Skip to main content
Log in

Interaction of H-2Eb with an IAP retrotransposon in the A20/2J B cell lymphoma

  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

In the A20/2J BALB/c B cell lymphoma, Southern analysis revealed an insertion of approximately 6 kilobases of DNA into the first intron of one Eb d-allele. Two observations suggest that the rearrangement did not occur recently in the A20/2J subline. Firstly, normal and altered Eb d-alleles are present in equal numbers, and secondly, the LB 27.4 and LS 102.9 somatic cell hybrids formed at an earlier date both possess the rearrangement. Sequences of two cDNA clones, λEb-7 and λEb-125, selected from an A20/2J cDNA library prepared from poly [A+] RNA indicate that the rearranged Eb d-allele directs the synthesis of atypical Eb transcripts. The clones contain Eb sequence linked to a portion of retroviral-like intracisternal A-particle (IAP) genomic sequence, and they appear to be copies of mRNA produced by splicing between a 5′ donor site in the retroviral transcript and the 3′ acceptor site of the Eb gene's first intron. The longer λEb-125 insert corresponds to RNA that initiated in the 5′-untranslated region of the Eb gene. The 3′-end of the first Eb exon joins to long terminal repeat sequence, and retroviral sequence extends up to the splice junction with the second Eb exon; 3′ of the junction, the λEb-125 sequence corresponds to that of a correctly spliced Eb transcript. It seems feasible that the cDNA clones represent hybrid RNA synthesized by read-through transcription of the Eb coding region and an IAP element inserted into the first intron of the rearranged Eb d-allele.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L., and Wiley, D. C.: The foreign antigen binding site and T cell recognition regions of class I histocompatability antigens. Nature 329: 512–518, 1987

    Google Scholar 

  • Blankenstein, T., Qin, Z., Li, W., and Diamanstein, T.: DNA rearrangement and constitutive expression of the interleukin 6 gene in a mouse plasmacytoma. J Exp Med 171: 965–970, 1990

    Google Scholar 

  • Blatt, C., Aberdam, D., Schwartz, R., and Sachs, L.: DNA rearrangement of a homeobox gene in myeloid leukaemic cells. EMBO J 7: 4283–4290, 1988

    Google Scholar 

  • Breathnach, R. and Chambon, P.: Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50: 349–383, 1981

    Article  CAS  PubMed  Google Scholar 

  • Brown, J. H., Jardetzky, T., Saper, M. A., Samraoui, B., Bjorkman, P. J., and Wiley, D. C.: A hypothetical model of the foreign antigen binding site of class II histocompatibility molecules. Nature 332: 845–850, 1988

    Article  CAS  PubMed  Google Scholar 

  • Canaani, E., Dreazen, O., Klar, A., Rechavi, G., Ram, D., Cohen, J. B., and Givol, D.: Activation of the c-mos oncogene in a mouse plasmacytoma by insertion of an endogenous intracisternal A-particle genome. Proc Natl Acad Sci USA 80: 7118–7122, 1983

    Google Scholar 

  • Dalton, A. J., Potter, M., and Merwin, R. M.: Some ultrastructural characteristics of a series of primary and transplanted plasma cell tumors of the mouse. J Nat Cancer Inst 26: 1221–1267, 1961

    Google Scholar 

  • Gillies, S. D., Folsom, V., and Tonegawa, S.: Cell type-specific enhancer element associated with a mouse MHC gene, Eβ. Nature 310: 594–597, 1984

    Google Scholar 

  • Gopinathan, K. P., Weymouth, L. A., Kunkel, T. A., and Loeb, L. A.: Mutagenesis in vitro by DNA polymerase from an RNA tumor virus. Nature 278: 857–859, 1979

    Google Scholar 

  • Grossman, Z., Mietz, J. A., and Kuff, E. L.: Nearly identical members of the heterogeneous IAP gene family are expressed in thymus of different mouse strains. Nucleic Acids Res 15: 3823–3834, 1987

    Google Scholar 

  • Gubler, U. and Hoffman, B. J.: A simple and very efficient method for generating cDNA libraries. Gene 25: 263–269, 1983

    Google Scholar 

  • Hawley, R. G., Shulman, M. J., and Hozumi, N.: Transposition of two different intracisternal A particle elements into an immunoglobulin kappa-chain gene. Mol Cell Biol 4: 2565–2572, 1984

    Google Scholar 

  • Hawley, R. G., Shulman, M. J., and Hozumi, N.: Intracisternal A-particle genes: a family of copia-like transposable elements in Mus musculus. In G. F. Van de Woude, A. J. Levine, W. C. Topp, and J. D. Walsh (eds.): Cancer Cells 2 Oncogenes and Viral Genes, pp. 273–279, Cold Spring Harbor Press, New York, 1987

    Google Scholar 

  • Henry, C., Marbrook, J., Vann, D. C., Kodlin, D., and Wofsy, C.: Limiting dilution analysis. In B. B. Mishell and S. M. Shiigi (eds.): Selected Methods in Cellular Immunology, p. 138, W. H. Freeman, San Francisco, 1980

    Google Scholar 

  • Jones, B., Tite, J. P., and Janeway Jr. C. A.: Different phenotypic variants of the mouse B cell tumor A20/2J are selected by antigen- and mitogen-triggered cytotoxicity of L2T4-positive, Ia-restricted T cell clones. J Immunol 136: 348–356, 1986

    CAS  PubMed  Google Scholar 

  • Kappler, J., White, J., Wegmann, D., Mustain, E., and Marrack, P.: Antigen presentation by Ia+ B cell hybridomas to H-2-restricted T cell hybridomas. Proc Natl Acad Sci USA 79: 3604–3607, 1982

    Google Scholar 

  • Larhammar, D., Hammerling, U., Denaro, M., Lund, T., Flavell, R. A., Rask, L., and Peterson, P. A.: Structure of the murine immune response I-Aβ locus: sequence of the I-Aβ gene and an adjacent β-chain second domain exon. Cell 34: 179–188, 1983

    Google Scholar 

  • Maniatis, T., Fritsch, E. F., and Sambrook, J.: Isolation of high-molecular-weight, eukaryotic DNA from cells grown in tissue culture. In T. Maniatis, E. F. Fritsch, and J. Sambrook (eds.): Molecular Cloning: a Laboratory Manual, pp. 280–281, Cold Spring Harbor Laboratory, New York, 1982a

    Google Scholar 

  • Maniatis, T., Fritsch, E. F., and Sambrook, J.: Southern transfer. In T. Maniatis, E. F. Fritsch, and J. Sambrook (eds.): Molecular Cloning: a Laboratory Manual, pp. 382–386, Cold Spring Harbor Laboratory, New York, 1982b

    Google Scholar 

  • Maniatis, T., Fritsch, E. F., and Sambrook, J.: Escherichia coli DNA polymerase I. In T. Maniatis, E. F. Fritsch, and J. Sambrook (eds.): Molecular Cloning: a Laboratory Manual, pp. 108–112, Cold Spring Harbor Laboratory, New York, 1982c

    Google Scholar 

  • Maniatis, T., Fritsch, E. F., and Sambrook, J.: The identification of recombinant clones. In T. Maniatis, E. F. Fritsch, and J. Sambrook (eds.): Molecular Cloning: a Laboratory Manual, pp. 320–321, Cold Spring Harbor Laboratory, New York, 1982d

    Google Scholar 

  • Mengle-Gaw, L. and McDevitt, H. O.: Isolation and characterization of a cDNA clone for the murine I-Eβ polypeptide chain. Proc Natl Acad Sci USA 80: 7621–7625, 1983

    Google Scholar 

  • Rogers, M. J., Germain, R. N., Hare, J., Long, E., and Singer, D. S.: Comparison of MHC genes among distantly related members of the genus Mus. J Immunol 134: 630–636, 1985

    Google Scholar 

  • Rosloniec, E. F., Vitez, L. J., Buus, S., and Freed, J. H.: MHC class II-derived peptides can bind to class II molecules, including self molecules, and prevent antigen presentation. J Exp Med 171: 1419–1430, 1990

    Google Scholar 

  • Saito, H., Maki, R. A., Clayton, L. K., and Tonegawa, S.: Complete primary structure of the Eβ chain and gene of the mouse major histocompatibility complex. Proc Natl Acad Sci USA 80: 5520–5524, 1983

    Google Scholar 

  • Sanger, F., Miklen, S., and Coulson, A. R.: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467, 1977

    CAS  PubMed  Google Scholar 

  • Scholl, T., Pitcock, A., and Jones, B.: Hypomethylation of MHC class II Eb gene is associated with expression. Immunogenetics 36, this issue

  • Shapiro, M. B. and Senapathy, P.: RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res 17: 7155–7174, 1987

    Google Scholar 

  • Steinmetz, M., Minard, K., Horvath, S., McNicholas, J., Frelinger, J., Wake, C., Long, E., Mach, B., and Hood, L.: A molecular map of the immune response region from the major histocompatibility complex of the mouse. Nature 300: 35–42, 1982

    Google Scholar 

  • Tite, J. P. and Janeway, C. A.: Antigen-dependent selection of B lymphoma cells varying in Ia density by cloned antigen-specific L3T4+ T cells: a possible in vitro model for B cell adaptive differentiation. J Mol Cell Immunol 1: 253–265, 1981

    Google Scholar 

  • Varmus, H. and Swanstrom, R.: Retroviral replication. In R. Weiss, N. Teich, H. Varmus, and J. Coffin (eds.): RNA Tumor Viruses 2/Supplement and Appendixes, pp. 75–134, Cold Spring Harbor Press Spring Harbor, 1984

    Google Scholar 

  • Widera, G. and Flavell, R. A.: The nucleotide sequence of the murine I-E bβ immune response gene: evidence for gene conversion events in class II genes of the major histocompatibility complex. EMBO J 3: 1221–1225, 1984

    Google Scholar 

  • Wilson, S. H. and Kuff, E. D.: A novel DNA polymerase activity found in association with intracisternal A-type particles. Proc Natl Acad Sci USA 69: 1531–1536, 1972

    Google Scholar 

  • Ymer, S., Tucker, W. Q. J., Sanderson, C.J., Hapel, A. J., Campbell, H. D., and Young, I. G.: Constitutive synthesis of interleukin-3 by leukemia cell line WEHI-3B is due to retroviral insertion near the gene. Nature 317: 255–258, 1985

    Google Scholar 

  • Ymer, S., Tucker, W. Q. J., Campbell, H. D., and Young, I. G.: Nucleotide sequence of the intracisternal A-particle genome inserted 5′ to the interleukin-3 gene ofthe leukemia cell line WEHI-3B. Nucleic Acids Res 14: 5901–5918, 1986

    Google Scholar 

  • Zinkernagel, R. M. and Doherty, P. C.: Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248: 701–702, 1974

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers: M73959 and M73960 for Eb-7 and Eb-125 respectively.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Malstrom, C.E., Kotsenas, A.L. & Jones, B. Interaction of H-2Eb with an IAP retrotransposon in the A20/2J B cell lymphoma. Immunogenetics 36, 238–247 (1992). https://doi.org/10.1007/BF00215054

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00215054

Keywords

Navigation