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Biochemical characterization and cellular distribution of a polymorphic, murine cell-surface glycoprotein expressed on lymphoid tissues

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Abstract

A murine leukocyte surface glycoprotein (Mr = 95 000) has been defined by means of xenogeneic monoclonal antibodies. In normal hematopoietic tissues, the glycoprotein is found in highest amounts in the bone marrow. Flow cytometric analysis shows that essentially all bone-marrow cells express the glycoprotein and that it is a major component of a subpopulation of cells containing predominantly granulocytic precursors. In contrast, only about 5 percent of thymocytes express sufficient glycoprotein to be detected by flow cytometric analysis, although under stringent conditions up to 20 percent of thymocytes are susceptible to complement-mediated cytotoxicity using a monoclonal antibody against the glycoprotein. Functional assays showed that both prothymocytes and colony forming unit-spleen express the glycoprotein which is broadly distributed on murine hematopoietic tumor cell lines. However, although some Thy-I+ (T) cell lymphomas express large amounts of the glycoprotein, others do not express detectable quantities of the molecule. The glycoprotein is not restricted to hematopoietic cells and can be detected on lung, kidney, brain, and liver as well as cultured fibroblasts. Monoclonal antibodies against the glycoprotein cross-react with an antigen present on human cells. As described in the accompanying paper, the glycoprotein exists in two antithetical allelic forms and we show that it is identical to a polymorphic surface molecule independently characterized by Colombatti and co-workers.

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References

  • Brown, W. R. A., Barclay, N., Sunderland, C. A., and Williams, A. F.: Identification of a glycophorin-like molecule at the cell surface of rat thymocytes. Nature 289: 456–460, 1981

    Google Scholar 

  • Boyle, W.: An extension of the 51Cr-release assay for the estimation of mouse cytotoxins. Transplantation 6: 761–764, 1968

    Google Scholar 

  • Collins, S. J., Ruscetti, F. W., Gallagher, R. E., and Gallo, R. C.: Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc. Natl. Acad. Sci. U.S.A. 75: 2458–2462, 1978

    Google Scholar 

  • Colombatti, A., Hughes, E. N., Taylor, B. A., and August, J. T.: The gene for a major cell surface glycoprotein of mouse macrophages and other phagocytic cells is located on chromosome 2. Proc. Natl. Acad. Sci. U.S.A., in press, 1981

  • Coulter, J.: Model BCS-176. Biological Cell Separator, Reserach Developments. 3150 B Villa, Los Alamos, New Mexico 87544, 1976

  • Dennert, G., Hyman, R., Lesley, J., and Trowbridge, I. S.: Effects of cytotoxic monoclonal antibody specific for T200 glycoprotein on functional lymphoid cell populations. Cell. Immunol. 53: 350–364, 1980

    Google Scholar 

  • Emerman, J. T., Enami, J., Pitelka, D. R., and Nandi, S.: Hormonal effects on intracellular and secreted casein in cultures of mouse mammary eipthelial cells on floating collagen membranes. Proc. Natl. Acad. Sci. U.S.A. 74: 4466–4470, 1977

    Google Scholar 

  • Greaves, M. and Janossy, G.: Patterns of gene expression and the cellular origins of human leukemias. Biochim. Biophys. Acta. 516: 193–230, 1978

    Google Scholar 

  • Hiebert, R.: Model 8130 Dual Log Amplifier, Los Alamos Scientific Laboratory, Dwg. No. 4Y-89749, 1975

  • Hoffman, R. A., Kung, P. C., Hansen, W. P., and Goldstein, G.: Simple and rapid measurement of human T lymphocytes and their subclasses in peripheral blood. Proc. Natl. Acad. Sci. U.S.A. 77: 4914–4917, 1980

    Google Scholar 

  • Horan, P. and Kappler, J.: Automated fluorescent analysis for cytotoxicity assays. J. Immunol. Methods 18: 309–316, 1977

    Google Scholar 

  • Horibata, K. and Harris, A.: Mouse myelomas and lymphomas in culture. Exp. Cell Res. 60: 61–77, 1970

    Google Scholar 

  • Hughes, E. N. and August, J. T.: Characterization of plasma membrane proteins identified by monoclonal antibodies. J. Biol. Chem. 256: 664–671, 1981

    Google Scholar 

  • Hyman, R. and Stallings, V.: Complementation patterns of Thy-1 variants and evidence that antigen-loss variants “pre-exist” in the parental population. J. Natl. Cancer Inst. 52: 429–436, 1974

    Google Scholar 

  • Hyman, R., Trowbridge, I., and Cunningham, K.: Cell surface molecules of Friend erythroleukemias: Decrease in T200 glycoprotein expression after induction. J. Cell. Physiol. 105: 469–482, 1980a

    Google Scholar 

  • Hyman, R., Cunningham, K., and Stallings, V.: Evidence for a genetic basis for the class A Thy-1− defect. Immunogenetics 10: 261–271, 1980b

    Google Scholar 

  • Hyman, R. and Trowbridge, I.: Two complementation classes of T200 (Ly-5) glycoprotein-negative mutants. Immunogenetics 12: 511–523, 1981

    Google Scholar 

  • Hyman, R., Cunningham, K., and Stallings, V.: Effect of gene dosage on cell-surface expression of Thy-1 antigen in somatic cell hybrids between Thy-1− Abelson-leukemia-virus induced lymphomas and Thy-1+ mouse lymphomas. Immunogenetics 12: 381–395, 1981

    Google Scholar 

  • Ichikawa, Y.: Differentiation of a cell line of myeloid leukemia: J. Cell. Physiol. 74: 223–234, 1970

    Google Scholar 

  • Kadish, J. L. and Basch, R. S.: Hematopoietic thymocyte precursors I. Assay and kenetics of the appearance of progeny. J. Exp. Med. 143: 1082–1099

  • Klein, G., Dombos, L., and Gothoskar, B.: Sensitivity of Epstein-Barr virus (EBV) producer and nonproducer human lymphoblastoid cell lines to superinfection with EB-virus. Int. J. Cancer 10: 44–57, 1972

    Google Scholar 

  • Klein, G., Sugden, B., Liebold, W., and Menezes, J.: Infection of EBV-genome-negative and -positive human lymphoblastoid cell lines with biologically different preparations of EBV. Intervirology 3: 232–244, 1974

    Google Scholar 

  • Köhler, G. and Milstein, C.: Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256: 495–497, 1975

    Google Scholar 

  • Kornfeld, K., Reitman, M. L., and Kornfeld, R.: The carbohydrate binding specificity of pea and lentil lectins: Fucose is an important determinant. J. Biol. Chem. 256: 6663–6640, 1981

    Google Scholar 

  • Lesley, J. and Trowbridge, I. S.: Genetic characterization of a polymorphic murine cell-surface glycoprotein. Immunogenetics 15: 313–320, 1982

    Google Scholar 

  • Metcalf, D.: Thymus and immune responses. Cold Spring Harbor Symp. Quant. Biol. 32: 583–590, 1967

    Google Scholar 

  • Minowada, J., Janossy, G., Greaves, M. F., Tsubota, T., Srivastava, B. I. S., Morikawa, S., and Tatsumi, E.: Expression of an antigen associated with acute lymphoblastic leukemia in human leukemia-lymphoma cell lines. J. Natl. Cancer Inst. 60: 1269–1276, 1978

    Google Scholar 

  • Morris, R. J. and Williams, A. F.: Antigens on mouse and rat lymphocytes recognized by rabbit antiserum against rat brain: the quantitative analysis of a xenogeneic antiserum. Eur. J. Immunol. 5: 274–281, 1975

    Google Scholar 

  • Omary, M. B. and Trowbridge, I. S.: Disposition of T200 glycoprotein in the plasma membrane of a murine lymphoma cell line. J. Biol. Chem. 255: 1662–1669, 1980

    Google Scholar 

  • Omary, M. B. and Trowbridge, I. S.: Covalent binding of fatty acid to the transferrin receptor in cultured human cells. J. Biol. Chem. 256: 4715–4718, 1981

    Google Scholar 

  • Ritz, J., Pesando, J. M., Notis-McConarty, J., Lazarus, H., and Schlossman, S. F.: A monoclonal antibody to human acute lymphoblastic leukemia antigen. Nature 283: 583–585, 1980

    Google Scholar 

  • Scheid, M. P. and Triglia, D.: Further description of the Ly-5 system. Immunogenetics 9: 423–433, 1979

    Google Scholar 

  • Steinkamp, J. A., Fulwyler, M. J., Coulter, J. R., Hiebert, R. D., Horney, J. L., and Mullaney, P. F.: A new multiparameter separator for microscopic particles and biological cells. Rev. Sci. Instrum. 44: 1301–1310, 1973

    Google Scholar 

  • Sugiyama, K., Tomida, M., and Hozumi, M.: Differentiation-associated changes in membrane proteins of mouse myeloid leukemia cells. Biochim. Biophys. Acta 587: 169–179, 1979

    Google Scholar 

  • Till, J. and McCulloch, E.: A direct measurement of the radiation sensitivity of normal bone marrow cells. Radiat. Res. 14: 213–222, 1961

    Google Scholar 

  • Todaro, G. J. and Green H.: Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell. Biol. 17: 299–313, 1963

    Google Scholar 

  • Trowbridge, I. S.: Isolation and chemical characterization of a mitogenic lectin from Pisum sativum. J. Biol. Chem. 249: 6004–6012, 1974

    Google Scholar 

  • Trowbridge, I. S., Nilsen-Hamilton, M., Hamilton, R. T., and Bevan, M. J.: Preliminary characterization of two thymus-dependent xenoantigens from mouse lymphocytes. Biochem. J. 163: 211–217, 1977

    Google Scholar 

  • Trowbridge, I. S.: Interspecies spleen-myeloma hybrid-producing monoclonal antibodies against mouse lymphocyte surface glycoprotein, T200. J. Exp. Med. 148: 313–323, 1978

    Google Scholar 

  • Trowbridge, I. S., Hyman, R., and Mazauskas, C.: The synthesis and properties of T25 glycoprotein in Thy-I-negative mutant lymphoma cells. Cell 14: 21–32, 1978

    Google Scholar 

  • Trowbridge, I. S. and Omary, M. B.: Human cell surface glycoprotein related to cell proliferation is the receptor for transferrin. Proc. Natl. Acad. Sci. U.S.A. 78: 3039–3043, 1981

    Google Scholar 

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Authors and Affiliations

  1. Department of Cancer Biology, The Salk Institute, Post Office Box 85800, 92138, San Diego, California

    Ian S. Trowbridge, Jayne Lesley, Roberta Schulte, Robert Hyman & Joseph Trotter

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  1. Ian S. Trowbridge
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  2. Jayne Lesley
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  3. Roberta Schulte
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  4. Robert Hyman
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  5. Joseph Trotter
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Trowbridge, I.S., Lesley, J., Schulte, R. et al. Biochemical characterization and cellular distribution of a polymorphic, murine cell-surface glycoprotein expressed on lymphoid tissues. Immunogenetics 15, 299–312 (1982). https://doi.org/10.1007/BF00364338

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  • DOI: https://doi.org/10.1007/BF00364338

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