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Covalently closed circles of adenovirus 5 DNA

Abstract

The genome of adenoviruses is a double-stranded linear DNA molecule with inverted terminal repeats about 100 base pairs (bp) in length1,2 and a terminal protein covalently linked to the 5′ nucleotide of each strand3,4. Both of these features permit the formation of DNA circles, the inverted repeats allowing the circularization of single-stranded DNA5,6 and the terminal protein the joining of one or more molecules to yield double-stranded circles or concatemers7. However, although the existence of covalently closed circles has been postulated7, double-stranded viral DNA purified from virions or infected cells by conventional methods (that is, using proteases and phenol or chloroform) has always been obtained in a linear form8. Here we present evidence for the existence in adenovirus 5 (Ad5) infected cells of novel structures resulting from covalent head-to-tail joining of viral DNA molecules and show that these structures are due at least in part to the formation of covalently closed circles.

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References

  1. Steenberg, P. H., Maat, J., van Ormondt, H. & Sussenbach, J. S. Nucleic Acids Res. 4, 4371–4389 (1977).

    Article  Google Scholar 

  2. Arrand, J. R. & Roberts, R. J. J. molec. Biol. 128, 577–594 (1979).

    Article  CAS  PubMed  Google Scholar 

  3. Rekosh, D. M. K., Russell, W. C., Bellett, A. J. D. & Robinson, A. J. D. & Robinson, A. J. Cell 11, 283–295 (1977).

    Article  CAS  PubMed  Google Scholar 

  4. Desiderio, S. V. & Kelly, T. J. Jr J. molec. Biol. 145, 319–337 (1981).

    Article  CAS  PubMed  Google Scholar 

  5. Garon, C. F., Berry, K. & Rose, J. A. Proc. natn. Acad. Sci. U.S.A. 69, 2391–2395 (1972).

    Article  ADS  CAS  Google Scholar 

  6. Wolfson, J. & Dressier, D. Proc. natn. Acad. Sci. U.S.A. 69, 3054–3057 (1972).

    Article  ADS  CAS  Google Scholar 

  7. Robinson, A. J., Younghusband, H. B. & Bellett, A. J. D. Virology 56, 54–69 (1973).

    Article  CAS  PubMed  Google Scholar 

  8. Tooze, J. (ed.) The Molecular Biology of Tumor Viruses P2, 2nd edn (Cold Spring Harbor Laboratory, New York, 1980).

  9. Graham, F. L. et al. Cold Spring Harb. Symp. quant. Biol. 39, 637–650 (1974).

    Article  Google Scholar 

  10. van der Eb, A. J., Mulder, C., Graham, F. L. & Houweling, A. Gene 2, 115–132 (1977).

    Article  CAS  PubMed  Google Scholar 

  11. Gallimore, P. H., Sharp, P. A. & Sambrook, J. J. molec. Biol. 89, 49–72 (1974).

    Article  CAS  PubMed  Google Scholar 

  12. Dorsch-Häsler, K., Fisher, P., Weinstein, B. & Ginsberg, H. J. Virol. 34, 305–314 (1980).

    PubMed  PubMed Central  Google Scholar 

  13. Ibelgaufts, H., Doerfler, W., Scheidtmann, K. H. & Wechsler, W. J. Virol. 33, 423–437 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Ruben, M., Bacchetti, S. & Graham, F. L. J. Virol. 41, 674–685 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Visser, L. et al. J. Virol. 39, 684–693 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Vardimon, L. & Doerfler, W. J. molec. Biol. 147, 227–246 (1981).

    Article  CAS  PubMed  Google Scholar 

  17. Harrison, T., Graham, F. L. & Williams, J. Virology 77, 319–329 (1977).

    Article  CAS  PubMed  Google Scholar 

  18. Graham, F. L., Harrison, T. & Williams, J. Virology 86, 10–21 (1978).

    Article  CAS  PubMed  Google Scholar 

  19. Lilly, D. M. J. Nature 292, 380–382 (1981).

    Article  ADS  Google Scholar 

  20. Challberg, M. D. & Kelly, T. J. Jr Proc. natn. Acad. Sci. U.S.A. 76, 655–659 (1979).

    Article  ADS  CAS  Google Scholar 

  21. Lichy, J. H., Horwitz, M. S. & Hurwitz, J. Proc. natn. Acad. Sci. U S. A. 78, 2678–2682 (1981).

    Article  ADS  CAS  Google Scholar 

  22. Tamanoi, F. & Stillman, B. W. Proc. natn. Acad. Sci. U.S.A. 79, 2221–2225 (1982).

    Article  ADS  CAS  Google Scholar 

  23. Pearson, G. D. et al. ICN-UCLA Symp. molec. cell. Biol. 21, 581–595 (1981).

    Google Scholar 

  24. Shank, P. R. & Varmus, H. E. J. Virol. 25, 104–114 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Guntaka, R. V., Mahy, B. W. J., Bishop, J. M. & Varmus, H. E. Nature 253, 507–511 (1975).

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Yang, W. K., Yang, D. M. & Kiggans, J. O. Jr J. Virol. 36, 181–188 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Jolicoeur, P. & Rassart, E. J. Virol. 33, 183–195 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Chinsky, J. & Soeiro, R. J. Virol. 43, 182–190 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Hsu, T. W. & Taylor, J. M. J. Virol. 44, 47–53 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Lindahl, T. et al. J. molec. Biol. 102, 511–530 (1976).

    Article  CAS  PubMed  Google Scholar 

  31. Flavell, A. J. & Ish-Horowicz, D. Nature 292, 591–595 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Southern, E. M. J. molec. Biol. 98, 503–517 (1975).

    Article  CAS  PubMed  Google Scholar 

  33. Keiner, G. & Kelly, T. J. Jr, Proc. natn. Acad. Sci. U.S.A. 73, 1102–1106 (1976).

    Article  ADS  Google Scholar 

  34. McKinnon, R. D., Bacchetti, S. & Graham, F. L. Gene 19, 33–42 (1982).

    Article  CAS  PubMed  Google Scholar 

  35. Maniatis, T., Jeffrey, A. & Kleid, D. Proc. natn. Acad. Sci. U.S.A. 72, 1184–1188 (1975).

    Article  ADS  CAS  Google Scholar 

  36. Wahl, G. M. & Stark, G. R. Proc. natn. Acad. Sci. U.S.A. 76, 3683–3687 (1979).

    Article  ADS  CAS  Google Scholar 

  37. Kimura, G., Itagaki, A. & Summers, J. Int. J. Cancer 15, 694–706 (1975).

    Article  CAS  PubMed  Google Scholar 

  38. Birnboim, H. C. & Doly, J. Nucleic Acids Res. 7, 1513–1523 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Ruben, M., Bacchetti, S. & Graham, F. Covalently closed circles of adenovirus 5 DNA. Nature 301, 172–174 (1983). https://doi.org/10.1038/301172a0

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