Advertisement

Synergism Between Oncogenes in T-cell Lymphomagenesis

  • Anton Berns
  • Marco Breuer
  • Sjef Verbeek
  • Maarten van Lohuizen
Part of the NATO ASI Series book series (volume 34)

Summary

Insertional mutagenesis is one of the mechanisms by which retroviruses can transform cells. A number of proto-oncogenes have been shown to be activated by proviral insertion in retrovirally-induced tumors. Cloning of common proviral insertion sites has led to the discovery of a series of new (putative) oncogenes. Here we report on the involvement of pim-1. pim-2. c-myc. and N-myc in MuLV-induced T-cell lymphomas. Furthermore, we show that transgenic mice carrying an activated pim-1 gene are predisposed to lymphomagenesis and that these mice can be used to show cooperation between pim-1 and c-mvc or N-mvc in tumorigenesis.

Keywords

Insertional Mutagenesis Mouse Mammary Tumor Virus Myeloid Tumor Tumorigenic Process Putative Oncogene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Berns A (1988) Provirus tagging as an instrument to identify oncogenes and to establish synergism between oncogenes. Arch Virol 102: 1–18PubMedCrossRefGoogle Scholar
  2. Berns A, Cuypers H, Selten G, Domen J (1988) The putative oncogene pim-1. In: Skalka, Reddy (eds) The oncogene handbook, p 121Google Scholar
  3. Bordereaux D, Fichelson S, Sola B, Tambourin PE, Gisselbrecht S (1987) Frequent involvement of the fim-3 region in Friend murine leukemia virus-induced mouse myeloblasts leukemias. J Virol 61: 4043–4045PubMedGoogle Scholar
  4. Breuer M, Cuypers HT, Berns A (1989) Evidence for the involvement of pim-2. a new common proviral insertion site, in progression of lymphomas. EMBO J (in press)Google Scholar
  5. Cairns J (1975) Mutation selection and the natural history of cancer. Nature 255:197- 200Google Scholar
  6. Cuypers HT, Selten G, Quint W, Zijlstra M, Robanus-Maandag E, Boelens W, van Wezenbeek P, Melief C, Berns A (1984) Murine leukemia virus-induced T-cell lymphomagenesis: integration of proviruses in a distinct chromosomal region. Cell 37: 141–150PubMedCrossRefGoogle Scholar
  7. Cuypers HT, Selten G, Berns A, Geurts van Kessel A (1986a) Assignment of the human homolog of pim-1, a mouse gene implicated in leukemogenesis, to the pter-12 region of chromosome 6. Human Genet 72: 262–265CrossRefGoogle Scholar
  8. Cuypers HT, Selten G, Zijlstra M, de Goede R, Melief C, Berns A (1986b) Tumor progression in MuLV induced T-cell lymphomas: monitoring of clonal selections with viral and cellular probes. J Virol 60: 230–241Google Scholar
  9. Dauntry F, Weil D, Yu J, Dautry-Varsat A (1988) Regulation of pim and myb mRNA accumulation by interleukin 2 and interleukin 3 in murine hematopoietic cell lines. J Biol Chem 263: 17615–17620Google Scholar
  10. Domen J, von Lindern J, Hermans A, Breuer M, Grosveld G, Berns A (1987) Comparison of the human and mouse pim-1 cDNAs: nucleotide sequence and immunological identification of the ‘in vitro’ synthesized pim-1 protein. Oncogene Res 1: 103–112PubMedGoogle Scholar
  11. Farber E (1984) The multistep nature of cancer development. Cancer Res 44: 4217–4223PubMedGoogle Scholar
  12. Farber E, Cameron R (1980) The sequential analysis of cancer development. Adv Cancer Res 31: 125–226CrossRefGoogle Scholar
  13. Gisselbrecht S, Fichelson S, Sola B, Bordereaux D, Hampe A, Andre C, Galibert F, Tambourin P (1987) Frequent c-fms activation by proviral insertion in mouse mye-loblastic leukaemias. Nature 329: 259–261PubMedCrossRefGoogle Scholar
  14. Harris AW, Pinkert CA, Crawford M, Langdon WY, Brinster RL, Adams JM (1988) The Efi-myc transgenic mouse: a model for high-incidence spontaneous lymphoma and leukemia of early B cells. J Exp Med 167: 353–371PubMedCrossRefGoogle Scholar
  15. Hayward WS, Neel BG, Astrin SM (1981) Activation of a cellular onco gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 290: 475–480PubMedCrossRefGoogle Scholar
  16. Hilkens J, Cuypers HT, Selten G, Kroezen V, Hilgers J, Berns A (1986) Genetic mapping of pim-1 putative oncogene to mouse chromosome 17. Som Cell Mol Gen 12: 81–88CrossRefGoogle Scholar
  17. Kanter MR, Smith RE, Hayward WS (1988) Rapid induction of B cell lymphomas: insertional activation of c-myb by avian leukosis virus. J Virol 62: 1423–1432PubMedGoogle Scholar
  18. Klein G, Klein E (1985) Evolution of tumors and the impact of molecular oncology. Nature 315: 190–195PubMedCrossRefGoogle Scholar
  19. Klein G, Klein E (1986) Conditioned tumorigenicity of activated oncogenes. Cancer Res 46: 3211–3224PubMedGoogle Scholar
  20. Langdon WY, Harris AW, Cory S, Adams JM (1986) The c-mvc oncogene perturbs B lymphocyte development in Eµ-myc transgenic mice. Nature 47: 11–18Google Scholar
  21. Mally MI, Vogt M, Swift SE, Haas M (1985) Oncogene expression in murine splenic T cells and in murine T-cell neoplasms. Virology 144: 115–126PubMedCrossRefGoogle Scholar
  22. Meeker TC, Nagarajan L, Ar-Rushdi A, Rovera G, Huebner K, Croce CM (1987) Characterization of the human pim-1 gene: a putative proto-oncogene coding for a tissue specific member of the protein kinase family. Oncogene Res 1: 87–101PubMedGoogle Scholar
  23. Moreau-Gachelin F, Tavitian A, Tambourin P (1988) Spi-1 is a putative oncogene in virally induced murine erythroleukaemias. Nature 331: 277–280PubMedCrossRefGoogle Scholar
  24. Mucenski ML, Gilbert DJ, Taylor BA, Jenkins NA, Copeland NG (1987) Common sites of viral integration in lymphomas arising in AKXD recombinant inbred mouse strains. Oncogene Res 2: 33–48PubMedGoogle Scholar
  25. Mucenski ML, Taylor BA, Ihle JN, Hartley JW, Morse III HC, Jenkins NA, Copeland NG (1988) Identification of a common ecotropic viral integration site, Evi-1, in the DNA of AKXD murine myeloid tumors. Mol Cell Biol 8: 301–308Google Scholar
  26. Nüsse R, Varmus HE (1982) Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31: 99–09PubMedCrossRefGoogle Scholar
  27. Nüsse R, Berns A (1988) Cellular oncogene activation by insertion of retroviral DNA. Genes identified by provirus tagging. In: Klein G (ed) Cellular oncogene activation. Marcel Dekker, New York, p 95Google Scholar
  28. O’Donnell PV, Fleissner E, Lonial H, Koehne CF, Reicin A (1985) Early clonality and high-frequency proviral integration into the c-myc locus in AKR leukemias. J Virol 55: 500–503PubMedGoogle Scholar
  29. Peters G, Brookes S, Smith R, Dickson C (1983) Tumorigenesis by mouse mammary tumor virus: evidence for a common region for provirus integration in mammary tumors. Cell 33: 369–377PubMedCrossRefGoogle Scholar
  30. Peters G, Lee AL, Dickson C (1986) Concerted activation of two potential proto-oncogenes in carcinomas induced by mouse mammary tumor virus. Nature 320: 628–631PubMedCrossRefGoogle Scholar
  31. Pitot HC (1979) Biological and enzymatic events in chemical carcinogenesis. Annu Rev Med 30: 25–39PubMedCrossRefGoogle Scholar
  32. Poste G, Fidler IJ (1980) The pathogenesis of cancer metastasis. Nature 283: 139–146PubMedCrossRefGoogle Scholar
  33. Roos E, La Rivière G, Collard JG, Stukart MJ, De Baetselier P (1985) Invasiveness of T-cell hybridomas in vitro and their metastatic potential in vivo. Cancer Res 45: 6238–6243PubMedGoogle Scholar
  34. Selten G, Cuypers HT, Zijlstra M, Melief C, Berns A (1984) Involvement of c-myc in MuLV-induced T cell lymphomas in mice: frequency and mechanisms of activation. EMBO J 3: 3215–3222PubMedGoogle Scholar
  35. Selten G, Cuypers HT, Boelens W, Robanus-Maandag E, Verbeek J, Domen J, van Beveren C, Berns A (1986) The primary structure of the putative oncogene pim- 1 shows extensive homology with protein kinases. Cell 46:603-611Google Scholar
  36. Shen-Ong GL, Morse HC, Potter M, Mushinski JF (1986) Two modes of c-myb activation in virus-induced mouse myeloid tumors. Mol Cell Biol 6:380–392Google Scholar
  37. Sola B, Fichelson S, Bordereaux D, Tambourin PE, Gisselbrecht S (1986) fim-1 and fim-2: two new integration regions of Friend murine leukemia virus in myelobl¬asts leukemias. J 60:718–725Google Scholar
  38. Tsichlis PN, Strauss PG, Lohse MA (1985) Concerted DNA rearrangement in Moloney murine leukemia virus-induced thymomas: a potential synergistic relationship in oncogenesis. J Virol 56:258–267Google Scholar
  39. Van Lohuizen M, Verbeek S, Krimpenfort P, Radaszkiewicz T, Berns A (1989a) Predisposition to lymphomagenesis in pim-1 transgenic mice: cooperation with c- mvc and N-mvc in MuLV induced tumors. Cell (in press)Google Scholar
  40. Van Lohuizen M, Breuer M, Berns A (1989b) N-myc is frequently activated by proviral insertion in MuLV-induced T-cell lymphomas. EMBO J (in press)Google Scholar
  41. Zakut-Houri R, Hazum S, Givol D, Telerman A (1987) The cDNA sequence and gene analysis of the human pim oncogene. Gene 54:105-111Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • Anton Berns
    • 1
    • 2
  • Marco Breuer
    • 1
    • 2
  • Sjef Verbeek
    • 1
    • 2
  • Maarten van Lohuizen
    • 1
    • 2
  1. 1.Division of Molecular GeneticsThe Netherlands Cancer InstituteAmsterdamThe Netherlands
  2. 2.The Department of Biochemistry of the University of AmsterdamAmsterdamThe Netherlands

Personalised recommendations