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Properties of reticulum cell sarcomas in SJL/J mice

VIII. Prominent role of RCS cell I-A antigens in the stimulation of syngeneic T cells

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Abstract

While T cells from SJL and from F1 hybrids of SJL that do not express I-E antigens give strong proliferative responses to RCS, T cells from F1 hybrids expressing surface I-E do not. The nature of the stimulating antigen on the RCS cell surface was examined using monoclonal antibodies. Complete inhibition of the T-cell proliferative response was obtained with antibodies to I-A antigens, whereas antibodies to I-E antigens did not inhibit at all. This inhibition was mediated via an effect of the antibodies on the stimulating cells. Biochemical characterization of immunoprecipitated 125I- and 's S-labeled RCS antigens was performed using two-dimensional gel electrophoresis. Using this technique, I-A antigens were readily detected. However, neither Ia.7-specific antibodies nor antibodies specific for Eα : E β complexes precipitated any E alpha or E beta chains. Comparison of I-A antigens from RCS and normal SJL spleen cells revealed minor mobility differences in the gels, possibly due to differences in glycosylation, the significance of which needs to be further evaluated. Examination of RNA extracted from RCS, using E alpha and A alpha cDNA probes showed that RCS cells do not transcribe the E alpha gene as has been shown previously for normal H-2 s cells. Furthermore, DNA from RCS cells showed a defect in the E alpha gene similar to that known to exist in normal H-2 s cells. Our findings exclude the presence of E alpha on RCS cells and suggest a major role for I-A, either alone or in conjunction with another as yet unidentified cell surface antigen, in the stimulation of T cells.

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Abbreviations

RCS:

reticulum cell sarcoma

MLR:

mixed lymphocyte response

IEF:

isoelectric focusing

NEPHGE:

nonequilibrium pH gel electrophoresis

SDS:

sodium dodecyl sulfate

PAGE:

polyacrylamide gel electrophoresis

DNA:

deoxyribonucleic acid

RNA:

ribonucleic acid

References

  • Benoist, C. O., Mathis, D. J., Kanter, M. R., Williams, V. E., and McDevitt, H. O.: The murine la a chains, Eα and Aα, show a surprising degree of sequence homology. Proc. Natl. Acad. Sci. U.S.A. 80: 534–538, 1983

    Google Scholar 

  • Carswell, E. A., Wanebo, H. J., Old, L. J., and Boyse, E. A.: Immunogenic properties of reticulum cell sarcomas of SJL/J mice. J. Natl. Cancer Inst. 44: 1281–1288, 1970

    Google Scholar 

  • Cone, R. E. and Brown, W. B.: Isolation of membrane-associated immunoglobulins from T lymphocytes by non-ionic detergents. Immunochemistry 13: 571–579, 1976

    Google Scholar 

  • Dunn, T. B. and Deringer, M. K.: Reticulum cell neoplasm, type B or the “Hodgkin's-like lesion” of the mouse. J. Natl. Cancer Inst. 40: 771–821, 1968

    Google Scholar 

  • Hayama, T., Nagler, C., Umetsu, D. T., Chapman-Alexander, J., and Thorbecke, G. J.: Ia restricted interaction of normal lymphoid cells and SJL lymphoma (RCS) leading to lymphokine production. I. Enhancement and suppression of antibody formation in co-cultures of RCS and lymphoid cells. Cell. Immunol. 79: 134–149, 1983a

    Google Scholar 

  • Hayama, T., Ponzio, N. M., Nagler, C., Vilcek, J., and Thorbecke, G. J.: la restricted interaction of normal lymphoid cells and SJL lymphoma (RCS) leading to lymphokine production. III. Relative roles of RCS and normal lymphoid cells in lymphokine production. J. Natl. Cancer Inst., in press, 1983b

  • Jones, P. P.: Analysis of H-2 and Ia molecules by two-dimensional gel electrophoresis. J. Exp. Med. 146: 1261–1279, 1977

    Google Scholar 

  • Jones, P. P., Murphy, D. B., Hewgill, D., and McDevitt, H. O.: Detection of a common polypeptide chain in I-A and I-E subregion immunoprecipitates. Immunochemistry 16: 51–60, 1978a

    Google Scholar 

  • Jones, P. P., Murphy, D. B., and McDevitt, H. O.: Two-gene control of the expression of a murine Ia antigen. J. Exp. Med. 148: 925–939, 1978b

    Google Scholar 

  • Jones, P. P., Murphy, D. B., and McDevitt, H. O.: Variable synthesis and expression of Eα and Ae (E β ) Ia polypeptide chains in mice of different H-2 haplotypes. Immunogenetics 12: 321–337, 1981

    Google Scholar 

  • Kappler, J. W., Skidmore, B., White, J., and Marrack, P.: Antigen-inducible, H-2-restricted, interleukin2-producing T cell hybridomas. J. Exp. Med. 153:1198–1214, 1981

    Google Scholar 

  • Katz, I. R.: Influence of Host-Tumor Cell Interactions on the Growth of Reticulum Cell Sarcomas in SJL/J and F 1 Hybrids, doctoral dissertation, New York University Medical Center, 1982a

  • Katz, I. R., Chapman-Alexander, J., Lerman, S. P., David, C. S., and Thorbecke, G. J.: Growth of SJL/J-derived RCS as related to its ability to induce T cell proliferation in the host. II. Negative influence of H-2d. Transplantation 33: 134–137, 1982b

    Google Scholar 

  • Katz, I. R., Lerman, S. P., Ponzio, N. M., Schreffler, D. C., and Thorbecke, G. J.: Growth of SJL/J-derived transplantable reticulum cell sarcoma as related to its ability to induce T-cell proliferation in the host. I. Dominant negative genetic influences of other parent haplotype in F1 hybrids of SJL/mice. J. Exp. Med. 151: 347–361, 1980

    Google Scholar 

  • Kim, K. J., Kanellopoulos-Langevin, C., Merwin, R., Sachs, D. H., and Asofsky, R.: Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 122: 549–554, 1979

    Google Scholar 

  • Lemke, H., Hämmerling, G. J., and Hämmerling, U.: Fine specificity analysis with monoclonal antibodies of antigens controlled by the major histocompatibility complex and by the Qa/TL region in mice. Immunol. Rev. 47: 175–206, 1979

    Google Scholar 

  • Lerman, S. P., Chapman, J. M. Carswell, E. A., and Thorbecke, G. J.: Properties of reticulum cell sarcomas in SJL/J mice. I. Proliferative responses to tumor cells of T-derived lymphoid cells from normal mice. Int. J. Cancer 14: 808–816, 1974

    Google Scholar 

  • Lerman, S. P., Carswell, E. A., Chapman, J., and Thorbecke, G. J.: Properties of reticulum cell sarcomas in SJL/J mice. III. Promotion of tumor growth in irradiated mice by normal lymphoid cells. Cell. Immunol. 23: 53–67, 1976

    Google Scholar 

  • Lerner, E. A., Matis, L. A., Janeway, C. A., Jones, P. P., Schwartz, R. H., and Murphy, D. B.: Monoclonal antibody against an Ir gene product? J. Exp. Med. 152: 1085–1101, 1980

    Google Scholar 

  • Mathis, D. J., Benoist, C. O., Williams, V. E., Kanter, M. R., and McDevitt, H. O.: The murine Eα immune response gene. Cell 32: 745–754, 1983a

    Google Scholar 

  • Mathis, D. J., Benoist, C. O., Williams, V. E., Kanter, M., and McDevitt, H. O.: Several mechanisms can account for defective Eα gene expression in different mouse haplotypes. Proc. Natl. Acad. Sci. U.S.A. 80: 273–277, 1983b

    Google Scholar 

  • O'Farrell, P. H.: High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250: 4007–4021, 1975

    Google Scholar 

  • O'Farrell, P. Z., Goodman, H. M., and O'Farrell, P. H.: High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12: 1133–1142, 1977

    Google Scholar 

  • Ozato, K., Mayer, N., and Sachs, D. H.: Hybridoma cell lines secreting monoclonal antibodies to mouse H-2 and Ia antigens. J. Immunol. 124: 533–540, 1980

    Google Scholar 

  • Ponzio, N. M.: Lymphocyte responses to syngeneic antigens. I. Enhancement of murine autologous mixed lymphocyte response by polyethylene glycol. Cell. Immunol. 49: 266–282, 1979

    Google Scholar 

  • Ponzio, N. M., David, C. S., Schreffler, D. C., and Thorbecke, G. J.: Properties of reticulum cell sarcoma in SJL/mice. V. Nature of reticulum cell sarcoma surface antigens which induce proliferation of normal SJL/J T cells. J. Exp. Med. 146: 132–145, 1977a

    Google Scholar 

  • Ponzio, N. M., Lerman, S. P., Chapman, J. M., and Thorbecke, G. J.: Properties of reticulum cell sarcomas in SJL/J mice. IV. Minimal development of cytotoxic cells despite marked proliferation to syngeneic RCS in vivo and in vitro. Cell Immunol. 32: 10–22, 1977b

    Google Scholar 

  • Ponzio, N. M., Hayama, T., Nagler, C., Katz, I. R., Hoffman, M. K., Gilbert, C., V ilcek, J., and Thorbecke, G. J.: Ia restricted interaction of normal lymphoid cells and SJL lymphoma (RCS) leading to lymphokine production. II. Rapid production of antibody enhancing factor, interleukin-2 and immune interferon. in press, 1983

  • Rosenstreich, D. L. and Mizel, S. B.: The participation of macrophages and macrophage cell lines in the activation of T lymphocytes by mitogens. Immunol. Rev. 40: 102–135, 1978

    Google Scholar 

  • Scheid, M. P., Chapman-Alexander, J. M., Hayama, T., Katz, I. R., Lerman, S. P., Nagler, C., Ponzio, N. M., and Thorbecke, G. J.: Identification of transplantable reticulum cell sarcomas in SJL/J mice as belonging to the B cell lineage. In Klinman, Mosier, Scher, and Vitetta (eds): B Lymphocytes in the Immune Response, pp. 475–482, Elsevier North Holland, 1981

  • Sung, E. and Jones, P. P.: The invariant chain of murine Ia antigens: its glycosylation, abundance, and subcellular localization. Mol. Immunol. 18: 899–913, 1981

    Google Scholar 

  • Wilbur, S. M. and Bonavida, B.: Expression of hybrid la molecules on the cell surface of reticulum cell sarcoma that are undetectable on host SJL/J lymphocytes. J. Exp. Med. 153: 501–513, 1981

    Google Scholar 

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Brown, P.H., Mathis, D., Cone, R.E. et al. Properties of reticulum cell sarcomas in SJL/J mice. Immunogenetics 18, 399–413 (1983). https://doi.org/10.1007/BF00372472

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