Dependence of T cell antigen recognition on the dimensions of an accessory receptor-ligand complex

Journal of Experimental Medicine

Volumn 190, Issue 1, 1999, Pages 31-41

  Wild, Martin K ^a   Cambiaggi, Anna ^a   Brown, Marion H ^a   Davies, Elizabeth A ^a   Ohno, Hiroshi ^b   Saito, Takashi ^c   Van Der Merwe, P Anton ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KANAZAWA UNIVERSITY   (Japan)

^c CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

CD2; CD48; Plasma membrane; T cell activation; T cell receptor

Indexed keywords

CD2 ANTIGEN; CD28 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; INTEGRIN; INTERLEUKIN 2; LEUKOSIALIN; MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; LIGAND BINDING; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD2; BLOTTING, WESTERN; CHO CELLS; CRICETINAE; DOWN-REGULATION; FLOW CYTOMETRY; LIGANDS; MACROMOLECULAR SUBSTANCES; MICE; PROTEIN BINDING; RATS; RECEPTORS, ANTIGEN, T-CELL;

EID: 0033526773     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.1.31     Document Type: Article

References (68)

1. Springer, T.A. 1990. The sensation and regulation of interactions with the extracellular environment: the cell biology of lymphocyte adhesion receptors. Annu. Rev. Cell Biol. 6:359-402.
2. Barclay, A.N., M.L. Birkeland, M.H. Brown, A.D. Beyers, S.J. Davis, C. Somoza, and A.F. Williams. 1993. The Leucocyte Antigen Factsbook. 1st ed. Academic Press Ltd., London. 424 pp.
3. Garboczi, D.N., P. Ghosh, U. Utz, Q.R. Fan, W.E. Biddison, and D.C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature. 384:134-141.
4. Garcia, K.C., M. Degano, R.L. Stanfield, A. Brunmark, M.R. Jackson, P.A. Peterson, L. Teyton, and I.A. Wilson. 1996. An αβ T cell receptor structure at 2.5 Å and its orientation in the TCR-MHC complex. Science. 274:209-219.
5. Bjorkman, P.J., M.A. Saper, B. Samraoui, W.S. Bennett, J.L. Strominger, and D.C. Wiley. 1987. Structure of the human class I histocompatibility antigen HLA-A2. Nature. 329: 506-512.
6. Brown, J.H., T.S. Jardetsky, J.C. Gorga, L.J. Stern, R.G. Urban, J.L. Strominger, and D.C. Wiley. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature. 364:33-39.
7. Barclay, A.N., M.H. Brown, S.K.A. Law, A.J. McKnight, M.G. Tomlinson, and P.A. van der Merwe. 1997. The Leucocyte Antigen Factsbook. 2nd ed. Factsbook Series. Academic Press Ltd., London. 613 pp.
8. van der Merwe, P.A., P.N. McNamee, E.A. Davies, A.N. Barclay, and S.J. Davis. 1995. Topology of the CD2-CD48 cell-adhesion molecule complex: implications for antigen recognition by T cells. Curr. Biol. 5:74-84.
9. Shaw, A.S., and M.L. Dustin. 1997. Making the T cell receptor go the distance: a topological view of T cell activation. Immunity. 6:361-369.
10. Springer, T. A. 1990. Adhesion receptors of the immune system. Nature. 346:425-434.
11. Springer, T.A., M.L. Dustin, T.K. Kishimoto, and S.D. Marlin. 1987. The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system. Anna. Rev. Immunol. 5:223-252.
12. Bierer, B.E., and S.J. Burakoff. 1989. T-lymphocyte activation: the biology and function of CD2 and CD4. Immunol. Rev. 111:267-294.
13. Davis, S.J., and P.A. van der Merwe. 1996. Structure and ligand interactions of CD2: implications for T-cell function. Immunol. Today. 17:177-187.
14. Jones, E.Y., S.J. Davis, A.F. Williams, K. Harlos, and D.A. Stuart. 1992. Crystal structure of a soluble form of the cell adhesion molecule CD2 at 2.8 Å. Nature. 360:232-239.
15. Bodian, D.L., E.Y. Jones, D.I. Stuart, K.H. Harlos, E.A. Davies, and S.J. Davis. 1994. Crystal structure of the extracellular region of the human cell adhesion molecule CD2 at 2.5 Å resolution. Structure. 2:755-766.
16. Bell, G.M., J. Fargnoli, J.B. Bolen, L. Kish, and J.B. Imboden. 1996. The SH3 domain of p56lck binds to proline-rich sequences in the cytoplasmic domain of CD2. J. Exp. Med. 183:169-178.
17. Dustin, M.L., M.W. Olszowy, A.D. Holdorf, J. Li, S. Bromley, N. Desai, P. Widder, F. Rosenberger, P.A. van der Merwe, P.M. Allen, and A.S. Shaw. 1998. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T cell contacts. Cell. 94:667-677.
18. Li, J., K. Nishizawa, W. An, R.E. Hussey, F.E. Lialios, R. Salgia, R. Sunder-Plassmann, and E.L. Reinherz. 1998. A cdc15-like adaptor protein (CD2BP1) interacts with the CD2 cytoplasmic domain and regulates CD2-triggered adhesion. EMBO (Eur. Mol. Biol. Organ.) J. 17:7320-7336.
19. Hunig, T. 1985. The cell surface molecule recognized by the erythrocyte receptor of T lymphocytes. Identification and partial characterization using a monoclonal antibody. J. Exp. Med. 162:890-901.
20. Selvaraj, P., M.L. Plunkett, M. Dustin, M.E. Sanders, S. Shaw, and T.A. Springer. 1987. The T lymphocyte glycoprotein CD2 binds the cell surface ligand LFA-3. Nature. 326:400-403.
21. Kato, K., M. Koyanaga, H. Okada, T. Takanashi, Y.W. Wong, A.F. Williams, K. Okumura, and H. Yagita. 1992. CD48 is a counter-receptor for mouse CD2 and involved in T cell activation. J. Exp. Med. 176:1241-1249.
22. van der Merwe, P.A., D.C. McPherson, M.H. Brown, A.N. Barclay, J.G. Cyster, A.F. Williams, and S.J. Davis. 1993. The NH2-terminal domain of rat CD2 binds rat CD48 with a low affinity and binding does not require glycosylation of CD2. Eur. J. Immunol. 23:1373-1377.
23. Wong, Y.W., A.F. Williams, S.F. Kingsmore, and M.F. Seldin. 1990. Structure, expression, and genetic linkage of the mouse BCM1 (OX45 or Blast-1) antigen. Evidence for genetic duplication giving rise to the BCM1 region on mouse chromosome 1 and the CD2/LFA3 region on mouse chromosome 3. J. Exp. Med. 171:2115-2130.
24. Williams, A.F., and A.N. Barclay. 1988. The immunoglobulin superfamily-domains for cell surface recognition. Annu. Rev. Immunol. 6:381-405.
25. Moingeon, P., H.C. Chang, P.H. Sayre, L.K. Clayton, A. Alcover, P. Gardner, and E.L. Reinherz. 1989. The structural biology of CD2. Immunol. Rev. 111:111-144.
26. Ohno, H., T. Nakamura, H. Yagita, K. Okumura, M. Taniguchi, and T. Saito. 1991. Induction of negative signal through CD2 during antigen-specific T cell activation. J. Immunol. 147:2100-2106.
27. Killeen, N., S.G. Stuart, and D.R. Littman. 1992. Development and function of T cells in mice with a disrupted CD2 gene. EMBO (Eur. Mol. Biol. Organ.) J. 11:4329-4336.
28. Evans, C.F., G.F. Rall, N. Killeen, D. Littman, and M.B.A. Oldstone. 1993. CD2-deficient mice generate virus-specific cytotoxic T lymphocytes upon infection with lymphocytic choriomeningitis. J. Immunol. 151:6259-6264.
29. Teh, S.J., N. Killeen, A. Tarakhovsky, D.R. Littman, and H.S. Teh. 1997. CD2 regulates positive selection and function of antigen-specific CD4-CD8+ T cells. Blood. 89: 1308-1318.
30. Beyers, A.D., A.N. Barclay, D.A. Law, Q. He, and A.F. Williams. 1989. Activation of T lymphocytes via monoclonal antibodies against rat cell surface antigens with particular reference to CD2 antigen. Immunol. Rev. 111:59-77.
31. Garcia, K.C., M. Degano, L.R. Pease, M. Huang, P.A. Peterson, L. Teyton, and I.A. Wilson. 1998. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science. 279:1166-1172.
32. Hedrick, S.M., L.A. Matis, T.T. Hecht, L.E. Samelson, D.L. Longo, E. Heber-Katz, and R.H. Schwartz. 1982. The fine specificity of antigen and Ia determinant recognition by T cell hybridoma clones specific for pigeon cytochrome c. Cell. 30:141-152.
33. Wettstein, D.A., J.J. Boniface, P.A. Reay, H. Schild, and M.M. Davis. 1991. Expression of a class II major histocompatibility complex (MHC) heterodimer in a lipid-linked form with enhanced peptide/soluble MHC complex formation at low pH. J. Exp. Med. 174:219-228.
34. Jorgensen, J.L., U. Esser, B. Fazekas de St. Groth, P. Reay, and M.M. Davis. 1992. Mapping the T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature. 355:224-230.
35. Yagita, H., T. Nakamura, H. Karasuyama, and K. Okumura. 1989. Monoclonal antibodies specific for murine CD2 reveal its presence on B as well as T cells. Proc. Natl. Acad. Sci. USA. 86:645-648.
36. Hunt, S.V., and M.H. Fowler. 1981. A repopulation assay for B and T lymphocyte stem cells employing radiation chimaeras. Cell Tissue Kinet. 14:445-464.
37. Dyer, M.J., and S.V. Hunt. 1981. Committed T lymphocyte stem cells of rats. Characterization by surface W3/13 antigen and radiosensitivity. J. Exp. Med. 154:1164-1177.
38. Leo, O., M. Foo, D.H. Sachs, L.E. Samelson, and J.A. Bluestone. 1987. Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc. Natl. Acad. Sci. USA. 84: 1374-1378.
39. Samelson, L.E., R.N. Germain, and R.H. Schwartz. 1983. Monoclonal antibodies against the antigen receptor on a cloned T-cell hybrid. Proc. Natl. Acad. Sci. USA. 80:6972-6976.
40. Brown, M.H., K. Boles, P.A. van der Merwe, V. Kumar, P.A. Mathew, and A.N. Barclay. 1998. 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J. Exp. Med. 188:2083-2090.
41. van der Merwe, P.A., A.N. Barclay, D.W. Mason, E.A. Davies, B.P. Morgan, M. Tone, A.K.C. Krishnam, C. Ianelli, and S.J. Davis. 1994. The human cell-adhesion molecule CD2 binds CD58 with a very low affinity and an extremely fast dissociation rate but does not bind CD48 or CD59. Biochemistry. 33:10149-10160.
42. Sewell, W.A., M.H. Brown, J. Dunne, M.J. Owen, and M.J. Crumpton. 1986. Molecular cloning of the human T-lymphocyte surface CD2 (T11) antigen. Proc. Natl. Acad. Sci. USA. 83:8718-8722.
43. van der Merwe, P.A., P. Crocker, M. Vincent, A.N. Barclay, and S. Kelm. 1996. Localization of the putative sialic acid binding site on the immunoglobulin superfamily cell surface molecule CD22. J. Biol. Chem. 271:9273-9280.
44. Bebbington, C.R., and C.C.G. Hentschel. 1987. The use of vectors based on gene amplification for the expression of cloned genes in mammalian cells. In DNA Cloning: A Practical Approach. D.M. Glover, editor. IRL Press, Oxford. 163-188.
45. Bebbington, C.R. 1991. Expression of antibody genes in nonlymphoid mammalian cells. Methods: A Companion to Methods in Enzymology. 2:136-145.
46. Davis, S.J., S. Ikemizu, M.K. Wild, and P.A. van der Merwe. 1998. CD2 and the nature of protein interactions mediating cell-cell recognition. Immunol. Rev. 163:217-236.
47. Brown, M.H., S. Preston, and A.N. Barclay. 1995. A sensitive assay for detecting low affinity interactions at the cell surface reveals no additional ligands for the adhesion pair rat CD2 and CD48. Em. J. Immunol. 25:3222-3228.
48. van der Merwe, P.A., D.L. Bodian, S. Daenke, P. Linsley, and S.J. Davis. 1997. CD80 (B7-1) binds both CD28 and CTLA-4 with a low affinity and very fast kinetics. J. Exp. Med. 185:393-403.
49. Moingeon, P., H.-C. Chang, B.P. Wallner, C. Stebbins, A.Z. Frey, and E.L. Reinherz. 1989. CD2-mediated adhesion facilitates T lymphocyte antigen recognition function. Nature. 339:312-314.
50. Samelson, I.E., and R.H. Schwartz. 1983. T cell clone-specific alloantisera that inhibit or stimulate antigen-induced T cell activation. J. Imnnmol. 131:2645-2650.
51. Reay, P.A., R.M. Kantor, and M.M. Davis. 1994. Use of global amino acid analysis replacements to define the requirements for MHC binding and T cell recognition of moth cytochrome c (93-103). J. Imnnmol 152:3946-3957.
52. Melton, E., N. Sarner, M. Torkar, P.A. van der Merwe, J.Q. Russell, R.C. Budd, C. Mamalaki, M. Tolaini, D. Kioussis, and R. Zamoyska. 1996. Transgene-encoded human CD2 acts in a dominant negative fashion to modify thymocyte selection signals in mice. Eur. J. Immunol. 26:2952-2963.
53. van der Merwe, P.A., M.H. Brown, S.J. Davis, and A.N. Barclay. 1993. Affinity and kinetic analysis of the interaction of the cell-adhesion molecules rat CD2 and CD48. EMBO (Eur. Mol. Biol. Organ.) J. 12:4945-4954.
54. Dustin, M.L., D.E. Golan, D.M. Zhu, J.M. Miller, W. Meier, E.A. Davies, and P.A. van der Merwe. 1997. Low affinity interaction of human or rat cell adhesion molecule CD2 with ligands aligns adhering membranes to achieve high physiological affinity. J. Biol. Chem. 272:30889-30898.
55. Meuer, S.C., R.E. Hussey, M. Fabbi, D. Fox, O. Acuto, K.A. Fitzgerald, J.C. Hodgdon, J.P. Protentis, S.F. Schlossman, and E.L. Reinherz. 1984. An alternative pathway of T-cell activation: a functional role for the 50 kd T11 sheep erythrocyte receptor protein. Cell. 36:897-906.
56. Hahn, W.C., Y. Rosenstein, V. Calvo, S.J. Burakoff, and B.E. Bierer. 1992. A distinctive cytoplasmic domain of CD2 regulates avidity and T-cell responsiveness to antigen. Proc. Natl. Acad. Sci. USA. 89:7179-7183.
57. Valitutti, S., S. Müller, M. Cella, E. Padovan, and A. Lanzavecchia. 1995. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature. 375:148-151.
58. Viola, A., and A. Lanzavecchia. 1996. T cell activation determined by T cell receptor number and tunable thresholds. Science. 273:104-106.
59. Biberfeld, P., and A. Johansson. 1975. Contact areas of cytotoxic lymphocytes and target cells. Exp. Cell Res. 94:79-87.
60. Monks, C.R., B.A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature. 395:82-86.
61. Sperling, A.I., J.R. Sedy, N. Manjunath, A. Kupfer, A. Ardman, and J.K. Burkhardt. 1998. Cutting edge: TCR signaling induces selective exclusion of CD43 from the T cell-antigen-presenting cell contact site. J. Immunol. 161:6459-6462.
62. Bachmann, M.F., K. McKall-Faienza, R. Schmits, D. Bouchard, J. Beach, D.E. Speiser, T.W. Mak, and P.S. Ohashi. 1997. Distinct roles for LFA-1 and CD28 during activation of naive T cells: adhesion versus costimulation. Immunity. 7:549-557.
63. Penninger, J.M., and G.R. Crabtree. 1999. The actin cytoskeleton and lymphocyte activation. Cell. 96:9-12.
64. Lenschow, D.J., T.L. Walunas, and J.A. Bluestone. 1996. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14:233-258.
65. Nagel, T., J. Shi, K.E. Truitt, and J.B. Imboden. 1998. Adhesion of CD28 to its ligands B7-1 and B7-2, but not CD28-mediated signalling is critical for T cell costimulation in an antigen-specific in vitro model. The Immunologist. 1(Suppl.):388. (Abstr.)
66. Cocks, B.G., C.C.J. Chang, J.M. Carballido, H. Yssel, J.E. Devries, and G. Aversa. 1995. A novel receptor involved in T-cell activation. Nature. 376:260-263.
67. Garni-Wagner, B.A., A. Purohit, P.A. Mathew, M. Bennett, and V. Kumar. 1993. A novel function-associated molecule related to non-MHC-restricted cytotoxicity mediated by activated natural killer and T cells. J. Immunol. 151:60-70.
68. Mathew, P.A., B.A. Garni-Wagner, K. Land, A. Takashima, E. Stoneman, M. Bennett, and V. Kumar. 1993. Cloning and characterization of the 2B4 gene encoding a molecule associated with non-MHC-restricted killing mediated by activated natural killer and T cells. J. Immunol. 151:5328-5337.