Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1982 Sep 11;10(17):5333–5343. doi: 10.1093/nar/10.17.5333

Long terminal repeat (LTR)-derived recombination of retroviral DNA: sequence analyses of an aberrant clone of baboon endogenous virus DNA which carries an inversion from the LTR to the gag region.

T Tamura, T Takano
PMCID: PMC320875  PMID: 6292838

Abstract

Nucleotide sequences of a cloned proviral DNA of baboon endogenous virus M7 were analyzed, which carried an internal inversion. The inversion of 2.2 kilobase pairs was occurred between the junction of two tandem LTRs and a site locating in the p30 region of the gag gene. The ATAA sequence was a target for recombination generating the inversion, which was duplicated at both ends of the inverted segment. AAA and CA were lost at the 5'- and 3'-ends of the LTRs by the inversion, respectively. On both sides of the target sequence, long AG-rich stretches were detected, which may specify the site of recombination together with the target sequence. The characteristic base changes in the inversion are concluded to result from an illegitimate recombination associated with LTRs, as well as in case of provirus integration into the host cell DNA. We propose and discuss models to explain the processes of recombination to generate both inversion and integration.

Full text

PDF
5333

Selected References

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

  1. Bishop J. M. Retroviruses. Annu Rev Biochem. 1978;47:35–88. doi: 10.1146/annurev.bi.47.070178.000343. [DOI] [PubMed] [Google Scholar]
  2. Calos M. P., Miller J. H. Transposable elements. Cell. 1980 Jul;20(3):579–595. doi: 10.1016/0092-8674(80)90305-0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Copeland T. D., Henderson L. E., Vanlaningham-Miller E. S., Stephenson J. R., Smythers G. W., Oroszlan S. Amino- and carboxyl-terminal sequences of proteins coded by gag gene of endogenous baboon and cat type C viruses. Virology. 1981 Feb;109(1):13–24. doi: 10.1016/0042-6822(81)90467-0. [DOI] [PubMed] [Google Scholar]
  5. Dhar R., McClements W. L., Enquist L. W., Vande Woude G. F. Nucleotide sequences of integrated Moloney sarcoma provirus long terminal repeats and their host and viral junctions. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3937–3941. doi: 10.1073/pnas.77.7.3937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dunsmuir P., Brorein W. J., Jr, Simon M. A., Rubin G. M. Insertion of the Drosophila transposable element copia generates a 5 base pair duplication. Cell. 1980 Sep;21(2):575–579. doi: 10.1016/0092-8674(80)90495-x. [DOI] [PubMed] [Google Scholar]
  7. Farabaugh P. J., Fink G. R. Insertion of the eukaryotic transposable element Ty1 creates a 5-base pair duplication. Nature. 1980 Jul 24;286(5771):352–356. doi: 10.1038/286352a0. [DOI] [PubMed] [Google Scholar]
  8. Galas D. J., Calos M. P., Miller J. H. Sequence analysis of Tn9 insertions in the lacZ gene. J Mol Biol. 1980 Nov 25;144(1):19–41. doi: 10.1016/0022-2836(80)90213-2. [DOI] [PubMed] [Google Scholar]
  9. Giard D. J., Aaronson S. A., Todaro G. J., Arnstein P., Kersey J. H., Dosik H., Parks W. P. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst. 1973 Nov;51(5):1417–1423. doi: 10.1093/jnci/51.5.1417. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Ju G., Skalka A. M. Nucleotide sequence analysis of the long terminal repeat (LTR) of avian retroviruses: structural similarities with transposable elements. Cell. 1980 Nov;22(2 Pt 2):379–386. doi: 10.1016/0092-8674(80)90348-7. [DOI] [PubMed] [Google Scholar]
  12. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Noda M., Wagatsuma M., Tamura T., Takano T., Matsubara K. Structure of the baboon endogenous virus genome: cloning of circular virus DNA in bacteriophage lambda. Nucleic Acids Res. 1981 May 11;9(9):2173–2185. doi: 10.1093/nar/9.9.2173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Oroszlan S., Copeland T., Summers M. R., Smythers G., Gilden R. V. Amino acid sequence homology of mammalian type C RNA virus major internal proteins. J Biol Chem. 1975 Aug 25;250(16):6232–6239. [PubMed] [Google Scholar]
  15. Oroszlan S., Henderson L. E., Stephenson J. R., Copeland T. D., Long C. W., Ihle J. N., Gilden R. V. Amino- and carboxyl-terminal amino acid sequences of proteins coded by gag gene of murine leukemia virus. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1404–1408. doi: 10.1073/pnas.75.3.1404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Reed R. R., Grindley N. D. Transposon-mediated site-specific recombination in vitro: DNA cleavage and protein-DNA linkage at the recombination site. Cell. 1981 Sep;25(3):721–728. doi: 10.1016/0092-8674(81)90179-3. [DOI] [PubMed] [Google Scholar]
  17. Reed R. R. Resolution of cointegrates between transposons gamma delta and Tn3 defines the recombination site. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3428–3432. doi: 10.1073/pnas.78.6.3428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Reed R. R. Transposon-mediated site-specific recombination: a defined in vitro system. Cell. 1981 Sep;25(3):713–719. doi: 10.1016/0092-8674(81)90178-1. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Shapiro J. A. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1933–1937. doi: 10.1073/pnas.76.4.1933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Shimotohno K., Temin H. M. No apparent nucleotide sequence specificity in cellular DNA juxtaposed to retrovirus proviruses. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7357–7361. doi: 10.1073/pnas.77.12.7357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Shoemaker C., Hoffman J., Goff S. P., Baltimore D. Intramolecular integration within Moloney murine leukemia virus DNA. J Virol. 1981 Oct;40(1):164–172. doi: 10.1128/jvi.40.1.164-172.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Takano T., Noda M., Tamura T. Transfection of cells from a xeroderma pigmentosum patient with normal human DNA confers UV resistance. Nature. 1982 Mar 18;296(5854):269–270. doi: 10.1038/296269a0. [DOI] [PubMed] [Google Scholar]
  27. Tamura T., Noda M., Takano T. Structure of the baboon endogenous virus genome: nucleotide sequences of the long terminal repeat. Nucleic Acids Res. 1981 Dec 11;9(23):6615–6626. doi: 10.1093/nar/9.23.6615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Temin H. M. Structure, variation and synthesis of retrovirus long terminal repeat. Cell. 1981 Nov;27(1 Pt 2):1–3. doi: 10.1016/0092-8674(81)90353-6. [DOI] [PubMed] [Google Scholar]
  29. Van Beveren C., Goddard J. G., Berns A., Verma I. M. Structure of Moloney murine leukemia viral DNA: nucleotide sequence of the 5' long terminal repeat and adjacent cellular sequences. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3307–3311. doi: 10.1073/pnas.77.6.3307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Van Beveren C., Rands E., Chattopadhyay S. K., Lowy D. R., Verma I. M. Long terminal repeat of murine retroviral DNAs: sequence analysis, host-proviral junctions, and preintegration site. J Virol. 1982 Feb;41(2):542–556. doi: 10.1128/jvi.41.2.542-556.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES