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. 1982 Jun;42(3):880–888. doi: 10.1128/jvi.42.3.880-888.1982

Conservation of protein coding potential in the long terminal repeats of exogenous and endogenous mouse mammary tumor viruses.

G Peters, R Smith, S Brookes, C Dickson
PMCID: PMC256922  PMID: 6285002

Abstract

In vitro protein synthesis and DNA sequence analysis indicate that mouse mammary tumor virus differs from other well-characterized retroviruses in that the long terminal repeat region of the provirus has the capacity to encode proteins. Different exogenously transmitted mouse mammary tumor virus strains and endogenous proviral units conserved this open reading frame feature in the long terminal repeat despite a variation in nucleotide sequence. The proteins encoded by the different long terminal repeats were clearly related, but showed minor variations in size and tryptic peptide maps. In each case, the largest in vitro product had a molecular weight of about 36,000 to 37,000, suggesting that the open reading frame sequences must extend for approximately 1,000 nucleotides beginning at the extreme 5' end of the long terminal repeat. The fact that the reading frame was conserved among these viruses argues in favor of an in vivo function for the open reading frame protein.

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Selected References

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

  1. Arthur L. O., Lovinger G. G., Schochetman G. Establishment of a C3Hf mammary tumor cell line expressing endogenous mouse mammary tumor virus: antigenic and genetic relationships of this virus with highly oncogenic mouse mammary tumor viruses. J Virol. 1979 Dec;32(3):852–859. doi: 10.1128/jvi.32.3.852-859.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benz E. W., Jr, Wydro R. M., Nadal-Ginard B., Dina D. Moloney murine sarcoma proviral DNA is a transcriptional unit. Nature. 1980 Dec 25;288(5792):665–669. doi: 10.1038/288665a0. [DOI] [PubMed] [Google Scholar]
  3. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bishop J. M. Retroviruses. Annu Rev Biochem. 1978;47:35–88. doi: 10.1146/annurev.bi.47.070178.000343. [DOI] [PubMed] [Google Scholar]
  5. Coffin J. M. Structure, replication, and recombination of retrovirus genomes: some unifying hypotheses. J Gen Virol. 1979 Jan;42(1):1–26. doi: 10.1099/0022-1317-42-1-1. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Cohen J. C., Varmus H. E. Proviruses of mouse mammary tumor virus in normal and neoplastic tissues from GR and C3Hf mouse strains. J Virol. 1980 Aug;35(2):298–305. doi: 10.1128/jvi.35.2.298-305.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dickson C., Atterwill M. Composition, arrangement and cleavage of the mouse mammary tumor virus polyprotein precursor Pr77gag and p110gag. Cell. 1979 Aug;17(4):1003–1012. doi: 10.1016/0092-8674(79)90339-8. [DOI] [PubMed] [Google Scholar]
  10. Dickson C., Peters G. Protein-coding potential of mouse mammary tumor virus genome RNA as examined by in vitro translation. J Virol. 1981 Jan;37(1):36–47. doi: 10.1128/jvi.37.1.36-47.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dickson C., Smith R., Peters G. In vitro synthesis of polypeptides encoded by the long terminal repeat region of mouse mammary tumour virus DNA. Nature. 1981 Jun 11;291(5815):511–513. doi: 10.1038/291511a0. [DOI] [PubMed] [Google Scholar]
  12. Donehower L. A., Huang A. L., Hager G. L. Regulatory and coding potential of the mouse mammary tumor virus long terminal redundancy. J Virol. 1981 Jan;37(1):226–238. doi: 10.1128/jvi.37.1.226-238.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fine D. L., Plowman J. K., Kelley S. P., Arthur L. O., Hillman E. A. Enhanced production of mouse mammary tumor virus in dexamethasone-treated, 5-iododeoxyuridine-stimulated mammary tumor cell cultures. J Natl Cancer Inst. 1974 Jun;52(6):1881–1886. doi: 10.1093/jnci/52.6.1881. [DOI] [PubMed] [Google Scholar]
  14. Groner B., Hynes N. E. Number and location of mouse mammary tumor virus proviral DNA in mouse DNA of normal tissue and of mammary tumors. J Virol. 1980 Mar;33(3):1013–1025. doi: 10.1128/jvi.33.3.1013-1025.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Majors J. E., Varmus H. E. Nucleotide sequences at host-proviral junctions for mouse mammary tumour virus. Nature. 1981 Jan 22;289(5795):253–258. doi: 10.1038/289253a0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Moore D. H., Long C. A., Vaidya A. B., Sheffield J. B., Dion A. S., Lasfargues E. Y. Mammary tumor viruses. Adv Cancer Res. 1979;29:347–418. doi: 10.1016/s0065-230x(08)60850-7. [DOI] [PubMed] [Google Scholar]
  20. Neel B. G., Hayward W. S., Robinson H. L., Fang J., Astrin S. M. Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion. Cell. 1981 Feb;23(2):323–334. doi: 10.1016/0092-8674(81)90128-8. [DOI] [PubMed] [Google Scholar]
  21. Ringold G., Lasfargues E. Y., Bishop J. M., Varmus H. E. Production of mouse mammary tumor virus by cultured cells in the absence and presence of hormones: assay by molecular hybridization. Virology. 1975 May;65(1):135–147. doi: 10.1016/0042-6822(75)90014-8. [DOI] [PubMed] [Google Scholar]
  22. Sen G. C., Racevskis J., Sarkar N. H. Synthesis of murine mammary tumor viral proteins in vitro. J Virol. 1981 Mar;37(3):963–975. doi: 10.1128/jvi.37.3.963-975.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sharp P. A., Sugden B., Sambrook J. Detection of two restriction endonuclease activities in Haemophilus parainfluenzae using analytical agarose--ethidium bromide electrophoresis. Biochemistry. 1973 Jul 31;12(16):3055–3063. doi: 10.1021/bi00740a018. [DOI] [PubMed] [Google Scholar]
  24. Shimotohno K., Mizutani S., Temin H. M. Sequence of retrovirus provirus resembles that of bacterial transposable elements. Nature. 1980 Jun 19;285(5766):550–554. doi: 10.1038/285550a0. [DOI] [PubMed] [Google Scholar]
  25. Shoemaker C., Goff S., Gilboa E., Paskind M., Mitra S. W., Baltimore D. Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3932–3936. doi: 10.1073/pnas.77.7.3932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sutcliffe J. G. Nucleotide sequence of the ampicillin resistance gene of Escherichia coli plasmid pBR322. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3737–3741. doi: 10.1073/pnas.75.8.3737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yamamoto T., de Crombrugghe B., Pastan I. Identification of a functional promoter in the long terminal repeat of Rous sarcoma virus. Cell. 1980 Dec;22(3):787–797. doi: 10.1016/0092-8674(80)90555-3. [DOI] [PubMed] [Google Scholar]
  28. van Nie R., Verstraeten A. A. Studies of genetic transmission of mammary tumour virus by C3Hf mice. Int J Cancer. 1975 Dec 15;16(6):922–931. doi: 10.1002/ijc.2910160606. [DOI] [PubMed] [Google Scholar]

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