The Ig/myc Translocation in Burkitt’s Lymphoma Is a Rate Limiting Step in Tumor Development with Multiple Phenotypic Consequences

  • G. Klein
Conference paper

Abstract

Reciprocal translocation between the c-myc carrying chromosome and one of the three Ig loci is a regular feature of certain B-cell derived tumors in three species: Burkitt lymphomas (BL) in humans, induced plasmacytomas in Balb/c mice (MPC), and the spontaneous immunocytomas (RIC) of the Louvain rat (for review see Klein and Klein 1985). I know of no other example in the cancer field where equally homologous oncogene activation events are associated with tumors of different species and of different natural histories, that have their cell linage derivation as the only common denominator.

Keywords

Burkitt Lymphoma Random Break Burkitt Lymphoma Virus Latent Gene Expression Burkitt Lymphoma Line 
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Bibliography

  1. Adams J M, Harris A W, Pinkert C A, Corcoran L M, Alexander W S, Cory S, Palmiter R D and Brinster R L: The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318:533–538, 1985.PubMedCrossRefGoogle Scholar
  2. Alt F W, Blackwell T K, De Pinho R A, Reth M G and Yancopoulos G D: Regulation of genome rearrangement events during lymphocyte differentiation. Immunological Reviews 89:5–30,1986.PubMedCrossRefGoogle Scholar
  3. Altiok E, Klein G, Zech L, Uno M, Ehlin-Henriksson B, Battat S, Ono Y and Ernberg I: EBV-transformed pro-B cells are prone to illegimate recombination between the Su region and other chromosomes. PNAS, in press.Google Scholar
  4. Avila-Carino J, Torsteinsdottir S, Bejarano M T, Klein G, Klein E and Masucci, M G: Combined treatment with interferon (IFN)- and tumor necrosis factor (TNF)- up-regulates the expression of HLA class I determinants in Burkitt lymphoma lines. Cel Immunol 117:303–311, 1988.CrossRefGoogle Scholar
  5. Claesson M, Henriksson M, Sumegi J, Klein G and Hammarskjöld M-L: Elevated c-myc expression facilitates the replication of SV 40 DNA in human lymphoma cells. Nature 330:272–274, 1987.CrossRefGoogle Scholar
  6. Coppola J A and Cole M D: Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature 320:760–763, 1986.PubMedCrossRefGoogle Scholar
  7. Cory S: Activation of cellular oncogenes in hemopoietic cells by chromosome translocation. Adv Cancer Res 47:189–234, 1986.PubMedCrossRefGoogle Scholar
  8. Dmitrovsky E, Kuehl W M, Hoilis G F, Kirsch I R, Bender T P and Segal S: Expression of a transfected human c-myc oncogene inhibits differentiation of a mouse erythroleukaemia cell line. Nature 322:748–750, 1986.PubMedCrossRefGoogle Scholar
  9. Ehlin-Henriksson B, Manneborg-Sandlund A and Klein G: Expression of B-cell specific markers in different Burkitt lymphoma subgroups. Int J Cancer 39:211–218, 1987.PubMedCrossRefGoogle Scholar
  10. Ernberg I, Falk, K, Minarovits, J, Busson P, Tursz T, Masucci M G and Klein, G: The role of methylation in the phenotype dependent modulation of EBNA 2 and LMP genes in latently EBV infected cells. J Gen Virol, in press.Google Scholar
  11. Gordon J, Guy G and Walker L: Autocrine models of B-lymphocyte growth. I. Role of cell contact and soluble factors in T-independent B-cell responses. Immunology 56:329–335, 1985.PubMedCentralPubMedGoogle Scholar
  12. Gratama J W, Oosterveer, MAP, Zwaan F E, Lepoutre J, Klein G and Ernberg I: Eradication of Epstein-Barr virus by allogeneic bone marrow transplantation: Implications for sites of viral latency. Proc Natl Acad Sci USA 85:8693–8696, 1988.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Gregory C D, Tursz T, Edwards C F, Tetaud C, Talbot M, Caillou B, Rickinson A B and Lipinski M: Identification of a subset of normal B cells with a Burkitt’s lymphoma (BL)-like phenotype. J Immunol 139:313–318, 1987.PubMedGoogle Scholar
  14. Gregory C D, Murray, R J, Edwards C F and Rickinson A B: Downregulation of cell adhesion molecules LFA-3 and ICAM-1 in Epstein-Barr virus-positive Burkitt’s lymphoma underlies tumor cell escape from virus-specific T cell surveillance. J Exp Med 167:1811–1824, 1988.PubMedCrossRefGoogle Scholar
  15. Hayward W S, Neel B G and Astrin S M: Activation of a cellular one gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 290:475–480, 1981.PubMedCrossRefGoogle Scholar
  16. Katamine S, Otsu M, Tada K, Tsuchiya S, Sato T, Ishida N, Honjo T and Ono Y: Epstein-Barr virus transforms precursor B-cells even before immunoglobulin gene rearrangements. Nature 309:369–372, 1984.PubMedCrossRefGoogle Scholar
  17. Klein G, Viral latency and transformation: The strategy of Epstein-Bar virus. Cell, in press.Google Scholar
  18. Klein G and Klein E: Myc/Ig juxtaposition by chromosomal translocations: some new insights, puzzles and paradoxes. Immunology Today 6:208–215, 1985.CrossRefGoogle Scholar
  19. Larsson L-G, Ivhed I, Gidlund M, Pettersson U, Vennstrom B and Nilsson K: Phorbol ester-induced terminal differentiation is inhibited in human U-937 monoblastic cells expressing a v-myc oncogene. PNAS 85:2638–2642.Google Scholar
  20. Lewin N, Aman P, Masucci M G, Klein E, Klein G, Oberg B, Strander H, Henle W and Henle G: Characterization of EBV-carrying B-cell populations in healthy seropositive individuals with regard to density, release of transforming virus and spontaneous outgrowth. Int J Cancer 39:472–476, 1987.PubMedCrossRefGoogle Scholar
  21. Magrath I: The pathogenesis of Burkitts lymphoma. Adv Cancer Res, in press.Google Scholar
  22. Masucci M G, Torsteinsdottir S, Colombani J, Brautbar C, Klein E and Klein G: Down-regulation of Cl I HLA antigens and of the Epstein-Barr virus-encoded latent membrane protein in Burkitt lymphoma lines. PNAS 84:4567–4571, 1987.PubMedCentralPubMedCrossRefGoogle Scholar
  23. Masucci M G, Stam N J, Torsteinsdottir S, Neefjes J J, Klein G and Ploegh H J: Allele specific down-regulation of MHC Class I antigens in Burkitt lymphoma lines. Cell Immunol 1220: 396–400, 1989.CrossRefGoogle Scholar
  24. Masucci, M G, Contreras-Salazar, B, Ragnar, E, Falk,K, Minarovits, J, Ernberg I and Klein, G: 5-Azacytidine up-regulates the expression of EBNA 2–6 and LMP in an EBNA-1 positive, EBNA 2–6 and LMP negative Burkitt lymphoma line. J Virol, in press.Google Scholar
  25. Nilsson, K. In INSERM Symposium no 8: Human lymphocyte differentiation in its application to cancer. B Seru and C Rosenfeld, eds. (Elsevier/North Holland Biomedical Press, Amsterdam) pp 307–317, 1987.Google Scholar
  26. Otsu M, Katamine S, Uno M, Yamaki M, Ono Y, Klein G, Sasaki M S, Yaoita Y and Honjo T: Molecular characterization of novel reciprocal translocation t (6?14) in an Epstein-barr virus-transformed B-cell precursor. Mol Cell Biol 7:708–717, 1987.PubMedCentralPubMedGoogle Scholar
  27. Pear W S, Nelson S F, Axelsson H, Wahlstrom G, Bazin H, Klein G and Sumegi J: Aberrant class switching juxtaposes c-myc with a middle repetitive element (line) and an IgH intron in two spontaneously arising rat immuncytomas. Oncogene 2:499–507, 1988 a.PubMedGoogle Scholar
  28. Pear W S, Wahlström G, Nelson S F, Axelsson H, Szeles A, Wiener F, Bazin H, Klein G and Sumegi J: 6;7 chromosomal translocation in spontaneously arising rat immunocytomas: evidence for c-myc breakpoint clustering and correlation between isotypic expression and the c-myc target. Mol Cell Biol 8:441–451, 1988 b.PubMedCentralPubMedGoogle Scholar
  29. Potter M, Mushinski J F, Mushinski E B, Brust S, Wax J S, Wiener F, Babonits M, Rapp U R and Morse I H C: Avian v-myc replaces chromosomal translocation in murine plasmacytomagenesis. Science 235:787–789, 1987.PubMedCrossRefGoogle Scholar
  30. Prochownik E V and Kukowska J: Deregulated expression of c-myc by murine erythroleukemia cells prevents differentiation. Nature 322:848–850, 1986.PubMedCrossRefGoogle Scholar
  31. Rickinson A B: Cellular immunological responses to the virus infection. In: The Epstein-Barr virus: recent advances. M A Epstein and B G Achong, eds. William Heinemann Medical Books, London, pp 75–125, 1987.Google Scholar
  32. Rooney C M, Rickinson A B, Moss D J, Lenoir G M and Epstein M A: Paired Epstein-barr virus-carrying lymphoma and lymphoblastoid cell lines from Burkitt’s lymphoma patients: comparative sensitivity to non-specific and to allo-specific cytotoxic responses in vitro. Int J Cancer 34:339–348, 1984.PubMedCrossRefGoogle Scholar
  33. Rooney C M, Gregory C D, Rowe M, Finerty S, Edwards C, Rupani H and Rickinson A B: Endemic Burkitt’s lymphoma: phenotypic analysis of tumor biopsy cells and of derived tumor cell lines. JNCI 77: 681–687, 1986.PubMedGoogle Scholar
  34. Rowe M, D T Rowe, Gregory C D, Young L S, Farrell, P J, Rupani H and Rickinson A B: Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt’s lymphoma cells. The EMBO Journal, 6:2743–2751 1987.PubMedCentralPubMedGoogle Scholar
  35. Sakthivel R, Christensson B, Ehlin-Henriksson B and Klein G: Immunophenotypic characterization of follicle center cell derived non-Hodgkin’s lymphoma. Int J Cancer 43:624–63 0, 1989.PubMedCrossRefGoogle Scholar
  36. Torsteinsdottir S, Brautbar C, Klein G, Klein E and Masucci M G: Differential expression of HLA antigens on human B-cell lines of normal and malignant origin: a consequence of immune surveillance or a phenotypic vestige of the progenitor cells? Int J Cancer 41:913–919, 1988.PubMedCrossRefGoogle Scholar
  37. Torsteinsdottir S, Andersson M L, Avila-Carino J, Ehün-Henriksson B, Masucci M G, Klein G and Klein E: Reversion of tumorigenicity and decreased agarose clonability after EBV conversion of an IgH/myc translocation carrying BL line. Int J Cancer 43:273–278, 1989.PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 1989

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  • G. Klein

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