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Are the Classic Transplantation Antigens Primitive Cell-Surface Antibodies?

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Current Trends in Histocompatibility

Abstract

The existence of a well-developed immune system is restricted to the vertebrates. Foreign substances are recognized by antibodies that exhibit an almost endless variety of antigen-combining sites. Although some of the antibody variability may be due to somatic mutations, the vertebrate genome contains substantial numbers of genes coding for immunoglobulin variable regions (see Scidman et al., 1978). It appears possible that these sets of genes evolved under environmental selection by a gradual expansion of duplicated and mutated genes. At some time during the course of this development, the gene products may have occurred as a family of proteins displaying a restricted genetic polymorphism. These ancestral proteins may have participated in recognitive processes such as the discrimination between self and nonself wherein genetic polymorphism should have provided a selective advantage. Assuming that the evolution of the variable regions included organisms lacking a circulatory system, it can be envisaged that the predecessors of the immunoglobulins were cell-surface proteins.

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References

  • Binz, H., and Wigzell H., 1977, Idiotypic, alloantigen-reactive T lymphocyte receptors and their use to induce specific transplantation tolerance, Prog. Allergy 23:154–198.

    PubMed  CAS  Google Scholar 

  • Bodmer, W.F., 1972, Evolutionary significance of the HLA system, Nature (London) 237:139–145.

    Article  CAS  Google Scholar 

  • Bubbers, J.E., Chen, S., and Lilly, F., 1978, Nonrandom inclusion of the H-2K and H-2D antigens in Friend virus particles from mice of various strains, J. Exp. Med. 147:340–351.

    Article  PubMed  CAS  Google Scholar 

  • Callahan, G.N., Allison, J.P., Pellegrino, M.A., and Reisfeld, R.A., 1979, Physical association of histocompatibility antigens and tumor-associated antigens on the surface of murine lymphoma cells, J. Immunol. 122:80–81.

    Google Scholar 

  • Coligan, J.E., Kindt, T.J., Ewenstein, B.M., Uehara, H., Nisizawa, T., and Nathenson, S.G., 1978, Primary structure of murine major histocompatibility complex alloantigens: Amino acid sequence studies of the cyanogen bromide fragments of the H-2 K b glycoprotein, Proc. Natl. Acad. Sci. U.S.A. 75:3390–3394.

    Article  PubMed  CAS  Google Scholar 

  • Cunningham, B.A., Wang, J.L., Berggard, I., and Peterson, P.A., 1973, The complete amino acid sequence of β2-microglobulin, Biochemistry 12:4811–4822.

    Article  PubMed  CAS  Google Scholar 

  • Dayhoff, M.O., Hunt, L.T., Barker, W.C., and Orcutt, B.C., 1976, Atlas of Protein Sequence and Structure, Vol. 5 (M.O. Dayhoff, ed.), Suppl. 1 and 2, National Biomedical Research Foundation, Washington, D.C.

    Google Scholar 

  • Doherty, P.A., Blanden, R.V., and Zinkernagel, R.M., 1976, Specificity of virus-immune effector T-cells for H-2K or H-2D compatible interactions: Implications for H-antigen diversity, Transplant. Rev. 29:89–124.

    PubMed  CAS  Google Scholar 

  • Edelman, G.M., 1970, The covalent structure of a human IgG-immunoglobulin. XI. Functional implications, Biochemistry 9:3197–3205.

    Article  PubMed  CAS  Google Scholar 

  • Edelman, G.M., and Gall, W.E., 1969, The antibody problem, Annu. Rev. Biochem. 38:415–466.

    Article  PubMed  CAS  Google Scholar 

  • Gaily, J.A., and Edelman, G.M., 1972, The genetic control of immunoglobulin synthesis, Annu. Rev. Genet. 6:1–46.

    Article  Google Scholar 

  • Germain, R.N., Dorf, M.E., and Benacerraf, B., 1975, Inhibition of T-lymphocyte mediated tumor-specific lysis by alloantisera directed against the H-2 serological specificities of the tumor, J. Exp. Med. 142:1023–1028.

    Article  PubMed  CAS  Google Scholar 

  • Grey, H.M., Kubo, R.T., Colon, S.M., Poulik, M.D., Cresswell, P., Springer, T., Turner, M., and Strominger, J.L., 1973, The small subunit of HL-A antigens is β2-microglobulin, J. Exp. Med. 138:1608–1612.

    Article  PubMed  CAS  Google Scholar 

  • Gross, E., and Witkopf, B., 1962, Nonenzymatic cleavage of peptide bonds: The methionine residues in bovine pancreatic ribonuclease, J. Biol. Chem. 237:1856–1860.

    PubMed  CAS  Google Scholar 

  • Hale, A.H., Whitte, O.W., Baltimore, D., and Eisen, H.N., 1978, Vesicular stomatitis virus glycoprotein is necessary for H-2-restricted lysis of infected cells by cytotoxic T-lymphocytes, Proc. Natl. Acad. Sci. U.S.A. 75:970–974.

    Article  PubMed  CAS  Google Scholar 

  • Hecht, T.T., and Summers, D.F., 1976, Interactions of vesicular stomatitis virus with murine cell surface antigens, J. Virol. 19:833–845.

    PubMed  CAS  Google Scholar 

  • Helenius, A., Morein, B., Fries, E., Simons, K., Robinson, P., Schirrmacher, V., Terhorst, C., and Strominger, J.L., 1978, Human (HLA-A and HLA-B) and murine (H-2K and H-2D) histocompatibility antigens are cell surface receptors for Semliki Forest virus, Proc. Natl. Acad. Sci. U.S.A. 75:3846–3850.

    Article  PubMed  CAS  Google Scholar 

  • Henning, R., Schrader, J.E., and Edelman, G.M., 1976, Antiviral antibodies inhibit the lysis of tumor cells by anti-H-2 sera, Nature (London) 263:689–691.

    Article  CAS  Google Scholar 

  • Hildemann, W.H., Raison, R.L., Cheong, G., Hull, C.J., Akaka, L., and Okamoto, J., 1977, Immunological specificity and memory in a scleractinian coral, Nature (London) 270:219–223.

    Article  CAS  Google Scholar 

  • Hill, R.L., 1965, Hydrolysis of proteins, Adv. Protein Chem. 20:37–107.

    Article  PubMed  CAS  Google Scholar 

  • Hill, R.L., Delaney, R., Fellows, R.E., Jr., and Lebovitz, M.E., 1966, The evolutionary origins of the immunoglobulins, Proc. Natl. Acad. Sci. U.S.A. 56:1762–1769.

    Article  PubMed  CAS  Google Scholar 

  • Inman, J.K., 1974, Multispecificity of the antibody combining region and antibody diversity, in: The Immune System (E.E. Sercarz, A.R. Williamson, and C.F. Fox, eds.), pp. 37–52, Academic Press, New York.

    Google Scholar 

  • Jacobson, G.R., Schaffer, M.H., Stark, G.R., and Vanaman, T.C., 1973, Specific chemical cleavage in high yield at the amino peptide bonds of cysteine and cystine residues, J. Biol. Chem. 248:6583–6591.

    PubMed  CAS  Google Scholar 

  • Klareskog, L., Banck, G., Forsgren, A., and Peterson, P.A., 1978, Binding of HLA antigen-containing liposomes to bacteria, Proc. Natl. Acad. Sci. U.S.A. 75:6197–6201.

    Article  PubMed  CAS  Google Scholar 

  • Koszinowski, U., and Ertl, H., 1975a, Lysis mediated by T cells and restricted by H-2 antigen of target cells infected with vaccinia virus, Nature (London) 255:552–554.

    Article  CAS  Google Scholar 

  • Koszinowski, U., and Ertl, H., 1975b, Target cell-dependent T cell-mediated lysis of vaccinia virus-infected cells, Eur. J. Immunol. 5:245–251.

    Article  PubMed  CAS  Google Scholar 

  • Kvist, S., Östberg, L., and Peterson, P.A., 1978a, Reactions and crossreactions of a rabbit anti-H2 antigen serum, Scand. J. Immunol. 7:265–276.

    Article  PubMed  CAS  Google Scholar 

  • Kvist, S., Östberg, L., Person, H., Philipson, L., and Peterson, P.A., 1978b, Molecular association between transplantation antigens and a cell surface antigen in an adenovirus-transformed cell line, Proc. Natl. Acad. Sci. U.S.A. 75:5674–5678.

    Article  PubMed  CAS  Google Scholar 

  • López de Castro, J.A., Orr, H.T., Robb, R.J., Kostyk, T.G., Mann, D.L., and Strominger, J.L., 1979, Complete amino acid sequence of papain-solubilized human histocompatibility antigen, HLA-B7. 1. Isolation and amino acid composition of fragments and of tryptic and chymotryptic peptides, Biochemistry 18:5704–5711.

    Article  Google Scholar 

  • Nakamuro, K., Tanigaki, N., and Pressman, D., 1973, Multiple common properties of human ß2-microglobulin and the common portion fragment derived from HL-A antigen molecules, Proc. Natl. Acad. Sci. U.S.A. 70:2863–2865.

    Article  PubMed  CAS  Google Scholar 

  • Neauport-Sautes, C., Lilly, F., Silvestre, D., and Kourilsky, F.M., 1973, Independence of H-2K and H-2D antigenic determinants on the surface of mouse lymphocytes, J. Exp. Med. 137:511–526.

    Article  PubMed  CAS  Google Scholar 

  • Orr, H.T., Lancet, D., Robb, R.J., López de Castro, J.A., and Strominger, J.L., 1979, The heavy chain of human histocompatibility antigen, HLA-B7, contains an immunoglobinlike region, Nature 282:266–270.

    Article  PubMed  CAS  Google Scholar 

  • Orr, H.T., López de Castro, J.A., Parham, P., Pleogh, H.L., and Strominger, J.L., 1979a Comparison of amino acid sequences of two human histocompatibility antigens, HLA-A2 and HLA-B7: Location of putative alloantigenic sites, Proc. Natl. Acad. Sci. U.S.A. 76:4395–4399.

    Article  CAS  Google Scholar 

  • Orr, H.T., López de Castro, J. A., Lancet, D., and Strominger, J.L., 1979b, Complete amino acid sequence of a papain-solubilized histocompatibility antigen, HLA-B7. 2. Sequence determination and search for homologies, Biochemistry 18:5711–5720.

    Article  CAS  Google Scholar 

  • Parham, P., Alpert, B.W., Orr, H.T., and Strominger, J.L., 1977, Carbohydrate moiety of HLA-antigens, J. Biol. Chem. 252:7555–7567.

    PubMed  CAS  Google Scholar 

  • Peterson, P.A., Cunningham, B.A., Berggard, I., and Edelman, G.M., 1972, β 2-Microglobulin—a free immunoglobulin domain, Proc. Natl. Acad. Sci. U.S.A. 69:1697–1701.

    Article  PubMed  CAS  Google Scholar 

  • Peterson, P.A., Rask, L., and Lindblom, J.B., 1974, Highly purified papain-solubilized HLA-antigens contain β 2-microglobulin, Proc. Natl. Acad. Sci. U.S.A. 71:35–39.

    Article  PubMed  CAS  Google Scholar 

  • Peterson, P.A., Rask, L., Sege, K., Klareskog, L., Anundi, H., and Ostberg, L., 1975, Evolutionary relationship between immunoglobulins and transplantation antigens, Proc. Natl. Acad. Sci. U.S.A. 72:1612–1616.

    Article  PubMed  CAS  Google Scholar 

  • Peterson, P.A., Östberg, L., and Rask, L., 1977, β 2-Microglobulin and the major histocompatibility complex, Adv. Cancer Res. 24:115–163.

    Article  PubMed  CAS  Google Scholar 

  • Poljak, R.J., 1975, Three-dimensional structure, function and genetic control of immunoglobulins, Nature (London) 256:373–376.

    Article  CAS  Google Scholar 

  • Poulsen, K., Fraser, K.J., and Haber, E., 1972, An active derivative of rabbit antibody light chain composed of the constant and the variable domains held together only by a native disulfide bond, Proc. Natl. Acad. Sci. U.S.A. 69:2495–2499.

    Article  PubMed  CAS  Google Scholar 

  • Rask, L., Lindblom, J.B., and Peterson, P.A., 1976, Structural and immunological similarities between HLA antigens for three loci, Eur. J. Immunol. 6:93–100.

    Article  PubMed  CAS  Google Scholar 

  • Richards, F.F., Anzel, L.M., Konigsberg, W.H., Manjula, B.N., Poljak, R.J., Rosenstein, R.W., Saul, F., and Varga, J.M., 1974, Polyfunctional antibody combining regions, in: The Immune System (E.E. Sercarz, A.R. Williamson, and C.F. Fox, eds.), pp. 53–68, Academic Press, New York.

    Google Scholar 

  • Richards, F.F., Konigsberg, W.H., Rosenstein, R.W., and Varga, J.M., 1975, On the specificity of antibodies, Science 187:130–137.

    Article  PubMed  CAS  Google Scholar 

  • Rosenthal, A., 1978, Determinant selection and macrophage function in genetic control of the immune response, Immunol. Rev. 40:136–152.

    Article  PubMed  CAS  Google Scholar 

  • Schrader, J.W., and Edelman, G.M., 1976, Participation of the H-2 antigens of tumor cells in their lysis by syngeneic T cells, J. Exp. Med. 143:601–604.

    Article  PubMed  CAS  Google Scholar 

  • Schrader, J.W., Cunningham, B.A., and Edelman, G.M., 1975, Functional interactions of viral and histocompatibility antigens at tumor cell surfaces, Proc. Natl. Acad. Sci. U.S.A. 72:5066–5070.

    Article  PubMed  CAS  Google Scholar 

  • Scidman, J.G., Leder, A., Nav, M., Norman, B., and Leder, P., 1978, Antibody diversity, Science 202:11–17.

    Article  Google Scholar 

  • Shearer, G.M., Rehn, T.G., and Garbarino, C.A., 1975, Cell-mediated lympholysis of trinitrophenyl-modified antologous lymphocytes, J. Exp. Med. 141:1348–1364.

    Article  PubMed  CAS  Google Scholar 

  • Shreffler, D., and David, C.S., 1975, The H-2 major histocompatibility complex and the I immune response region: Genetic variation, function and organization, Adv. Immunol. 20:125–196.

    Article  PubMed  CAS  Google Scholar 

  • Singer, S.J., and Doolittle, R.F., 1966, Antibody active sites and immunoglobulin molecules, Science 153:13–25.

    Article  PubMed  CAS  Google Scholar 

  • Smithies, O., and Poulik, M.D., 1972, Initiation of protein synthesis at an unusual position in an immunoglobulin gene?, Science 175:187–189.

    Article  PubMed  CAS  Google Scholar 

  • Snary, D., Barnstable, C.J., Bodmer, W.F., and Crumpton, M.J., 1977, Molecular structure of human histocompatibility antigens: The HLA-C-series, Eur. J. Immunol. 8:580–585.

    Article  Google Scholar 

  • Springer, T.A., and Strominger, J.L., 1976, Detergent-soluble HLA-antigens contain a hydrophilic region at the COOH-terminus and a penultimate hydrophobic region, Proc. Natl. Acad. Sci. U.S.A. 73:2481–2485.

    Article  PubMed  CAS  Google Scholar 

  • Talmage, D.E., 1959, Immunological specificity, Science 129:1643–1648.

    Article  PubMed  CAS  Google Scholar 

  • Terhorst, C., Robb, R., Jones, C., and Strominger, J.L., 1977, Further structural studies of the heavy chain of HLA-antigens and its similarity to immunoglobulins, Proc. Natl. Acad. Sci. U.S.A. 74:4002–4006.

    Article  PubMed  CAS  Google Scholar 

  • Trägårdh, L., Klareskog, L., Curman, B., Rask, L., and Peterson, P.A., 1978, Isolation and properties of detergent-solubilized HLA antigens obtained from platelets, Scand. J. Immunol. 8:563–568.

    Article  PubMed  Google Scholar 

  • Trägårdh, L., Wiman, K., Rask, L., and Peterson, P.A., 1979a, Fragmentation of human transplantation antigen heavy chains by limited proteolysis, acid cleavage and cyanogen bromide treatment, Biochemistry 18:1322–1328.

    Article  PubMed  Google Scholar 

  • Trägårdh, L., Curman, B., Wiman, K., Rask, L., and Peterson, P.A., 1979b, Chemical, physical-chemical, and immunological properties of papain-solubilized human transplantation antigens, Biochemistry 18:2218–2226.

    Article  PubMed  Google Scholar 

  • Trägårdh, L., Rask, L., Wiman, K., Fohlman, J., and Peterson, P.A., 1979c, Amino acid sequence of an immunoglobulin-like HLA antigen heavy chain domain, Proc. Natl. Acad. Sci. U.S.A. 76:5839–5842.

    Article  PubMed  Google Scholar 

  • Trägårdh, L., Rask, L., Wiman, K., and Peterson, P.A., 1979d, Primary structure of pooled, papain-solubilized HLA-A, -B, and -C antigens, Scand. J. Immunol. 10:597–600.

    Article  PubMed  Google Scholar 

  • Trägårdh, L., Rask, L., Wiman, K., Fohlman, J., and Peterson, P.A., 1980, Complete amino acid sequence of pooled papain-solubilized HLA-A, -B, and -C antigens: Relatedness to immunoglobulins and internal homologies, Proc. Natl. Acad. Sci. U.S.A. 77:1129–1133.

    Article  PubMed  Google Scholar 

  • Walter, G., Maizel, J.V., Jr., 1974, The polypeptides of adenovirus, Virology 57:402–408.

    Article  PubMed  CAS  Google Scholar 

  • Wikler, M., Titani, K., Shinoda, T., and Putnam, F.W., 1967, The complete amino acid sequence of a λtype Bence-Jones protein, J. Biol. Chem. 242:1668–1670.

    PubMed  CAS  Google Scholar 

  • Wiman, K., Trägådh, L., Rask, L., and Peterson, P.A., 1979, Similarities between immunoglobulins and transplantation antigens in amino acid sequence and disulfide bond distribution, Eur. J. Biochem. 95:265–273.

    Article  PubMed  CAS  Google Scholar 

  • Zarling, D.A., Keshet, I., Watson, A., and Bach, F.H., 1978, Association of mouse major histocompatibility and Rauscher murine leukemia virus envelope glycoprotein antigens on leukemia cells and their recognition by syngenic virus-immune cytotoxic T-lymphocytes, Scand. J. Immunol. 8:497–508.

    Article  PubMed  CAS  Google Scholar 

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Peterson, P.A., Kämpe, O. (1981). Are the Classic Transplantation Antigens Primitive Cell-Surface Antibodies?. In: Reisfeld, R.A., Ferrone, S. (eds) Current Trends in Histocompatibility. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-3758-4_18

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  • DOI: https://doi.org/10.1007/978-1-4684-3758-4_18

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