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. 1983;2(2):213–216. doi: 10.1002/j.1460-2075.1983.tb01407.x

Fusion of DNA region to murine immunoglobulin heavy chain locus corresponds to plasmacytoma-associated chromosome translocation.

S Cory 1, J M Adams 1, S D Gerondakis 1, J F Miller 1, J Gamble 1, F Wiener 1, J Spira 1, U Francke 1
PMCID: PMC555115  PMID: 11894928

Abstract

Murine plasmacytomas frequently exhibit a translocation of the distal region of chromosome 15 to the end of chromosome 12, where the immunoglobulin heavy chain locus resides. A candidate for the DNA across the chromosome fusion point is a cloned region of non-immunoglobulin DNA which in most plasmacytomas has recombined near the alpha heavy chain constant region gene. That the incoming DNA, provisionally designated LyR (lymphoid rearranging) DNA, does derive from chromosome 15 is shown here by blot analysis of DNA from two panels of somatic cell hybrids: hybridomas between an AKR T-lymphoma (Tikaut) and CBA mouse cells with a cytogenetically distinctive chromosome 15, and between mouse and Chinese hamster cells. LyR DNA segregated with chromosome 15 in all lines and the results assign LyR to the distal two thirds of that chromosome. This assignment, together with the previously reported high frequency of recombination between LyR and C(alpha) in plasmacytomas and associated alteration of LyR transcription suggests that translocation activates a LyR gene involved in plasmacytoma oncogenesis. Moreover, LyR rearrangement in certain T-lymphomas, such as the Tikaut line examined here, also implicate that gene in oncogenesis of some T-lymphomas.

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Selected References

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

  1. Adams J. M., Gerondakis S., Webb E., Mitchell J., Bernard O., Cory S. Transcriptionally active DNA region that rearranges frequently in murine lymphoid tumors. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6966–6970. doi: 10.1073/pnas.79.22.6966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Calame K., Kim S., Lalley P., Hill R., Davis M., Hood L. Molecular cloning of translocations involving chromosome 15 and the immunoglobulin C alpha gene from chromosome 12 in two murine plasmacytomas. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6994–6998. doi: 10.1073/pnas.79.22.6994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cory S., Adams J. M. Deletions are associated with somatic rearrangement of immunoglobulin heavy chain genes. Cell. 1980 Jan;19(1):37–51. doi: 10.1016/0092-8674(80)90386-4. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. D'Eustachio P., Pravtcheva D., Marcu K., Ruddle F. H. Chromosomal location of the structural gene cluster encoding murine immunoglobulin heavy chains. J Exp Med. 1980 Jun 1;151(6):1545–1550. doi: 10.1084/jem.151.6.1545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Davis M. M., Kim S. K., Hood L. Immunoglobulin class switching: developmentally regulated DNA rearrangements during differentiation. Cell. 1980 Nov;22(1 Pt 1):1–2. doi: 10.1016/0092-8674(80)90145-2. [DOI] [PubMed] [Google Scholar]
  7. Erikson J., Finan J., Nowell P. C., Croce C. M. Translocation of immunoglobulin VH genes in Burkitt lymphoma. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5611–5615. doi: 10.1073/pnas.79.18.5611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Erikson J., Martinis J., Croce C. M. Assignment of the genes for human lambda immunoglobulin chains to chromosome 22. Nature. 1981 Nov 12;294(5837):173–175. doi: 10.1038/294173a0. [DOI] [PubMed] [Google Scholar]
  9. Francke U., Tetri P., Taggart R. T., Oliver N. Conserved autosomal syntenic group on mouse (MMU) chromosome 15 and human (HSA) chromosome 22: assignment of a gene for arylsulfatase A to MMU 15 and regional mapping of DIA1, ARSA, and ACO2 on HSA 22. Cytogenet Cell Genet. 1981;31(2):58–69. doi: 10.1159/000131626. [DOI] [PubMed] [Google Scholar]
  10. Harris L. J., D'Eustachio P., Ruddle F. H., Marcu K. B. DNA sequence associated with chromosome translocations in mouse plasmacytomas. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6622–6626. doi: 10.1073/pnas.79.21.6622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  12. Hengartner H., Meo T., Müller E. Assignment of genes for immunoglobulin kappa and heavy chains to chromosomes 6 and 12 in mouse. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4494–4498. doi: 10.1073/pnas.75.9.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kirsch I. R., Morton C. C., Nakahara K., Leder P. Human immunoglobulin heavy chain genes map to a region of translocations in malignant B lymphocytes. Science. 1982 Apr 16;216(4543):301–303. doi: 10.1126/science.6801764. [DOI] [PubMed] [Google Scholar]
  14. Kirsch I. R., Ravetch J. V., Kwan S. P., Max E. E., Ney R. L., Leder P. Multiple immunoglobulin switch region homologies outside the heavy chain constant region locus. Nature. 1981 Oct 15;293(5833):585–587. doi: 10.1038/293585a0. [DOI] [PubMed] [Google Scholar]
  15. Klein G., Ohno S., Rosenberg N., Wiener F., Spira J., Baltimore D. Cytogenetic studies on abelson-virus-induced mouse leukemias. Int J Cancer. 1980 Jun 15;25(6):805–811. doi: 10.1002/ijc.2910250617. [DOI] [PubMed] [Google Scholar]
  16. Klein G. The role of gene dosage and genetic transpositions in carcinogenesis. Nature. 1981 Nov 26;294(5839):313–318. doi: 10.1038/294313a0. [DOI] [PubMed] [Google Scholar]
  17. Malcolm S., Barton P., Murphy C., Ferguson-Smith M. A., Bentley D. L., Rabbitts T. H. Localization of human immunoglobulin kappa light chain variable region genes to the short arm of chromosome 2 by in situ hybridization. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4957–4961. doi: 10.1073/pnas.79.16.4957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Manolov G., Manolova Y. Marker band in one chromosome 14 from Burkitt lymphomas. Nature. 1972 May 5;237(5349):33–34. doi: 10.1038/237033a0. [DOI] [PubMed] [Google Scholar]
  19. McBride O. W., Hieter P. A., Hollis G. F., Swan D., Otey M. C., Leder P. Chromosomal location of human kappa and lambda immunoglobulin light chain constant region genes. J Exp Med. 1982 May 1;155(5):1480–1490. doi: 10.1084/jem.155.5.1480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meo T., Johnson J., Beechey C. V., Andrews S. J., Peters J., Searle A. G. Linkage analyses of murine immunoglobulin heavy chain and serum prealbumin genes establish their location on chromosome 12 proximal to the T (5;12) 31H breakpoint in band 12F1. Proc Natl Acad Sci U S A. 1980 Jan;77(1):550–553. doi: 10.1073/pnas.77.1.550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ohno S., Babonits M., Wiener F., Spira J., Klein G., Potter M. Nonrandom chromosome changes involving the Ig gene-carrying chromosomes 12 and 6 in pristane-induced mouse plasmacytomas. Cell. 1979 Dec;18(4):1001–1007. doi: 10.1016/0092-8674(79)90212-5. [DOI] [PubMed] [Google Scholar]
  22. Owen F. L., Riblet R., Taylor B. A. The T suppressor cell alloantigen Tsud maps near immunoglobulin allotype genes and may be an heavy chain constant-region marker on a T cell receptor. J Exp Med. 1981 Apr 1;153(4):801–810. doi: 10.1084/jem.153.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  24. Rowley J. D. Identification of the constant chromosome regions involved in human hematologic malignant disease. Science. 1982 May 14;216(4547):749–751. doi: 10.1126/science.7079737. [DOI] [PubMed] [Google Scholar]
  25. Rowley J. D., Testa J. R. Chromosome abnormalities in malignant hematologic diseases. Adv Cancer Res. 1982;36:103–148. doi: 10.1016/s0065-230x(08)60423-6. [DOI] [PubMed] [Google Scholar]
  26. Shepard J. S., Pettengill O. S., Wurster-Hill D. H., Sorenson G. D. A specific chromosome breakpoint associated with mouse plasmacytomas. J Natl Cancer Inst. 1978 Jul;61(1):255–258. doi: 10.1093/jnci/61.1.255. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Spira J., Babonits M., Wiener F., Ohno S., Wirschubski Z., Haran-Ghera N., Klein G. Nonrandom chromosomal changes in thy-1-positive and thy-1-negative lymphomas induced by 7,12-dimethylbenzanthracene in SJL mice. Cancer Res. 1980 Jul;40(7):2609–2616. [PubMed] [Google Scholar]
  29. Spira J., Wiener F., Babonits M., Gamble J., Miller J., Klein G. The role of chromosome 15 in murine leukemogenesis. I. Contrasting behavior of the tumor vs. normal parent-derived chromosomes No. 15 in somatic hybrids of varying tumorigenicity. Int J Cancer. 1981 Dec;28(6):785–798. doi: 10.1002/ijc.2910280618. [DOI] [PubMed] [Google Scholar]
  30. Swan D., D'Eustachio P., Leinwand L., Seidman J., Keithley D., Ruddle F. H. Chromosomal assignment of the mouse kappa light chain genes. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2735–2739. doi: 10.1073/pnas.76.6.2735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Taggart R. T., Tetri P., Francke U. Assignment of the gene for NADH diaphorase Dia-1 to Mouse chromosome 15. Somatic Cell Genet. 1980 Nov;6(6):769–776. doi: 10.1007/BF01538975. [DOI] [PubMed] [Google Scholar]
  32. Wiener F., Babonits M., Spira J., Bregula U., Klein G., Merwin R. M., Asofsky R., Lynes M., Haughton G. Chromosome 15 trisomy in spontaneous and carcinogen-induced murine lymphomas of B-cell origin. Int J Cancer. 1981 Jan 15;27(1):51–58. doi: 10.1002/ijc.2910270109. [DOI] [PubMed] [Google Scholar]
  33. Wiener F., Babonits M., Spira J., Klein G., Potter M. Cytogenetic studies on IgA/lambda-producing murine plasmacytomas: regular occurrence of a T(12;15) translocation. Somatic Cell Genet. 1980 Nov;6(6):731–738. doi: 10.1007/BF01538972. [DOI] [PubMed] [Google Scholar]

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