Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1987 Jul;7(7):2614–2619. doi: 10.1128/mcb.7.7.2614

Rearrangement of rat immunoglobulin E heavy-chain and c-myc genes in the B-cell immunocytoma IR162.

S S Tian, C Faust
PMCID: PMC365400  PMID: 3112560

Abstract

Mammalian B-cell lymphoid malignancies frequently display aberrant translocations involving the c-myc proto-oncogene and one of the immunoglobulin loci. We have observed and characterized such a translocation in the immunoglobulin E-producing rat immunocytoma IR162 by using recombinant DNA technology. We show here for the first time that a c-myc gene has recombined with the excluded allele of the nonfunctional epsilon heavy-chain immunoglobulin gene. This recombination has resulted in the loss of 5'-proximal DNA and, consequently, potential regulatory information from the body of the c-myc structural gene via joining to the epsilon heavy-chain switch region in a head-to-head, i.e., 5'-to-5', configuration. As discussed in this report, these results, together with the previous results of others, have important implications for immunoglobulin heavy-chain class switching mechanisms controlling normal and abnormal translocations.

Full text

PDF
2614

Images in this article

2618Image
on p.2618
2618Image
on p.2618

Selected References

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

  1. Battey J., Moulding C., Taub R., Murphy W., Stewart T., Potter H., Lenoir G., Leder P. The human c-myc oncogene: structural consequences of translocation into the IgH locus in Burkitt lymphoma. Cell. 1983 Oct;34(3):779–787. doi: 10.1016/0092-8674(83)90534-2. [DOI] [PubMed] [Google Scholar]
  2. Chung J., Sinn E., Reed R. R., Leder P. Trans-acting elements modulate expression of the human c-myc gene in Burkitt lymphoma cells. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7918–7922. doi: 10.1073/pnas.83.20.7918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cole M. D. The myc oncogene: its role in transformation and differentiation. Annu Rev Genet. 1986;20:361–384. doi: 10.1146/annurev.ge.20.120186.002045. [DOI] [PubMed] [Google Scholar]
  4. Cory S. Activation of cellular oncogenes in hemopoietic cells by chromosome translocation. Adv Cancer Res. 1986;47:189–234. doi: 10.1016/s0065-230x(08)60200-6. [DOI] [PubMed] [Google Scholar]
  5. Faust C. H., Jr, Moore J. M. Physical and biological properties of an epsilon-heavy chain mRNA and a kappa-light chain mRNA coding for rat immunoglobulin E. J Biol Chem. 1981 Mar 10;256(5):2262–2267. [PubMed] [Google Scholar]
  6. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  7. Finger L. R., Harvey R. C., Moore R. C., Showe L. C., Croce C. M. A common mechanism of chromosomal translocation in T- and B-cell neoplasia. Science. 1986 Nov 21;234(4779):982–985. doi: 10.1126/science.3490692. [DOI] [PubMed] [Google Scholar]
  8. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  9. Hurwitz J. L., Coleclough C., Cebra J. J. CH gene rearrangements in IgM-bearing B cells and in the normal splenic DNA component of hybridomas making different isotypes of antibody. Cell. 1980 Nov;22(2 Pt 2):349–359. doi: 10.1016/0092-8674(80)90345-1. [DOI] [PubMed] [Google Scholar]
  10. Kindsvogel W. R., Reddy E. P., Moore J. M., Faust C. H., Jr A cloned cDNA probe for rat immunoglobulin epsilon heavy chain: construction, identification, and DNA sequence. DNA. 1982;1(4):335–343. doi: 10.1089/dna.1982.1.335. [DOI] [PubMed] [Google Scholar]
  11. Klein G., Klein E. Evolution of tumours and the impact of molecular oncology. Nature. 1985 May 16;315(6016):190–195. doi: 10.1038/315190a0. [DOI] [PubMed] [Google Scholar]
  12. Leder P., Battey J., Lenoir G., Moulding C., Murphy W., Potter H., Stewart T., Taub R. Translocations among antibody genes in human cancer. Science. 1983 Nov 18;222(4625):765–771. doi: 10.1126/science.6356357. [DOI] [PubMed] [Google Scholar]
  13. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  14. Mitchell K. F., Battey J., Hollis G. F., Moulding C., Taub R., Leder P. The effect of translocations on the cellular myc gene in Burkitt lymphomas. J Cell Physiol Suppl. 1984;3:171–177. doi: 10.1002/jcp.1041210420. [DOI] [PubMed] [Google Scholar]
  15. Nikaido T., Yamawaki-Kataoka Y., Honjo T. Nucleotide sequences of switch regions of immunoglobulin C epsilon and C gamma genes and their comparison. J Biol Chem. 1982 Jul 10;257(13):7322–7329. [PubMed] [Google Scholar]
  16. Pear W. S., Ingvarsson S., Steffen D., Münke M., Francke U., Bazin H., Klein G., Sümegi J. Multiple chromosomal rearrangements in a spontaneously arising t(6;7) rat immunocytoma juxtapose c-myc and immunoglobulin heavy chain sequences. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7376–7380. doi: 10.1073/pnas.83.19.7376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rabbitts T. H., Forster A., Hamlyn P., Baer R. Effect of somatic mutation within translocated c-myc genes in Burkitt's lymphoma. Nature. 1984 Jun 14;309(5969):592–597. doi: 10.1038/309592a0. [DOI] [PubMed] [Google Scholar]
  18. Radbruch A., Sablitzky F. Deletion of Cmu genes in mouse B lymphocytes upon stimulation with LPS. EMBO J. 1983;2(11):1929–1935. doi: 10.1002/j.1460-2075.1983.tb01681.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Reed K. C., Mann D. A. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res. 1985 Oct 25;13(20):7207–7221. doi: 10.1093/nar/13.20.7207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Remmers E. F., Yang J. Q., Marcu K. B. A negative transcriptional control element located upstream of the murine c-myc gene. EMBO J. 1986 May;5(5):899–904. doi: 10.1002/j.1460-2075.1986.tb04301.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shimizu A., Takahashi N., Yamawaki-Kataoka Y., Nishida Y., Kataoka T., Honjo T. Ordering of mouse immunoglobulin heavy chain genes by molecular cloning. Nature. 1981 Jan 15;289(5794):149–153. doi: 10.1038/289149a0. [DOI] [PubMed] [Google Scholar]
  22. Stanton L. W., Watt R., Marcu K. B. Translocation, breakage and truncated transcripts of c-myc oncogene in murine plasmacytomas. Nature. 1983 Jun 2;303(5916):401–406. doi: 10.1038/303401a0. [DOI] [PubMed] [Google Scholar]
  23. Steen M. L., Hellman L., Pettersson U. Rat immunoglobulin E heavy chain locus. J Mol Biol. 1984 Jul 25;177(1):19–32. doi: 10.1016/0022-2836(84)90055-x. [DOI] [PubMed] [Google Scholar]
  24. Stein L. D., Chan M. A., Hibi T., Dosch H. M. Epstein-Barr virus-induced IgE production in limiting dilution cultures of normal human B cells. Eur J Immunol. 1986 Sep;16(9):1167–1170. doi: 10.1002/eji.1830160922. [DOI] [PubMed] [Google Scholar]
  25. Sümegi J., Spira J., Bazin H., Szpirer J., Levan G., Klein G. Rat c-myc oncogene is located on chromosome 7 and rearranges in immunocytomas with t(6:7) chromosomal translocation. Nature. 1983 Dec 1;306(5942):497–498. doi: 10.1038/306497a0. [DOI] [PubMed] [Google Scholar]
  26. Taub R., Kirsch I., Morton C., Lenoir G., Swan D., Tronick S., Aaronson S., Leder P. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7837–7841. doi: 10.1073/pnas.79.24.7837. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES