Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1980 Dec;36(3):684–691. doi: 10.1128/jvi.36.3.684-691.1980

Integration, expression, and infectivity of exogenously acquired proviruses of Rous-associated virus-O.

N A Jenkins, G M Cooper
PMCID: PMC353696  PMID: 6257920

Abstract

We investigated the integration sites, infectivities, and expression of Rous-associated virus-0 (Rav-0) DNAs in exogenously infected turkey and chicken cells. Restriction endonuclease analyses of the DNAs of RAV-0-infected cells indicated that unique integration sites of RAV-0 DNA were detectable in clones of RAV-0-infected cells but not in mass-infected cell cultures. In addition, the sites of integration of RAV-0 DNA differed in each of the seven clones of RAV-0-infected cells examined. Thus, endogenous RAV-0 proviruses appeared to integrate at multiple sites in cellular DNA, which were distinct from the sites of integration of endogenous RAV-0 genomes. Since exogenous RAV-0 proviruses are expressed at 10(3)- to 10(4)-fold-higher levels and are 10(3)- to 10(4)-fold more infectious in transfection assays than the endogenous RAV-0 genome of uninfected V+ chicken cells, these results are consistent with the hypothesis that transcription of the endogenous RAV-0 genome is regulated by flanking cellular DNA sequences. Although all RAV-0-infected cells contained infectious RAV-0 DNA and produced high titers of RAV-0 compared with uninfected V+ cells, different clones of RAV-0 infected chicken cells differed by as much as 30-fold in their levels of virus production. The infectivity of the DNA of each clone of RAV-0-infected cells correlated with the amount of virus produced by that clone. However, these differences did not appear to be correlated either with the number of exogenous RAV-0 proviruses in different clones or with the infectivity of RAV-0 produced by different clones, indicating that differences either in modification of RAV-0 DNAs or in the cellular sequences flanking exogenous RAV-0 DNAs were responsible for the observed differences in expression and infectivity.

Full text

PDF
684

Images in this article

686Image
on p.686
687Image
on p.687
689Image
on p.689

Selected References

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

  1. Astrin S. M., Crittenden L. B., Buss E. G. Ev 2, a genetic locus containing structural genes for endogenous virus, codes for Rous-associated virus type 0 produced by line 72 chickens. J Virol. 1980 Jan;33(1):250–255. doi: 10.1128/jvi.33.1.250-255.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Astrin S. M. Endogenous viral genes of the White Leghorn chicken: common site of residence and sites associated with specific phenotypes of viral gene expression. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5941–5945. doi: 10.1073/pnas.75.12.5941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Astrin S. M., Robinson H. L., Crittenden L. B., Buss E. G., Wyban J., Hayward W. S. Ten genetic loci in the chicken that contain structural genes for endogenous avian leukosis viruses. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1105–1109. doi: 10.1101/sqb.1980.044.01.119. [DOI] [PubMed] [Google Scholar]
  4. Beug H., Graf T. Isolation of clonal strains of chicken embryo fibroblasts. Exp Cell Res. 1977 Jul;107(2):417–428. doi: 10.1016/0014-4827(77)90363-9. [DOI] [PubMed] [Google Scholar]
  5. Bird A. P., Taggart M. H., Smith B. A. Methylated and unmethylated DNA compartments in the sea urchin genome. Cell. 1979 Aug;17(4):889–901. doi: 10.1016/0092-8674(79)90329-5. [DOI] [PubMed] [Google Scholar]
  6. Coffin J. M., Champion M., Chabot F. Nucleotide sequence relationships between the genomes of an endogenous and an exogenous avian tumor virus. J Virol. 1978 Dec;28(3):972–991. doi: 10.1128/jvi.28.3.972-991.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohen J. C. Methylation of milk-borne and genetically transmitted mouse mammary tumor virus proviral DNA. Cell. 1980 Mar;19(3):653–662. doi: 10.1016/s0092-8674(80)80042-0. [DOI] [PubMed] [Google Scholar]
  8. Cooper G. M., Silverman L. Linkage of the endogenous avian leukosis virus genome of virus-producing chicken cells to inhibitory cellular DNA sequences. Cell. 1978 Oct;15(2):573–577. doi: 10.1016/0092-8674(78)90025-9. [DOI] [PubMed] [Google Scholar]
  9. Cooper G. M., Temin H. M. Infectious rous sarcoma virus and reticuloendotheliosis virus DNAs. J Virol. 1974 Nov;14(5):1132–1141. doi: 10.1128/jvi.14.5.1132-1141.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cooper G. M., Temin H. M. Lack of infectivity of the endogenous avian leukosis virus-related genes in the DNA of uninfected chicken cells. J Virol. 1976 Feb;17(2):422–430. doi: 10.1128/jvi.17.2.422-430.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Copeland N. G., Zelenetz A. D., Cooper G. M. Transformation of NIH/3T3 mouse cells by DNA of Rous sarcoma virus. Cell. 1979 Aug;17(4):993–1002. doi: 10.1016/0092-8674(79)90338-6. [DOI] [PubMed] [Google Scholar]
  12. Crittenden L. B., Motta J. V., Smith E. J. Genetic control of RAV-O production in chickens. Virology. 1977 Jan;76(1):90–97. doi: 10.1016/0042-6822(77)90285-9. [DOI] [PubMed] [Google Scholar]
  13. Crittenden L. B., Smith E. J., Weiss R. A., Sarma P. S. Host gene control of endogenous avian leukosis virus production. Virology. 1974 Jan;57(1):128–138. doi: 10.1016/0042-6822(74)90114-7. [DOI] [PubMed] [Google Scholar]
  14. Frisby D. P., Weiss R. A., Roussel M., Stehelin D. The distribution of endogenous chicken retrovirus sequences in the DNA of galliform birds does not coincide with avian phylogenetic relationships. Cell. 1979 Jul;17(3):623–634. doi: 10.1016/0092-8674(79)90270-8. [DOI] [PubMed] [Google Scholar]
  15. Guntaka R. V., Rao P. Y., Mitsialis S. A., Katz R. Modification of avian sarcoma proviral DNA sequences in nonpermissive XC cells but not in permissive chicken cells. J Virol. 1980 May;34(2):569–572. doi: 10.1128/jvi.34.2.569-572.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hayward W. S., Braverman S. B., Astrin S. M. Transcriptional products and DNA structure of endogenous avian proviruses. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1111–1121. doi: 10.1101/sqb.1980.044.01.120. [DOI] [PubMed] [Google Scholar]
  17. Hayward W. S., Hanafusa H. Independent regulation of endogenous and exogenous avian RNA tumor virus genes. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2259–2263. doi: 10.1073/pnas.73.7.2259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hayward W. S., Hanafusa H. Recombination between endogenous and exogenous RNA tumor virus genes as analyzed by nucleic acid hybridization. J Virol. 1975 Jun;15(6):1367–1377. doi: 10.1128/jvi.15.6.1367-1377.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hughes S. H., Payvar F., Spector D., Schimke R. T., Robinson H. L., Payne G. S., Bishop J. M., Varmus H. E. Heterogeneity of genetic loci in chickens: analysis of endogenous viral and nonviral genes by cleavage of DNA with restriction endonucleases. Cell. 1979 Oct;18(2):347–359. doi: 10.1016/0092-8674(79)90054-0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Humphries E. H., Glover C., Weiss R. A., Arrand J. R. Differences between the endogenous and exogenous DNA sequences of Rous-associated virus-O. Cell. 1979 Nov;18(3):803–815. doi: 10.1016/0092-8674(79)90133-8. [DOI] [PubMed] [Google Scholar]
  22. Keshet E., Temin H. M. Sites of integration of reticuloendotheliosis virus DNA in chicken DNA. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3372–3376. doi: 10.1073/pnas.75.7.3372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Linial M., Neiman P. E. Infection of chick cells by subgroup E viruses. Virology. 1976 Sep;73(2):508–520. doi: 10.1016/0042-6822(76)90412-8. [DOI] [PubMed] [Google Scholar]
  24. McGhee J. D., Ginder G. D. Specific DNA methylation sites in the vicinity of the chicken beta-globin genes. Nature. 1979 Aug 2;280(5721):419–420. doi: 10.1038/280419a0. [DOI] [PubMed] [Google Scholar]
  25. Neiman P. E., Das S., Macdonnell D., McMillin-Helsel C. Organization of shared and unshared sequences in the genomes of chicken endogenous and sarcoma viruses. Cell. 1977 Jun;11(2):321–329. doi: 10.1016/0092-8674(77)90048-4. [DOI] [PubMed] [Google Scholar]
  26. Neiman P. E. Measurement of endogenous leukosis virus nucleotide sequences in the DNA of normal avian embryos by RNA-DNA hybridization. Virology. 1973 May;53(1):196–203. doi: 10.1016/0042-6822(73)90478-9. [DOI] [PubMed] [Google Scholar]
  27. Robinson H. L. Intracellular restriction on the growth of induced subgroup E avian type C viruses in chicken cells. J Virol. 1976 Jun;18(3):856–866. doi: 10.1128/jvi.18.3.856-866.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Robinson H. L., Swanson C. A., Hruska J. F., Crittenden L. B. Production of unique C-type viruses by chicken cells grown in bromodeoxyuridine. Virology. 1976 Jan;69(1):63–74. doi: 10.1016/0042-6822(76)90194-x. [DOI] [PubMed] [Google Scholar]
  29. Roop D. R., Tsai M. J., O'Malley B. W. Definition of the 5' and 3' ends of transcripts of the ovalbumin gene. Cell. 1980 Jan;19(1):63–68. doi: 10.1016/0092-8674(80)90388-8. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Shank P. R., Hughes S. H., Kung H. J., Majors J. E., Quintrell N., Guntaka R. V., Bishop J. M., Varmus H. E. Mapping unintegrated avian sarcoma virus DNA: termini of linear DNA bear 300 nucleotides present once or twice in two species of circular DNA. Cell. 1978 Dec;15(4):1383–1395. doi: 10.1016/0092-8674(78)90063-6. [DOI] [PubMed] [Google Scholar]
  32. Shoyab M., Baluda M. A. Homology between avian oncornavirus RNAs and DNA from several avian species. J Virol. 1975 Dec;16(6):1492–1502. doi: 10.1128/jvi.16.6.1492-1502.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Smith E. J., Crittenden L. B., Brinsfield T. H., Jr Status of the endogenous avian leukosis virus in resistant cells from a producing line. Virology. 1974 Oct;61(2):594–596. doi: 10.1016/0042-6822(74)90293-1. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Vogt P. K., Friis R. R. An avian leukosis virus related to RSV(O): properties and evidence for helper activity. Virology. 1971 Jan;43(1):223–234. doi: 10.1016/0042-6822(71)90240-6. [DOI] [PubMed] [Google Scholar]
  36. Wang S. Y., Hayward W. S., Hanafusa H. Genetic variation in the RNA transcripts of endogenous virus genes in uninfected chicken cells. J Virol. 1977 Oct;24(1):64–73. doi: 10.1128/jvi.24.1.64-73.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. van der Ploeg L. H., Flavell R. A. DNA methylation in the human gamma delta beta-globin locus in erythroid and nonerythroid tissues. Cell. 1980 Apr;19(4):947–958. doi: 10.1016/0092-8674(80)90086-0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES