Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1988 Mar 25;16(5 Pt B):2077–2085. doi: 10.1093/nar/16.5.2077

The t(8;14) breakpoint of the EW 36 undifferentiated lymphoma cell line lies 5' of MYC in a region prone to involvement in endemic Burkitt's lymphomas.

F G Haluska 1, Y Tsujimoto 1, C M Croce 1
PMCID: PMC338200  PMID: 3128772

Abstract

One of the best analyzed tumor-specific cytogenetic abnormalities is the t(8;14) chromosomal translocation observed in cases of Burkitt's and undifferentiated lymphomas (ULs), and acute lymphoblastic leukemias (ALLs). Here we analyze the cloned (8;14) chromosomal breakpoint of the UL cell line EW 36. We show that the region of chromosome 8 involved in the translocation is situated near a site previously demonstrated to harbor a cluster of endemic Burkitt's lymphoma breakpoints, approximately 50 kb 5' of MYC. In those cases, we demonstrated that malfunction of the V-D-J recombinase generated the translocations. However, in this case the isotype switch mechanism of translocation is implicated: at the breakpoint, S mu/S gamma and C gamma sequences are found on chromosome 14. Thus, the features of the EW 36 t(8;14) breakpoint are consonant with our model for B-cell lymphomagenesis which relates the precursor cell that gives rise to malignancy, the mechanism of translocation, and the phenotype of the tumor.

Full text

PDF
2077

Images in this article

2080Image
on p.2080
2080Image
on p.2080
2081Image
on p.2081

Selected References

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

  1. Alexander A., Steinmetz M., Barritault D., Frangione B., Franklin E. C., Hood L., Buxbaum J. N. gamma Heavy chain disease in man: cDNA sequence supports partial gene deletion model. Proc Natl Acad Sci U S A. 1982 May;79(10):3260–3264. doi: 10.1073/pnas.79.10.3260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benjamin D., Magrath I. T., Maguire R., Janus C., Todd H. D., Parsons R. G. Immunoglobulin secretion by cell lines derived from African and American undifferentiated lymphomas of Burkitt's and non-Burkitt's type. J Immunol. 1982 Sep;129(3):1336–1342. [PubMed] [Google Scholar]
  3. Croce C. M., Shander M., Martinis J., Cicurel L., D'Ancona G. G., Dolby T. W., Koprowski H. Chromosomal location of the genes for human immunoglobulin heavy chains. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3416–3419. doi: 10.1073/pnas.76.7.3416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dalla-Favera R., Bregni M., Erikson J., Patterson D., Gallo R. C., Croce C. M. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7824–7827. doi: 10.1073/pnas.79.24.7824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ellison J., Hood L. Linkage and sequence homology of two human immunoglobulin gamma heavy chain constant region genes. Proc Natl Acad Sci U S A. 1982 Mar;79(6):1984–1988. doi: 10.1073/pnas.79.6.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Flanagan J. G., Rabbitts T. H. Arrangement of human immunoglobulin heavy chain constant region genes implies evolutionary duplication of a segment containing gamma, epsilon and alpha genes. Nature. 1982 Dec 23;300(5894):709–713. doi: 10.1038/300709a0. [DOI] [PubMed] [Google Scholar]
  7. Gelmann E. P., Psallidopoulos M. C., Papas T. S., Dalla-Favera R. Identification of reciprocal translocation sites within the c-myc oncogene and immunoglobulin mu locus in a Burkitt lymphoma. Nature. 1983 Dec 22;306(5945):799–803. doi: 10.1038/306799a0. [DOI] [PubMed] [Google Scholar]
  8. Haluska F. G., Finver S., Tsujimoto Y., Croce C. M. The t(8; 14) chromosomal translocation occurring in B-cell malignancies results from mistakes in V-D-J joining. Nature. 1986 Nov 13;324(6093):158–161. doi: 10.1038/324158a0. [DOI] [PubMed] [Google Scholar]
  9. Haluska F. G., Huebner K., Croce C. M. p380-8A 1.8 SaSs, a single copy clone 5' of c-myc at 8q24 which recognizes an SstI polymorphism. Nucleic Acids Res. 1987 Jan 26;15(2):865–865. doi: 10.1093/nar/15.2.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Haluska F. G., Tsujimoto Y., Croce C. M. Oncogene activation by chromosome translocation in human malignancy. Annu Rev Genet. 1987;21:321–345. doi: 10.1146/annurev.ge.21.120187.001541. [DOI] [PubMed] [Google Scholar]
  11. Haluska F. G., Tsujimoto Y., Croce C. M. The t(8;14) chromosome translocation of the Burkitt lymphoma cell line Daudi occurred during immunoglobulin gene rearrangement and involved the heavy chain diversity region. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6835–6839. doi: 10.1073/pnas.84.19.6835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hamlyn P. H., Rabbitts T. H. Translocation joins c-myc and immunoglobulin gamma 1 genes in a Burkitt lymphoma revealing a third exon in the c-myc oncogene. Nature. 1983 Jul 14;304(5922):135–139. doi: 10.1038/304135a0. [DOI] [PubMed] [Google Scholar]
  13. Krawinkel U., Rabbitts T. H. Comparison of the hinge-coding segments in human immunoglobulin gamma heavy chain genes and the linkage of the gamma 2 and gamma 4 subclass genes. EMBO J. 1982;1(4):403–407. doi: 10.1002/j.1460-2075.1982.tb01182.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Magrath I. T., Freeman C. B., Pizzo P., Gadek J., Jaffe E., Santaella M., Hammer C., Frank M., Reaman G., Novikovs L. Characterization of lymphoma-derived cell lines: comparison of cell lines positive and negative for Epstein-Barr virus nuclear antigen. II. Surface markers. J Natl Cancer Inst. 1980 Mar;64(3):477–483. [PubMed] [Google Scholar]
  15. Magrath I. T., Pizzo P. A., Whang-Peng J., Douglass E. C., Alabaster O., Gerber P., Freeman C. B., Novikovs L. Characterization of lymphoma-derived cell lines: comparison of cell lines positive and negative for Epstein-Barr virus nuclear antigen. I. Physical, cytogenetic, and growth characteristics. J Natl Cancer Inst. 1980 Mar;64(3):465–476. [PubMed] [Google Scholar]
  16. Nishikura K., Erikson J., ar-Rushdi A., Huebner K., Croce C. M. The translocated c-myc oncogene of Raji Burkitt lymphoma cells is not expressed in human lymphoblastoid cells. Proc Natl Acad Sci U S A. 1985 May;82(9):2900–2904. doi: 10.1073/pnas.82.9.2900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ott D. E., Alt F. W., Marcu K. B. Immunoglobulin heavy chain switch region recombination within a retroviral vector in murine pre-B cells. EMBO J. 1987 Mar;6(3):577–584. doi: 10.1002/j.1460-2075.1987.tb04793.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pelicci P. G., Knowles D. M., 2nd, Magrath I., Dalla-Favera R. Chromosomal breakpoints and structural alterations of the c-myc locus differ in endemic and sporadic forms of Burkitt lymphoma. Proc Natl Acad Sci U S A. 1986 May;83(9):2984–2988. doi: 10.1073/pnas.83.9.2984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rabbitts T. H., Forster A., Milstein C. P. Human immunoglobulin heavy chain genes: evolutionary comparisons of C mu, C delta and C gamma genes and associated switch sequences. Nucleic Acids Res. 1981 Sep 25;9(18):4509–4524. doi: 10.1093/nar/9.18.4509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rabbitts T. H., Hamlyn P. H., Baer R. Altered nucleotide sequences of a translocated c-myc gene in Burkitt lymphoma. Nature. 1983 Dec 22;306(5945):760–765. doi: 10.1038/306760a0. [DOI] [PubMed] [Google Scholar]
  21. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Showe L. C., Ballantine M., Nishikura K., Erikson J., Kaji H., Croce C. M. Cloning and sequencing of a c-myc oncogene in a Burkitt's lymphoma cell line that is translocated to a germ line alpha switch region. Mol Cell Biol. 1985 Mar;5(3):501–509. doi: 10.1128/mcb.5.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Showe L. C., Moore R. C., Erikson J., Croce C. M. MYC oncogene involved in a t(8;22) chromosome translocation is not altered in its putative regulatory regions. Proc Natl Acad Sci U S A. 1987 May;84(9):2824–2828. doi: 10.1073/pnas.84.9.2824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  25. Takahashi N., Ueda S., Obata M., Nikaido T., Nakai S., Honjo T. Structure of human immunoglobulin gamma genes: implications for evolution of a gene family. Cell. 1982 Jun;29(2):671–679. doi: 10.1016/0092-8674(82)90183-0. [DOI] [PubMed] [Google Scholar]
  26. Tsujimoto Y., Gorham J., Cossman J., Jaffe E., Croce C. M. The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science. 1985 Sep 27;229(4720):1390–1393. doi: 10.1126/science.3929382. [DOI] [PubMed] [Google Scholar]
  27. Tsujimoto Y., Jaffe E., Cossman J., Gorham J., Nowell P. C., Croce C. M. Clustering of breakpoints on chromosome 11 in human B-cell neoplasms with the t(11;14) chromosome translocation. Nature. 1985 May 23;315(6017):340–343. doi: 10.1038/315340a0. [DOI] [PubMed] [Google Scholar]
  28. Yunis J. J. The chromosomal basis of human neoplasia. Science. 1983 Jul 15;221(4607):227–236. doi: 10.1126/science.6336310. [DOI] [PubMed] [Google Scholar]
  29. ar-Rushdi A., Nishikura K., Erikson J., Watt R., Rovera G., Croce C. M. Differential expression of the translocated and the untranslocated c-myc oncogene in Burkitt lymphoma. Science. 1983 Oct 28;222(4622):390–393. doi: 10.1126/science.6414084. [DOI] [PubMed] [Google Scholar]

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

RESOURCES