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. 1985 Mar;53(3):998–1000. doi: 10.1128/jvi.53.3.998-1000.1985

Characterization of an endogenous retrovirus-repetitive DNA chimera in the mouse genome.

T G Fanning, D W Morris, R D Cardiff, H D Bradshaw Jr
PMCID: PMC254742  PMID: 2983106

Abstract

We found that an endogenous mouse mammary tumor provirus, GR-MTV-8, is embedded within a member of the BAM HI family of long interspersed repetitive mouse DNAs. GR-MTV-8 appears to be transcriptionally silent at its normal chromosomal position in the mouse genome. The provirus is transcriptionally active, however, when cloned and transfected into mouse cells (Kennedy et al., Nature (London) 295:622-624, 1982). We propose that the transcriptional inactivity of GR-MTV-8 in situ is due to an inhibitory effect, possibly involving DNA methylation, attributable to the flanking BAM HI element.

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Selected References

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

  1. Brown S. D., Dover G. Organization and evolutionary progress of a dispersed repetitive family of sequences in widely separated rodent genomes. J Mol Biol. 1981 Aug 25;150(4):441–466. doi: 10.1016/0022-2836(81)90374-0. [DOI] [PubMed] [Google Scholar]
  2. Chapman V., Forrester L., Sanford J., Hastie N., Rossant J. Cell lineage-specific undermethylation of mouse repetitive DNA. Nature. 1984 Jan 19;307(5948):284–286. doi: 10.1038/307284a0. [DOI] [PubMed] [Google Scholar]
  3. Chumakov I., Stuhlmann H., Harbers K., Jaenisch R. Cloning of two genetically transmitted Moloney leukemia proviral genomes: correlation between biological activity of the cloned DNA and viral genome activation in the animal. J Virol. 1982 Jun;42(3):1088–1098. doi: 10.1128/jvi.42.3.1088-1098.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Cohen J. C., Shank P. R., Morris V. L., Cardiff R., Varmus H. E. Integration of the DNA of mouse mammary tumor virus in virus-infected normal and neoplastic tissue of the mouse. Cell. 1979 Feb;16(2):333–345. doi: 10.1016/0092-8674(79)90010-2. [DOI] [PubMed] [Google Scholar]
  6. Cohen J. C., Varmus H. E. Endogenous mammary tumour virus DNA varies among wild mice and segregates during inbreeding. Nature. 1979 Mar 29;278(5703):418–423. doi: 10.1038/278418a0. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Fanning T. G. Characterization of a highly repetitive family of DNA sequences in the mouse. Nucleic Acids Res. 1982 Aug 25;10(16):5003–5013. doi: 10.1093/nar/10.16.5003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fanning T. G., Puma J. P., Cardiff R. D. Identification and partial characterization of an endogenous form of mouse mammary tumor virus that is transcribed into the virion-associated RNA genome. Nucleic Acids Res. 1980 Dec 11;8(23):5715–5723. doi: 10.1093/nar/8.23.5715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fanning T. G., Puma J. P., Cardiff R. D. Selective amplification of mouse mammary tumor virus in mammary tumors of GR mice. J Virol. 1980 Oct;36(1):109–114. doi: 10.1128/jvi.36.1.109-114.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fanning T. G. Size and structure of the highly repetitive BAM HI element in mice. Nucleic Acids Res. 1983 Aug 11;11(15):5073–5091. doi: 10.1093/nar/11.15.5073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fanning T. G., Vassos A. B., Cardiff R. D. Methylation and amplification of mouse mammary tumor virus DNA in normal, premalignant, and malignant cells of GR/A mice. J Virol. 1982 Mar;41(3):1007–1013. doi: 10.1128/jvi.41.3.1007-1013.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gebhard W., Meitinger T., Höchtl J., Zachau H. G. A new family of interspersed repetitive DNA sequences in the mouse genome. J Mol Biol. 1982 May 25;157(3):453–471. doi: 10.1016/0022-2836(82)90471-5. [DOI] [PubMed] [Google Scholar]
  14. Günzburg W. H., Groner B. The chromosomal integration site determines the tissue-specific methylation of mouse mammary tumour virus proviral genes. EMBO J. 1984 May;3(5):1129–1135. doi: 10.1002/j.1460-2075.1984.tb01941.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Herrlich P., Hynes N. E., Ponta H., Rahmsdorf U., Kennedy N., Groner B. The endogenous proviral mouse mammary tumor virus genes of the GR mouse are not identical and only one corresponds to the exogenous virus. Nucleic Acids Res. 1981 Oct 10;9(19):4981–4995. doi: 10.1093/nar/9.19.4981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hu W. S., Fanning T. G., Cardiff R. D. Mouse mammary tumor virus: specific methylation patterns of proviral DNA in normal mouse tissues. J Virol. 1984 Jan;49(1):66–71. doi: 10.1128/jvi.49.1.66-71.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hynes N. E., Kennedy N., Rahmsdorf U., Groner B. Hormone-responsive expression of an endogenous proviral gene of mouse mammary tumor virus after molecular cloning and gene transfer into cultured cells. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2038–2042. doi: 10.1073/pnas.78.4.2038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hynes N. E., Rahmsdorf U., Kennedy N., Fabiani L., Michalides R., Nusse R., Groner B. Structure, stability, methylation, expression and glucocorticoid induction of endogenous and transfected proviral genes of mouse mammary tumor virus in mouse fibroblasts. Gene. 1981 Dec;15(4):307–317. doi: 10.1016/0378-1119(81)90174-8. [DOI] [PubMed] [Google Scholar]
  19. Jaenisch R., Jähner D. Methylation, expression and chromosomal position of genes in mammals. Biochim Biophys Acta. 1984 May 15;782(1):1–9. doi: 10.1016/0167-4781(84)90099-x. [DOI] [PubMed] [Google Scholar]
  20. Kennedy N., Knedlitschek G., Groner B., Hynes N. E., Herrlich P., Michalides R., van Ooyen A. J. Long terminal repeats of endogenous mouse mammary tumour virus contain a long open reading frame which extends into adjacent sequences. Nature. 1982 Feb 18;295(5850):622–624. doi: 10.1038/295622a0. [DOI] [PubMed] [Google Scholar]
  21. Kuff E. L., Smith L. A., Lueders K. K. Intracisternal A-particle genes in Mus musculus: a conserved family of retrovirus-like elements. Mol Cell Biol. 1981 Mar;1(3):216–227. doi: 10.1128/mcb.1.3.216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Loenen W. A., Brammar W. J. A bacteriophage lambda vector for cloning large DNA fragments made with several restriction enzymes. Gene. 1980 Aug;10(3):249–259. doi: 10.1016/0378-1119(80)90054-2. [DOI] [PubMed] [Google Scholar]
  23. Michalides R., van Nie R., Nusse R., Hynes N. E., Groner B. Mammary tumor induction loci in GR and DBAf mice contain one provirus of the mouse mammary tumor virus. Cell. 1981 Jan;23(1):165–173. doi: 10.1016/0092-8674(81)90281-6. [DOI] [PubMed] [Google Scholar]
  24. Morris V. L., Medeiros E., Ringold G. M., Bishop J. M., Varmus H. E. Comparison of mouse mammary tumor virus-specific DNA in inbred, wild and Asian mice, and in tumors and normal organs from inbred mice. J Mol Biol. 1977 Jul;114(1):73–91. doi: 10.1016/0022-2836(77)90284-4. [DOI] [PubMed] [Google Scholar]
  25. Nusse R., Varmus H. E. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell. 1982 Nov;31(1):99–109. doi: 10.1016/0092-8674(82)90409-3. [DOI] [PubMed] [Google Scholar]
  26. Nusse R., de Moes J., Hilkens J., van Nie R. Localization of a gene for expression of mouse mammary tumor virus antigens in the GR/Mtv-2- mouse strain. J Exp Med. 1980 Sep 1;152(3):712–719. doi: 10.1084/jem.152.3.712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Peters G., Brookes S., Smith R., Dickson C. Tumorigenesis by mouse mammary tumor virus: evidence for a common region for provirus integration in mammary tumors. Cell. 1983 Jun;33(2):369–377. doi: 10.1016/0092-8674(83)90418-x. [DOI] [PubMed] [Google Scholar]
  28. Ringold G. M., Yamamoto K. R., Bishop J. M., Varmus H. E. Glucocorticoid-stimulated accumulation of mouse mammary tumor virus RNA: increased rate of synthesis of viral RNA. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2879–2883. doi: 10.1073/pnas.74.7.2879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sanford J., Forrester L., Chapman V., Chandley A., Hastie N. Methylation patterns of repetitive DNA sequences in germ cells of Mus musculus. Nucleic Acids Res. 1984 Mar 26;12(6):2823–2836. doi: 10.1093/nar/12.6.2823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Singer M. F. Highly repeated sequences in mammalian genomes. Int Rev Cytol. 1982;76:67–112. doi: 10.1016/s0074-7696(08)61789-1. [DOI] [PubMed] [Google Scholar]
  31. Soriano P., Meunier-Rotival M., Bernardi G. The distribution of interspersed repeats is nonuniform and conserved in the mouse and human genomes. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1816–1820. doi: 10.1073/pnas.80.7.1816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Traina V. L., Taylor B. A., Cohen J. C. Genetic mapping of endogenous mouse mammary tumor viruses: locus characterization, segregation, and chromosomal distribution. J Virol. 1981 Dec;40(3):735–744. doi: 10.1128/jvi.40.3.735-744.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Varmus H. E. Form and function of retroviral proviruses. Science. 1982 May 21;216(4548):812–820. doi: 10.1126/science.6177038. [DOI] [PubMed] [Google Scholar]
  34. Varmus H. E., Quintrell N., Medeiros E., Bishop J. M., Nowinski R. C., Sarkar N. H. Transcription of mouse mammary tumor virus genes in tissues from high and low tumor incidence mouse strains. J Mol Biol. 1973 Oct 5;79(4):663–679. doi: 10.1016/0022-2836(73)90070-3. [DOI] [PubMed] [Google Scholar]
  35. Voliva C. F., Jahn C. L., Comer M. B., Hutchison C. A., 3rd, Edgell M. H. The L1Md long interspersed repeat family in the mouse: almost all examples are truncated at one end. Nucleic Acids Res. 1983 Dec 20;11(24):8847–8859. doi: 10.1093/nar/11.24.8847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilson R., Storb U. Association of two different repetitive DNA elements near immunoglobulin light chain genes. Nucleic Acids Res. 1983 Mar 25;11(6):1803–1817. doi: 10.1093/nar/11.6.1803. [DOI] [PMC free article] [PubMed] [Google Scholar]

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