J Ghysdael, M Mammerickx, A Burny, G Bernardi
PMCID: PMC413029  PMID: 228266

Abstract

DNA preparations from circulating leukocytes, lymph node tumors, and spleens of three bovine leukemia virus-infected cattle were fractionated by Cs2SO4/3,6-bis(acetatomercurimethyl)dioxane density gradient centrifugation. Bovine leukemia virus proviral sequences were found in large GC-rich fragments having a buoyant density in CsCl close to 1.708 g/cm3. Provirus integration, therefore, does not take place at random locations in the host genome, but in a specific class of DNA segments. Hybridization of cDNA synthesized on viral RNA to EcoRI and Xba I restriction fragments of the DNA from infected cells showed that: (i) only one copy of proviral DNA is integrated per haploid genome; (ii) different restriction patterns were found in the proviral DNAs present in the genomes of different animals, providing evidence for the existence of several strains or mutants; and (iii) different integration sites for the proviral DNA were found in the genome of different animals and of different infected cells in the same animal. The latter finding strongly suggests a polyclonal origin of bovine leukemia virus-infected cells.

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Selected References

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  1. Benveniste R. E., Todaro G. J. Multiple divergent copies of endogenous C-type virogenes in mammalian cells. Nature. 1974 Nov 8;252(5479):170–173. doi: 10.1038/252170a0. [DOI] [PubMed] [Google Scholar]
  2. Burny A., Bex F., Chantrenne H., Cleuter Y., Dekegel D., Ghysdael J., Kettmann R., Leclercq M., Leunen J., Mammerickx M. Bovine leukemia virus involvement in enzootic bovine leukosis. Adv Cancer Res. 1978;28:251–311. doi: 10.1016/s0065-230x(08)60649-1. [DOI] [PubMed] [Google Scholar]
  3. Callahan R., Lieber M. M., Todaro G. J., Graves D. C., Ferrer J. F. Bovine leukemia virus genes in the DNA of leukemic cattle. Science. 1976 Jun 4;192(4243):1005–1007. doi: 10.1126/science.179141. [DOI] [PubMed] [Google Scholar]
  4. Collins C. J., Parsons J. T. Integration of avian sarcoma virus DNA sequences in transformed mammalian cells. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4301–4305. doi: 10.1073/pnas.74.10.4301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cortadas J., Macaya G., Bernardi G. An analysis of the bovine genome by density gradient centrifugation: fractionation in Cs2SO4/3,6-bis(acetatomercurimethyl)dioxane density gradient. Eur J Biochem. 1977 Jun 1;76(1):13–19. doi: 10.1111/j.1432-1033.1977.tb11565.x. [DOI] [PubMed] [Google Scholar]
  6. Cory S., Adams J. M. A very large repeating unit of mouse DNA containing the 18S, 28S and 5.8S rRNA genes. Cell. 1977 Aug;11(4):795–805. doi: 10.1016/0092-8674(77)90292-6. [DOI] [PubMed] [Google Scholar]
  7. Filipski J., Thiery J. P., Bernardi G. An analysis of the bovine genome by Cs2SO4-Ag density gradient centrifugation. J Mol Biol. 1973 Oct 15;80(1):177–197. doi: 10.1016/0022-2836(73)90240-4. [DOI] [PubMed] [Google Scholar]
  8. Ghysdael J., Kettmann R., Burny A. Translation of bovine leukemia virus virion RNAs in heterologous protein-synthesizing systems. J Virol. 1979 Mar;29(3):1087–1098. doi: 10.1128/jvi.29.3.1087-1098.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hughes S. H., Shank P. R., Spector D. H., Kung H. J., Bishop J. M., Varmus H. E., Vogt P. K., Breitman M. L. Proviruses of avian sarcoma virus are terminally redundant, co-extensive with unintegrated linear DNA and integrated at many sites. Cell. 1978 Dec;15(4):1397–1410. doi: 10.1016/0092-8674(78)90064-8. [DOI] [PubMed] [Google Scholar]
  10. Kettmann R., Portetelle D., Mammerickx M., Cleuter Y., Dekegel D., Galoux M., Ghysdael J., Burny A., Chantrenne H. Bovine leukemia virus: an exogenous RNA oncogenic virus. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1014–1018. doi: 10.1073/pnas.73.4.1014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lebowitz P., Siegel W., Sklar J. Hemophilus aegyptius restriction edonuclease cleavage map of the simian virus 40 genome and its colinear relation with the hemophilus influenzae cleavage map of SV40. J Mol Biol. 1974 Sep 5;88(1):105–123. doi: 10.1016/0022-2836(74)90297-6. [DOI] [PubMed] [Google Scholar]
  12. Macaya G., Cortadas J., Bernardi G. An analysis of the bovine genome by density-gradient centrifugation. Preparation of the dG+dC-rich DNA components. Eur J Biochem. 1978 Mar;84(1):179–188. doi: 10.1111/j.1432-1033.1978.tb12155.x. [DOI] [PubMed] [Google Scholar]
  13. Meunier-Rotival M., Cortadas J., Macaya G., Bernardi G. Isolation and organization of calf ribosomal DNA. Nucleic Acids Res. 1979;6(6):2109–2123. doi: 10.1093/nar/6.6.2109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mintz B. Gene expression in neoplasia and differentiation. Harvey Lect. 1978;71:193–246. [PubMed] [Google Scholar]
  15. Paul P. S., Pomeroy K. A., Castro A. E., Johnson D. W., Muscoplat C. C., Sorensen D. K. Detection of bovine leukemia virus in B-lymphocytes by the syncytia induction assay. J Natl Cancer Inst. 1977 Oct;59(4):1269–1272. doi: 10.1093/jnci/59.4.1269. [DOI] [PubMed] [Google Scholar]
  16. Polisky B., Greene P., Garfin D. E., McCarthy B. J., Goodman H. M., Boyer H. W. Specificity of substrate recognition by the EcoRI restriction endonuclease. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3310–3314. doi: 10.1073/pnas.72.9.3310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Prunell A., Kopecka H., Strauss F., Bernardi G. The mitochondrial genome of wild-type yeast cells. V. Genome evolution. J Mol Biol. 1977 Feb 15;110(1):17–47. doi: 10.1016/s0022-2836(77)80096-x. [DOI] [PubMed] [Google Scholar]
  18. Rice N. R., Simek S., Ryder O. A., Coggins L. Detection of proviral DNA in horse cells infected with equine infectious anemia virus. J Virol. 1978 Jun;26(3):577–583. doi: 10.1128/jvi.26.3.577-583.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Sabran J. L., Hsu T. W., Yeater C., Kaji A., Mason W. S., Taylor J. M. Analysis of integrated avian RNA tumor virus DNA in transformed chicken, duck and quail fibroblasts. J Virol. 1979 Jan;29(1):170–178. doi: 10.1128/jvi.29.1.170-178.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Steffen D., Weinberg R. A. The integrated genome of murine leukemia virus. Cell. 1978 Nov;15(3):1003–1010. doi: 10.1016/0092-8674(78)90284-2. [DOI] [PubMed] [Google Scholar]
  22. Tal J., Fujita D. J., Kawai S., Varmus H. E., Bishop J. M. Purification of DNA complementary to the env gene of avian sarcoma virus and analysis of relationships among the env genes of avian leukosis-sarcoma viruses. J Virol. 1977 Feb;21(2):497–505. doi: 10.1128/jvi.21.2.497-505.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wang L. H., Duesberg P., Mellon P., Vogt P. K. Distribution of envelope-specific and sarcoma-specific nucleotide sequences from different parents in the RNAs of avian tumor virus recombinants. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1073–1077. doi: 10.1073/pnas.73.4.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]

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