Advertisement

The Molecular Basis for Cytolytic T Lymphocyte Function: Analysis with Blocking Monoclonal Antibodies

  • Eric Martz
  • Denise Davignon
  • Konrad Kürzinger
  • Timothy A. Springer
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 146)

Abstract

Cytolytic T lymphocytes (CTL) were identified during the late 1960’s (1,2) and are thought to be important effector cells in immunity to viruses (3) and in allograft rejection (4), Despite considerable effort during the past decade, little has been learned about the biochemical basis for the killing event. Not only do the presumed molecular mediators remain unidentified, but fundamental physiological questions remain unanswered.

Keywords

Target Cell Mixed Lymphocyte Culture Lymphocyte Membrane Mediate Killing Osmotic Protection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Brunner, K.T., J. Mauel, J.-C. Cerottini, H. Rudolf, and B. Chapuis. In vitro studies of cellular and humoral immunity induced by tumor allografts. In “Mechanisms of Inflammation Induced by Immune Reactions,” P.A. Miescher and P. Grabar, eds., pp. 342–357 (1967).Google Scholar
  2. 2.
    Berke G., G. Yagil, H. Ginsburg, and M. Feldman. Kinetic analysis of a graft reaction induced in cell culture. Immunol. 17:723–740 (1969).Google Scholar
  3. 3.
    Doherty, P.C., and R.M. Zinkernagel. T-cell-mediated immuno-pathology in viral infections. Transplant. Rev. 19:89–120 (1974).PubMedGoogle Scholar
  4. 4.
    Cerottini, J.-C., and K.T. Brunner. Cell-mediated cytotoxicity, allograft rejection, and tumor immunity. Adv. Irmnunol, 18:67–132 (1974).CrossRefGoogle Scholar
  5. 5.
    Martz, E. Early steps in specific tumor cell lysis by sensitized mouse T lymphocytes. II. Electrolyte permeability increase in the target cell membrane concomitant with programming for lysis. J. Immunol. 117:1023–1027 (1976).PubMedGoogle Scholar
  6. 6.
    Sanderson, C.J. The mechanism of lymphocyte-mediated cytotoxicity. Biol Rev. 56:153–197 (1981).PubMedCrossRefGoogle Scholar
  7. 7.
    Boyle, M.D.P., S.H. Ohaninan, and T. Borsos. Studies on the terminal stages of antibody-complement-mediated killing of a tumor cell. II. Inhibition of transformation of T to dead cells by 3’5’CAMP. J. Immunol. 116:1276–1279 (1976).PubMedGoogle Scholar
  8. 8.
    Burakoff, S.J., E. Martz, and B. Benacerraf. Is the primary complement lesion insufficient for lysis? Failure of cells damaged under osmotic protection to lyse in EDTA or at low temperature after removal of osmotic protection. Clin. Immunol, and Immunopathol. 4:108–126 (1975).CrossRefGoogle Scholar
  9. 9.
    Martz, E. Mechanism of specific tumor cell lysis by allo-immune T-lymphocytes: Resolution and characterization of discrete steps in the cellular interaction. Contemp. Top. Immunobiol. 7:301–361 (1977).PubMedCrossRefGoogle Scholar
  10. 10.
    Hiserodt, J.C., G.J. Tiangco, and G.A. Granger. The LT system in experimental animals. IV. Rapid specific lysis of Cr-labeled allogeneic target cells by highly unstable high MW lymphotoxin-receptor complex (es) released in vitro by activated alloimmune murine T lymphocytes. J. Immunol. 123:332–341 (1979).PubMedGoogle Scholar
  11. 11.
    Martz, E., and B. Benacerraf. Multiple target cell killing by the cytolytic T-lymphocyte and the mechanism of cytotoxicity. Transplantation 21:5–11 (1976).PubMedCrossRefGoogle Scholar
  12. 12.
    Zagury, D., J. Bernard, N. Thierness, M. Feldman, and G. Berke. Isolation and characterization of individual functionally reactive cytotoxic T lymphocytes: conjugation, killing and recycling at the single cell level. Eur. J. Immunol. 5:818–822 (1975).CrossRefGoogle Scholar
  13. 13.
    Golstein, P. Sensitivity of cytotoxic T cells to T-cell mediated cytotoxicity. Nature 252:81–83 (1974).PubMedCrossRefGoogle Scholar
  14. 14.
    Küppers, R.C., and C.S. Henney. Evidence for direct linkage between antigen recogntion and lytic expression in effector T cells. J. Exp. Med. 143:684–689 (1976).PubMedCrossRefGoogle Scholar
  15. 15.
    Bubbers, J.E., and C.S. Henney. Studies on the synthetic capacity and antigenic expression of glutaraldehyde-fixed target cells. J. Immunol. 114:1126–1131 (1975).PubMedGoogle Scholar
  16. 16.
    Thorn R.M., and C.S. Henney. Studies on the mechanism of lymphocyte-mediated cytolysis. VI. A reappraisal of the requirement for protein synthesis during T cell-mediated lysis. J. Immunol. 116:146–149 (1976).PubMedGoogle Scholar
  17. 17.
    Bevan, M.J., and M. Cohn. Cytotoxic effects of antigen-and mitogen-induced T cells on various targets. J. Immunol. 114:559–565 (1975).PubMedGoogle Scholar
  18. 18.
    Gately, M., and E. Martz. Comparative studies on the mechanisms of nonspecific. Con A-dependent cytolysis and specific T cell-mediated cytolysis. J. Immunol. 119:1711–1722 (1977).PubMedGoogle Scholar
  19. 19.
    Parker, W.L., and E. Martz. Lectin-induced nonlethal adhesions between cytolytic T lymphocytes and antigenically unrecognizable tumor cells, and nonspecific “triggering” of cytolysis. J. Immunol. 124:25–35 (1980).PubMedGoogle Scholar
  20. 20.
    Küppers, R.C., and C.S. Henney. Studies on the mechanism of lymphocyte-mediated cytolysis. IX. Relationships between antigen recognition and lytic expression in killer T cells. J. Immunol. 118:71–76 (1977).PubMedGoogle Scholar
  21. 21.
    Grimm, E., and B. Bonavida. Mechanism of cell-mediated cytotoxicity at the single cell level. I. Estimation of cytotoxic T lymphocyte frequency and relative lytic efficiency. J. Immunol. 123:2861–2869 (1979).PubMedGoogle Scholar
  22. 22.
    Golstein, P., and E.T. Smith. The lethal hit stage of mouse T and non-T cell-mediated cytolysis. Differences in cation requirements and characterization of an analytical “cation pulse” method. Eur. J. Immunol. 6:31–37 (1976).PubMedCrossRefGoogle Scholar
  23. 23.
    Wagner, H., and M. Rollinghoff. T cell-mediated cytotoxicity: Discrimination between antigen recognition, lethal hit and cytolysis phase. Eur. J. Immunol. 4:745–750 (1974).PubMedCrossRefGoogle Scholar
  24. 24.
    Martz, E. Early steps in specific tumor cell lysis by sensitized mouse T-lymphocytes. I. Resolution and characterization. J. Immunol. 115:261–267 (1975).PubMedGoogle Scholar
  25. 25.
    Martz, E. Immune lymphocyte to tumor cell adhesion: magnesium sufficient, calcium insufficient. J. Cell Biol. 84:584–598 (1980).PubMedCrossRefGoogle Scholar
  26. 26.
    Gately, M.K., and E. Martz. Early steps in specific tumor cell lysis by sensitized mouse T lymphocytes. III. Resolution of two distinct roles for calcium in the cytolytic process. J. Immunol. 122:482–489 (1979).PubMedGoogle Scholar
  27. 27.
    Plaut, M., J.E. Bubbers, and C.S. Henney. Studies on the mechanism of lymphocyte-mediated cytolysis. VII. Two stages in the T cell-mediated lytic cycle with distinct cation requirements. J. Immunol. 116:150–155 (1976).PubMedGoogle Scholar
  28. 28.
    Golstein, P., C. Foa, and I.C.M. MacLennan. Mechanism of T-cell-mediated cytolysis: The differential impact of cyto-chalasins at the recognition and lethal hit stages. Eur. J. Immunol. 8:302–309 (1978).PubMedCrossRefGoogle Scholar
  29. 29.
    Gately, M.K., and E. Martz. Inhibition of the lethal hit phase of T cell-mediated cytolysis by pharmacologic agents. Fed. Proc. 38:1166 (Abs. #4960) (1979).Google Scholar
  30. 30.
    Golstein, P. and E.T. Smith. Mechanism of T cell-mediated cytolysis: The lethal hit stage. Contemp. Top. Immunobiol. 7:273–300 (1977).PubMedCrossRefGoogle Scholar
  31. 31.
    Martz E., C.D. Tsoukas, and W.J. Wechter. Evidence against Ca++ poisoning by killer cells: Mast cells killed by T lymphocytes do not secrete prelytically. J. Supramol. Struct. Suppl. 3:311 (Abstract 818) (1979).Google Scholar
  32. 32.
    Ko, L., and D. Lagunoff. Depletion of mast cell ATP inhibits complement-dependent cytotoxic histamine release. Exp. Cell Res. 100:313–321 (1976).PubMedCrossRefGoogle Scholar
  33. 33.
    Henney, C.S. T cell mediated cytolysis: Consideration of the role of a soluble mediator. J. Reticuloendothelial Soc. 17:231–235 (1975).Google Scholar
  34. 34.
    Todd, R.F., and G. Berke. Functional characterization of membrane components of cytotoxic peritoneal exudate T lymphocytes. I. Search for T cell receptor activity in lymphocyte membrane fractions. Immunochemistry 11:313–320 (1974).PubMedCrossRefGoogle Scholar
  35. 35.
    Whisnant, C.C., K.H. Singer, and D.B. Amos. Interaction of cytotoxic T lynnphocytes with target cells. I. Specific inhibition by detergent-solubilized, partially purified mouse histocompatibility anitgens. J. Immunol. 121:2253 (1978).PubMedGoogle Scholar
  36. 36.
    Todd, R.F. III, R.D. Stuiting, and D.B. Amos. Lymphocyte-mediated cytolysis of allogeneic tumor cells in vitro. I. Search for target antigens in subcellular fractions. Cellular Immunol. 18:304–323 (1975).CrossRefGoogle Scholar
  37. 37.
    Nagy, Z.A., and B.E. Elliott. The receptor specificity of alloreactive T cells. Distinction between stimulator K, I, and D region products and degeneracy of third-party H-2 recognition by low-affinity T cells. J. Exp. Med. 150:1520–1537 (1979).PubMedCrossRefGoogle Scholar
  38. 38.
    Linna, T.J., H.D. Engers, J.-C. Cerottini, and K.T. Brunner. Inhibition of cytolytic T lymphocyte activity with subcellular alloantigen preparations and with unlabeled allogenic target cells. J. Immunol. 120:1544–1549 (1978).PubMedGoogle Scholar
  39. 39.
    Gilmer, P.J., H.O. McDevitt, and H.M. McConnell. Inhibition of specific T cell-target cell conjugates by target cell plasma membranes. J. Immunol. 120:774 (1978).PubMedGoogle Scholar
  40. 40.
    Ozato, K., H.K. Ziegler, and C.S. Henney. Liposomes as model membrane systems for immune attack. I. Transfer of antigenic determinants to lymphocyte membranes after interactions with hapten-bearing liposomes. J. Immunol. 121:1376 (1978).PubMedGoogle Scholar
  41. 41.
    Kimura, A.K., and H. Wigzell. Cell surface glycoproteins of murine cytotoxic T lymphocytes. I. T 145, a new surface glycoprotein selectively expressed on Ly l cytotoxic T lymphocytes. J. Exp. Med. 147:1418–1434 (1978).PubMedCrossRefGoogle Scholar
  42. 42.
    Berke, G., Y. Kaufmann, and D. Gabison. Cell surface determinants of cytotoxic T lymphocytes: possible role in lymphocyte-target cell interaction. Fed. Proc. 39:1198 (Abstract #4891) (1980).Google Scholar
  43. 43.
    Gately, M.K., and E. Martz. Til: A new protein marker on activated murine T lymphocytes. J. Immunol. 126:709–714 (1981).PubMedGoogle Scholar
  44. 44.
    Reif, A.E., and J.M. Allen. The AKR thymic antigen and its distribution in leukemias and nervous tissues. J. Exp. Med. 120:413 (1964).PubMedCrossRefGoogle Scholar
  45. 45.
    Davignon, D., E. Martz, T. Reynolds, K. Kurzinger, and T.A. Springer. Lymphocyte function-associated antigen one (LFA-1): a surface antigen distinct from Lyt-2/3 that participates in T lymphocyte-mediated killing. Proc. Natl. Acad. Sci. USA 78:4535–4539 (1981).PubMedCrossRefGoogle Scholar
  46. 46.
    Kimura, A.K., and H. Wigzell. Cytotoxic T lymphocyte membrane components: An analysis of structures related to function. Cont. Top. Mol. Immunol. 6:209–244 (1977).Google Scholar
  47. 47.
    Redelman, D., and P.E. Trefts. In vitro studies of the rabbit immune system. VIII. Rabbit anti-mouse cytotoxic T-effector cells are inhibited by anti-rabbit T-cell serum in the absence of complement. J. Immunol. 121:1532–1539 (1978).PubMedGoogle Scholar
  48. 48.
    Rabinowitz, R., and M. Schlesinger. Inhibition of the activity of cytotoxic murine T lymphocytes by antibodies to idiotypic determinants. Immunol. 39:93–99 (1980).Google Scholar
  49. 49.
    Kimura, A.K. Inhibition of specific cell-mediated cytotoxicity by anti-T-cell receptor antibody. J. Exp. Med. 139:888–901 (1974).PubMedCrossRefGoogle Scholar
  50. 50.
    Rabinowitz, R., R. Laskov, and M. Schlesinger. Inhibition of cell-mediated lysis by xenoantibodies reactive with effector T lymphocytes. Eur. J. Immunol. 10:219–223 (1980).PubMedCrossRefGoogle Scholar
  51. 51.
    Hiserodt, J.C., and B. Bonavida. Studies on the induction and expression of T cell-mediated immunity. XI. Inhibition of the “Lethal Hit” in T cell-mediated cytotoxicity by heterologous rat antiserum made against alloimmune cytotoxic T lymphocytes. J. Immunol. 126:256–262 (1981).PubMedGoogle Scholar
  52. 52.
    Platsoucas, C.D., and R.A. Good. Inhibition of specific cell-mediated cytotoxicity by monoclonal antibodies to human T cell antigens. Proc. Natl. Acad. Sci. USA 78:4500–4504 (1981).PubMedCrossRefGoogle Scholar
  53. 53.
    Chang, T.W., P.C. Kung, S.P. Gingras, and G. Goldstein. Does 0KT3 monoclonal antibody react with an antigen-recognition structure on human T cells? Proc. Natl. Acad. Sci. USA 78: 1805–1808 (1981).PubMedCrossRefGoogle Scholar
  54. 54.
    Tsoukas, C.D., R.I. Fox, D.A. Carson, S. Fong, and J.H. Vaughan. Monoclonal antibody 0KT3 blocks the function of human cytotoxic T-lymphocytes against autologous EBV-transformed target cells. Submitted for publication.Google Scholar
  55. 55.
    Reinherz, E.I., R.E. Hussey, and S.F. Schlossman. A monoclonal antibody blocking htiman T cell function. Eur. J. Immunol. 10: 758–762 (1980).PubMedCrossRefGoogle Scholar
  56. 56.
    Evans, R.L., D.W. Wall, C.D. Platsoucas, F.P. Siegal, S.M. Fikrig, C.M. Testa, and R.A. Good. Thymus-dependent membrane antigens in man: inhibition of cell-mediated lympholysis by monoclonal antibodies to antigen. Proc. Natl. Acad. Sci. USA 78:544–548 (1981).PubMedCrossRefGoogle Scholar
  57. 57.
    Ledbetter, J.A., R.L. Evans, M. Lipinski, C. Cunningham-Rundles, R.A. Good, and L.A. Herzenberg. Evolutionary conservation of surface molecules that distinguish T Ijmiphocyte helper/inducer and cytotoxic/suppressor subpopulations in mouse and man. J. Exp. Med. 153:310–323 (1981).PubMedCrossRefGoogle Scholar
  58. 58.
    Ledbetter, J.A., and L.A. Herzenberg. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunological Rev. 47:63–89 (1979).CrossRefGoogle Scholar
  59. 59.
    Nakayama, E., H. Shiku, E. Stockert, H.F. Oettgen, and L.J. Old. Cytotoxic T cells: Lyt phenotype and blocking of killing activity by Lyt antisera. Proc. Natl. Acad. Sci. USA 76:1977–1981 (1979).PubMedCrossRefGoogle Scholar
  60. 60.
    Shinohara, N., and D.H. Sachs. Mouse alloantibodies capable of blocking cytotoxic T-cell function. I. Relationship between the antigen reactive with blocking antibodies and the Lyt-2 locus. J. Exp. Med. 150:432–444 (1979).PubMedCrossRefGoogle Scholar
  61. 61.
    Fan, J., A. Ahmed, and B. Bonavida. Studies on the induction and expression of T cell-mediated immunity. X. Inhibition by Lyt-2, 3 antisera of cytotoxic T lymphocyte-mediated antigen-specific and nonspecific cytotoxicity: Evidence for the blocking of the binding between T lymphocytes and target cells and not the post-binding cytolytic steps. J. Immunol. 125: 2444–2453 (1980).PubMedGoogle Scholar
  62. 62.
    Shinohara, N., M. Taniguchi, and M. Kojima. Mouse alloantibodies capable of blocking cytotoxic T cell function. III. Studies of the mechanism of blocking of CML by anti-Lyt-2 antibodies. J. Immunol. 127:1575–1578 (1981).PubMedGoogle Scholar
  63. 63.
    Pierres, P., C. Goridis, and P. Golstein. Inhibition of murine T cell-mediated cytolysis and T cell proliferation by a rat monoclonal antibody immunoprecipitating two lymphoid cell surface polypeptides of 94,000 and 180,000 molecular weight. Eur. J. Immunol., in press (1981).Google Scholar
  64. 64.
    MacDonald, H.R., N. Thiernesse, and J.-C. Cerottini. Inhibition of T cell-mediated cytolysis by monoclonal antibodies directed against Lyt-2: heterogeneity of inhibition at the clonal level. J. Immunol. 126:1671–1675 (1981).PubMedGoogle Scholar
  65. 65.
    Ledbetter, J.A., W.E. Seaman, T.T. Tsu, and L.A. Herzenberg. Lyt-2 and Lyt-3 antigens are on two different polypeptide sub-units linked by disulfide bonds. Relationship of subunits to T cell cytolytic activity. J. Exp. Med. 153:1503–1516 (1981).PubMedCrossRefGoogle Scholar
  66. 66.
    Fan, J., and B. Bonavida. Studies on the induction and expression of T cell-mediated immunity. XII. The concomitant loss and recovery of membrane-associated Lyt-2 antigens, Ijnnphocyte-target cell binding, and the antigen-specific and-nonspecific cytotoxic activity of alloimmune T lymphocytes after treatment with trypsin. J. Immunol. 127:1856–1864 (1981).PubMedGoogle Scholar
  67. 67.
    Dialynas, D.P., M.R. Loken, A.L. Glasebrook, and F.W. Fitch. Lyt-2/Lyt-3 variants of a cloned cytolytic T cell line lack an antigen receptor functional in cytolysis. J. Exp. Mèd. 153:595–604 (1981).PubMedCrossRefGoogle Scholar
  68. 68.
    Kurzinger, K., T. Reynolds, R.N. Germain, D. Davignon, E. Martz., and T.A. Springer. A novel lymphocyte function-associated antigen (LFA-1): cellular distribution, qxiantitative expression, and structure. J. Immunol. 127:596–602 (1981).PubMedGoogle Scholar
  69. 69.
    Davignon, D., E. Martz, T. Reynolds, K. Kurzinger, and T.A. Springer. Monoclonal antibody to a novel lymphocyte function-associated antigen (LFA-1). Mechanism of blockade of T lympho-cyte-mediated killing and effects on other T and B lymphocyte functions. J. Immunol. 127:590–595 (1981).PubMedGoogle Scholar
  70. 70.
    Shortman, K., and P. Golstein. Target cell recognition by cytolytic T cells: Different requirements for the formation of strong conjugates or for proceeding to lysis. J. Immunol. 123: 833–839 (1979).PubMedGoogle Scholar
  71. 71.
    Martz, E. Inability of EDTA to prevent damage mediated by cytolytic T-l3rmphocytes. Cellular Immunol. 20:304–314 (1975).CrossRefGoogle Scholar
  72. 72.
    Springer, T.A. Mac-1, 2, 3, and 4: Murine macrophage differentiation antigens identified by monoclonal antibodies. In: “Heterogeneity of mononuclear phagocytes,” O. Forster, ed., Academic Press, New York. In press (1980).Google Scholar
  73. 73.
    Shinohara, N., U. Hammerling, and D.H. Sachs. Mouse allo-antibodies capable of blocking cytotoxic T cell function. II. Further study on the relationship between the blocking antibodies and the products of the Lyt-2 locus. Eur. J. Immunol. 10:589–594 (1980).PubMedCrossRefGoogle Scholar
  74. 74.
    Hollander, N., E. Pillemer, and I.L. Weissman. The blocking effect of Lyt-2 antibodies on T cell functions. J. Exp. Med. 152:674–687 (1980).PubMedCrossRefGoogle Scholar
  75. 75.
    Sarmiento, M., A.L. Glasebrook, and F.W. Fitch. IgG or IgM monoclonal antibodies reactive with different determinants on the molecular complex bearing Lyt-2 antigen block T cell-mediated cytolysis in the absence of complement. J. Immunol. 125:2665–2672 (1980).PubMedGoogle Scholar
  76. 76.
    Springer, T.A., K. Kurzinger, T. Reynolds, R.N. Germain, D. Davignon, and E. Martz. MDnoclonal antibodies as probes of surface structures participating in T lymphocyte function. In: “Monoclonal Antibodies and T Cell Hybridomas,” U. Hammerling, G. Hammerling, and J. Kearney, eds., Elsevier. In press (1981).Google Scholar
  77. 77.
    Golstein, P., and M. Pierres. Monoclonal antibodies as probes to study the mechanism of T cell-mediated cytolysis. Proc. 14th Leukocyte Cult. Conf., in press (1981).Google Scholar
  78. 78.
    Lightbody, J.J., L. Urbani, and M.D. Poulik. Effect of beta-2 microglobulin antibody on effector function of T-cell mediated cytotoxicity. Nature 250:227–228 (1974).PubMedCrossRefGoogle Scholar
  79. 79.
    Golstein, P. H. Wigzell, H. Blomgren, and E.A.J. Svedmyr. Cells mediating specific in vitro cytotoxicity. II. Probable autonomy of thymus-processed lymphocytes (T cells) for the killing of allogeneic target cells. J. Exp. Med. 135:890–906 (1972).PubMedCrossRefGoogle Scholar
  80. 80.
    Undah K.F., and H. Lemke. Inhibition of killer-target cell interaction by monoclonal anti-H-2 antibodies. Eur. J. Immunol. 9:526–536 (1979).CrossRefGoogle Scholar
  81. 81.
    Epstein, S.L., K. Ozato, and D.H. Sachs. Blocking of allogeneic cell-mediated lympholysis by monoclonal antibodies to H-2 antigens. J. Immunol. 125:129–135 (1980).PubMedGoogle Scholar
  82. 82.
    Rothstein, T.L., M.G. Mage, J. Mond, and L.L. McHugh. Guinea pig antiserum to mouse cytotoxic T lymihocytes and their precursors. J. Immunol. 120:209 (1978).PubMedGoogle Scholar
  83. 83.
    Sullivan, K.A., G. Berke, and D.B. Amos. An antigenic determinant of cytotoxic Ijrmphocytes. Transplantation 16:388–391 (1973).PubMedCrossRefGoogle Scholar
  84. 84.
    Braun, M. and F. Saal. The T-cell receptor and cytotoxicity. An anti-idiotype antiserum that inhibits a graft-versus-host reaction does not inhibit cell-mediated cytotoxicity. Cellular Immunol. 30:254–260 (1977).CrossRefGoogle Scholar
  85. 85.
    Lindahl, K.F. Antisera against recognition sites: lack of effect on the mixed leucocyte culture interaction. Eur. J. Immunol. 2:501–504 (1972).PubMedCrossRefGoogle Scholar
  86. 86.
    Sherman, L.A., S.J. Burakoff, and B. Benacerraf. The induction of cytolytic T lymphocytes with specificity for p-azophenyl-arsonate coupled syngeneic cells. J. Immunol. 121:1432 (1978).PubMedGoogle Scholar
  87. 87.
    Rubin, B., P. Golstein, O. Nordfang, and B. Hertel-Wulff. Generation of H-2-reactive T cell lines that bear the 5936 idiotype(s). J. Immunol. 124:161–167 (1980).PubMedGoogle Scholar
  88. 88.
    Binz, H., and H. Wigzell. Antigen-binding, idiotypic T-lympho-cyte receptors. In: “Contemporary topics in immunobiology volume 7: T cells,” O. Stutman, Ed., Plenum Press, New York, pp. 113–177 (1977).CrossRefGoogle Scholar
  89. 89.
    Glasebrook, A.L. Conjugate formation by primary and secondary populations of murine immune T lymphocytes. J. Immunol. 121: 1870–1877 (1978).PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1982

Authors and Affiliations

  • Eric Martz
    • 1
  • Denise Davignon
    • 2
  • Konrad Kürzinger
    • 2
  • Timothy A. Springer
    • 2
  1. 1.The Department of MicrobiologyUniversity of MassachusettsAmherstUSA
  2. 2.The Laboratory of Membrane Immunochemistry, Sidney Farber Cancer InstituteHarvard Medical SchoolBostonUSA

Personalised recommendations