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A common region for proviral DNA integration in MoMuLV-induced rat thymic lymphomas

Abstract

Similarly to other mammalian and avian retroviruses that lack a transforming gene1, moloney murine leukaemia virus (MoMuLV) causes no morphological transformation in infected tissue culture cells. However, following injection in an appropriate animal host, MoMuLV induces mainly thymic lymphomas after a long latency period2,3. A common characteristic of neoplasms induced by retroviruses lacking transforming genes is their clonal origin4–9. Here we have generated MoMuLV-induced rat thymic lymphomas and confirmed their clonal nature. Furthermore, we took advantage of the clonality of these tumours to investigate the specificity of provirus integration in the tumour DNA. We reasoned that if several independently derived thymic lymphomas would contain the provirus integrated in the same region of cellular DNA, this would be a strong indication that this integration event is a contributing factor in oncogenesis. The results indicate that there is indeed a cellular DNA region (termed the ML VI-1 locus) that serves as the substrate for proviral DNA integration in 5 out of 16 tumours we examined.

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References

  1. Vogt, P. K. in Comprehensive Virology Vol. 9 (eds Fraenkel-Conrat, H. & Wagner, R. R.) 344–455 (Plenum, New York, 1977).

    Google Scholar 

  2. Moloney, J. B. J. natn. Cancer Inst. 24, 933–951 (1960).

    CAS  Google Scholar 

  3. Moloney, J. B. Natn. Cancer Inst. Monogr. 4, 7–33 (1960).

    CAS  Google Scholar 

  4. Neel, B. G., Hayward, W. S., Robinson, H. L., Fang, J. & Astrin, S. M. Cell 23, 323–334 (1981).

    Article  CAS  PubMed  Google Scholar 

  5. Hayward, W. S., Neel, B. G. & Astrin, S. M. Nature 290, 475–479 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Payne, G. S. et al. Cell 23, 311–312 (1981).

    Article  CAS  PubMed  Google Scholar 

  7. Payne, G. S., Bishop, J. M. & Varmus, H. E. Nature 295, 209–214 (1982).

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Noori-Daloii, M. R., Swift, R. A., Kung, H. J., Crittenden, L. B. & Witter, R. L. Nature 294, 574–576 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Cohen, J. C., Shank, P. R., Morris, V.L., Caridiff, R. & Varmus, H. E. Cell 16, 333–345 (1979).

    Article  CAS  PubMed  Google Scholar 

  10. Steffen, D. & Weinberg, R. A. Cell 15, 1003–1010 (1978).

    Article  CAS  PubMed  Google Scholar 

  11. Hughes, S. H. et al. Cell 15, 1397–1410 (1978).

    Article  CAS  PubMed  Google Scholar 

  12. Gilmer, T. M. & Parsons, J. T. J. Virol. 32, 762–769 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Ringold, G. M., Shank, P. R., Varmus, H. E., Ring, J. & Yamamoto, K. R. Proc. natn. Acad. Sci. U.S.A. 76, 665–669 (1979).

    Article  ADS  CAS  Google Scholar 

  14. Kettmann, R. et al. Proc. natn. Acad. Sci. U.S.A. 76, 4822–4826 (1979).

    Article  ADS  CAS  Google Scholar 

  15. O'Rear, J. J., Mizutani, S., Hoffman, G., Fiandt, M. & Temin, H. M. Cell 20, 423–430 (1980).

    Article  CAS  PubMed  Google Scholar 

  16. Hughes, S. H., Vogt, P. K., Stubblefield, E., Bishop, J. M. & Varmus, H. E. Virology 108, 208–221 (1981).

    Article  CAS  PubMed  Google Scholar 

  17. Varmus, H. & Swanstrom, R. in RNA Tumor Viruses (eds Weiss, R., Teich, N., Varmus, H. & Coffin, J.) 424–428 (Cold Spring Harbor Laboratory, New York, 1982).

    Google Scholar 

  18. Tsichlis, P. N. & Coffin, J. M. Cold Spring Harb. Symp. quant. Biol. 44, 1123–1132 (1979).

    Article  Google Scholar 

  19. Tsichlis, P. N. & Coffin, J. M. J. Virol. 33, 238–249 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Quintrell, N., Hughes, S. H., Varmus, H. E. & Bishop, J. M. J. molec. Biol. 143, 363–393 (1980).

    Article  CAS  PubMed  Google Scholar 

  21. Enquist, L., Tiemieir, P., Leder, P., Weisberg, R. & Sternberg, N. Nature 259, 596–598 (1976).

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Gilboa, E. et al. Cell 16, 863–874 (1979).

    Article  CAS  PubMed  Google Scholar 

  23. Shinnick, T. M., Lerner, R. A. & Sutcliffe, J. G. Nature 293, 543–548 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  24. Robinson, H. L., Blais, B. M., Tsichlis, P. N. & Coffin, J. M. Proc. natn. Acad. Sci. U.S.A. 79, 1225–1229 (1982).

    Article  ADS  CAS  Google Scholar 

  25. Lemons, R. S., Nash, W. G., O'Brien, S. J., Benveniste, R. E. & Sherr, C. J. Cell 14, 995–1005 (1978).

    Article  CAS  PubMed  Google Scholar 

  26. Nusse, R. & Varmus, H. E. Cell 31, 99–109 (1982).

    Article  CAS  PubMed  Google Scholar 

  27. Varmus, H. E., Quintrell, N. & Ortiz, S. Cell 25, 23–36 (1981).

    Article  CAS  PubMed  Google Scholar 

  28. Jenkins, N. A., Copeland, N. G., Taylor, B. A. & Lee, B. K. Nature 293, 370–374 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  29. Cooper, G. M. & Neiman, P. Nature 292, 857–858 (1980).

    Article  ADS  Google Scholar 

  30. Lane, M. A., Sainten, A. & Cooper, G. M. Proc. natn. Acad. Sci. U.S.A. 78, 5185–5189 (1981).

    Article  ADS  CAS  Google Scholar 

  31. Lane, M. A., Sainten, A. & Cooper, G. M. Cell 28, 873–880 (1982).

    Article  CAS  PubMed  Google Scholar 

  32. Southern, E. M. J. molec. Biol. 98, 505–517 (1975).

    Article  Google Scholar 

  33. Blattner, F. R. et al. Science 202, 1279–1284 (1978).

    Article  ADS  CAS  PubMed  Google Scholar 

  34. McMaster, G. K. & Carmichael, G. G. Proc. natn. Acad. Sci. U.S.A. 74, 4835–4838 (1977).

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  36. Vande Woude, G. W. et al. Proc. natn. Acad. Sci. U.S.A. 76, 4454–4468 (1979).

    Article  ADS  Google Scholar 

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Tsichlis, P., Strauss, P. & Hu, L. A common region for proviral DNA integration in MoMuLV-induced rat thymic lymphomas. Nature 302, 445–449 (1983). https://doi.org/10.1038/302445a0

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