The role of CTLA-4 in the regulation and initiation of T-Cell responses

Immunological Reviews

Volumn , Issue 153, 1996, Pages 27-46

  Chambers, Cynthia A ^a   Krummel, Matthew F ^b   Boitel, Brigitte ^a   Hurwitz, Andrew ^a   Sullivan, Tim J ^a   Fournier, Sylvie ^a   Cassell, Delanie ^a   Brunner, Monika ^a   Allison, James P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; ABATACEPT; ANTIBODY CONJUGATE; CYTOTOXIC T-LYMPHOCYTE ANTIGEN 4; DIFFERENTIATION ANTIGEN; IMMUNOSUPPRESSIVE AGENT; LEUKOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

CELLULAR IMMUNITY; IMMUNE RESPONSE; IMMUNOREGULATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANTIGEN PRESENTING CELL; BIOLOGICAL MODEL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM;

ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD28; ANTIGENS, CD80; ANTIGENS, DIFFERENTIATION; IMMUNOCONJUGATES; IMMUNOSUPPRESSIVE AGENTS; LYMPHOCYTE ACTIVATION; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0030300139     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065x.1996.tb00919.x     Document Type: Review

References (81)

1. Allison, J. P. (1994) CD28-B7 interactions in T-cell activation. Curr. Opin. Immunol. 6, 414.
2. Allison, J. P., Hurwitz, A. A. & Leach, D. R. (1995) Manipulation of costimulatory signals to enhance antitumor T-cell responses. Curr. Opin. Immunol. 7, 682.
3. August, A. & Dupont, B. (1993) CD28 of T lymphocytes associates with phosphatidylinositol 3-kinase. Int. Immunol. 6, 769.
4. Azuma, M., Ito, D., Yagita, H., Okumura, K., Phillips, J. H., Lanier, L. & Somoza, C. (1993) B70 antigen is a second ligand for CTLA-4 and CD28. Nature 366, 76.
5. Baskar, S., Ostrand-Rosenberg, S., Nabavi, N., Nadler, L. M., Freeman, G. J. & Glimcher, L. H. (1993) Constitutive expression of B7 restores immunogenicity of tumor cells expressing truncated major histocompatibility complex class II molecules. Proc. Natl. Acad. Sci. USA 90, 5687.
6. Boise, L. H., Noel, P. J. & Thompson, C. B. (1995a) CD28 and apoptosis. Curr. Opin. Immunol. 7, 620.
7. xL. Immunity 3, 87.
8. Brunet, J. F., Denizot, F., Luciani, M. F., Roux-Dosseto, M., Suzan, M., Mattei, M. F. & Golstein, P. (1987) A new member of the immunoglobulin superfamily CTLA-4. Nature 328, 267.
9. Burshtyn, D. N., Scharenberg, A. M., Wagtmann, N., Rajagoplan, S., Berrada, K., Yi, T., Kinet, J.-P. & Long, E.O. (1996) Recruitment of tyrosine phosphatase HCP by the killer cell inhibitory receptor. Immunity 4, 77.
10. Cai, Y.-C., Cefai, D., Schneider, H., Raab, M., Nabavi, N. & Rudd, C. E. (1995) Selective CD28pYMNM mutations implicate phosphatidylinositol 3-kinase in CD86-CD28-mediated costimulation. Immunity 3, 417.
11. Caux, C., Vanvervliet, B., Massacrier, C., Azuma, M., Okumura, K., Lanier, L. L. & Banchereau, J. (1994) B70/B7-2 is identical to CD86 and is the major functional ligand for CD28 expressed on human dendritic cells. J. Exp. Med. 180, 1841.
12. Chen, L., Ashe, S., Brady, W. A., Hellstrom, J., Hellstrom, K. E., Ledbetter, J. A., McGowan, P. & Linsley, P. S. (1992) Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4. Cell 71, 1093.
13. Crooks, M. E. C., Littman, D. R., Carter, R. H., Fearon, D. T., Weiss, A. & Stein, P. H. (1995) CD28-mediated costimulation in the absence of phosphatidylinositol 3-kinase association and activation. Mol. Cell. Biol. 15, 6820.
14. Cross, A. H., Girard, T. J., Giacoletto, K. S., Evans, R. J., Keeling, R. M., Lin, R. G., Trotter, J. L. & Karr, R. W. (1995) Long-term inhibition of marine experimental autoimmune encephalomyelitis using CTLA-4-Fc supports a key role for CD28 costimulation. J. Clin. Invest. 95, 2783.
15. D'Ambrosio, D., Hippen, K. L., Minskoff, S. A., Mellman, I., Pani, G., Siminovitch, K. A. & Cambier, J. C. (1995) Recruitment and activation of PTP-1C in negative regulation of antigen receptor signaling by FcγRHB1. Science 268, 293.
16. Dariavach, P., Mattel, M.-G., Golstein, P. & LeFranc, M.-P. (1988) Human Ig superfamily CTLA-4 gene: chromosomal localization and identity of protein sequence between murine and human CTLA-4 cytoplasmic domains. Eur. J. Immunol. 18, 1901.
17. Freeman, G. J., Freedman, A. S., Segil, J. M., Lee, G., Whitman, J. F. & Nadler, L. M. (1989) B7, a new member of the Ig superfamily with unique expression on activated and neoplastic B cells. J. Immunol. 143, 2714.
18. Freeman, G. J., Gray, G. S., Gimmi, C. D., Lombard, D. B., Zhou, L.-J., White, M., Fingeroth, J. D., Gribben, J. G. & Nadler, L. M. (1991) Structure, function, and T-cell costimulatory activity of the murine homologue of the human B lymphocyte activation antigen B7. J. Exp. Med. 174, 625.
19. Freeman, G. J., Lombard, D. B., Gimmi, C. D., Brod, S. A., Lee, K., Laning, J. C., Hafler, D. A., Dorf, M. E., Gray, G. S., Reiser, H., June, C. H., Thompson, C. B. & Nadler, L. M. (1992) CTLA-4 and CD28 mRNA are coexpressed in most T cells after activation. J. Immunol. 149, 3705.
20. Freeman, G. J., Gribben, J. G., Boussiotis, V. A., Ng, J. W., Restivo, Jr., V. A., Lombard, L.A., Gray, G.S. & Nadler, L.M. (1993) Cloning of B7-2: A CTLA-4 counterreceptor that costimulates human T-cell proliferation. Science 262, 909.
21. Freeman, G. J., Boussiotis, V. A., Anumanthan, A., Bernstein, G. M., Ke, X. Y., Rennert, P. D., Gray, G. S., Gribben, J. G. & Nadler, L. M. (1995) B7-1 and B7-2 do not deliver identical costimulatory signals, since B7-2 but not B7-1 preferentially costimulates the initial production of IL-4. Immunity 2, 523.
22. Gimmi, C. D., Freeman, G. J., Gribben, J. G., Sugita, K., Freedman, A. S., Morimoto, C. & Nadler, L. M. (1991) B-cell surface antigen B7 provides a costimulatory signal that induces T cells to proliferate and secrete interleukin 2. Proc. Natl. Acad. Sci. USA 88, 6575.
23. Green, J. M., Noel, P. J., Sperling, A. I., Walunas, T. L., Gray, G. S., Bluestone, J. A. & Thompson, C. B. (1994) Absence of B7-dependent responses in CD28-deficient mice. Immunity 1, 501.
24. Gribben, J. G., Freeman, G. J., Boussiotis, V. A., Rennert, P., Jellis, C. L., Greenfield, E., Barber, M., Restivo, V. A., Ke, X., Gray, G. S. & Nadler, L. M. (1995) CTLA-4 mediates antigen-specific apoptosis of human T-cells. Proc. Natl. Acad. Sci. USA 92, 811.
25. Harding, F. McArthur, J. G., Gross, J. A., Raulet, D. H. & Allison, J. P. (1992) CD28 mediated signalling costimulates murine T cells and prevents the induction of energy in T cell clones. Nature 356, 607.
26. Harper, K., Balzano, C., Rouvier, E., Mattei, M. G., Luciani, M. F. & Golstein, P. (1991) CTLA-4 and CD28 activated lymphocyte molecules are closely related in both mouse and human as to sequence, message expression, gene structure, and chromosomal location. J. Immunol. 147, 1037.
27. Hatada, M. H., Lu, X., Laird, E. R., Green, J., Morgenstern, J. P., Lou, M., Marr, C. S., Phillips, T. B., Ram, M. K. & Theriault, K. (1995) Molecular basis for interaction of the protein tyrosine kinase ZAP-70 with the T-cell receptor. Nature 376, 32.
28. Hathcock, K. S., Laszlo, G., Dickler, H. B., Bradshaw, J., Linsley, P. & Hodes, R. J. (1993) Identification of an alternative CTLA-4 ligand costimulatory for T cell activation. Science 262, 905.
29. Hathcock, K. S., Laszlo, G., Pucillo, C., Linsley, P. & Hodes, R. J. (1994) Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J. Exp. Med. 180, 631.
30. Inaba, K., Witmer-Pack, M., Inaba, M., Hathcock, K. S., Sakuta, H., Azuma, M., Yagita, H., Okumura, K., Linsley, P. S., Ikehara, S., Muramatsu, S., Hodes, R. J. & Steinman, R. M. (1994) The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J. Exp. Med. 180, 1849.
31. Jenkins, M. K. (1994) The ups and downs of costimulation. Immunity 1, 443.
32. June, C. H., Bluestone, J. A., Nadler, L. M. & Thompson, C. B. (1994) The B7 and CD28 receptor families. Immunol. Today 15, 321.
33. + T-cells in vivo is dependent on CD28 costimulation and inhibited by CTLA-4. J. Immunol. 155, 1033.
34. Krummel, M. F. & Allison, J. P. (1995) CD28 and CTLA-4 deliver opposing signals which regulate the response of T-cells to stimulation. J. Exp. Med. 182, 459.
35. Krummel, M. F. & Allison, J. P. (1996) CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J. Exp. Med. 183, 2533.
36. Krummel, M. F., Sullivan, T. J. & Allison, J.P. (1996) Superantigen responses and costimulation: CD28 and CTLA-4 have opposing effects on T cell expansion in vitro and in vivo. Int. Immunol. 8, 519.
37. Kuchroo, V. K., Das, M. P., Brown, J. A., Ranger, A. M., Zamvil, S. S., Sobel, R. A., Weiner, H. L., Nabavi, N. & Glimcher, L. H. (1995) B7-1 and B7-2 costimulatory molecules differentially activate the TH1/TH2 developmental pathways: application to autoimmune disease therapy. Cell 80, 707.
38. Lanier, L. L., O'Fallon, S., Somoza, C., Phillips, J. H., Linsley, P. S., Okumura, K., Ito, D. & Azuma, M. (1995) CD80 (B7) and CD86 (B70) provide similar costimulatory signals for T cell proliferation, cytokine production, and generation of CTL. J. Immunol. 154, 97.
39. Leach, D., Krummel, M. & Allison, J. P. (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734.
40. Lenschow, D. J., Zeng, Y., Thistlewaite, J. R., Montag, A., Brady, W., Gibson, M. G., Linsley, P. S. & Bluestone, J. A. (1992) Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4Ig. Science 257, 789.
41. Leung, H. T., Bradshaw, J., Cleaveland, J. S. & Linsley, P. S. (1995) Cytotoxic T lymphocyte-associated molecule-4, a high avidity receptor for CD80 and CD86, contains an intracellular localization motif in its cytoplasmic tail. J. Biol. Chem. 270, 25107.
42. + T cells and induce similar patterns of cytokine secretion in vitro. Int. Immunol. 7, 891.
43. Lindsten, T., Lee, K. P., Harris, E. S., Petryniak, B., Craighead, N., Reynolds, P. J., Lombard, D. B., Freeman, G. J., Nadler, L. M., Gray, G. S., Thompson, C. B. & June, C. H. (1993) Characterization of CTLA-4 structure and expression on human T-cells. J. Immunol. 151, 3489.
44. Linsley, P. S. (1995) Distinct roles for CD28 and Cytotoxic T lymphocyte-associated molecule-4 receptors during T-cell activation. J. Exp. Med. 182, 289.
45. Linsley, P. S. & Ledbetter, J. A. (1993) The role of the CD28 receptor during T cell responses to antigen. Annu. Rev. Immunol. 11, 191.
46. Linsley, P. S., Clark, E. A. & Ledbetter, J. A. (1990) The T-cell antigen, CD28, mediates adhesion with B cells by interacting with the activation antigen, B7/BB-1. Proc. Natl. Acad. Sci. USA 87, 5031.
47. Linsley, P. S., Brady, W., Grosmaire, L., Aruffo, A., Damle, N. K. & Ledbetter, J.A. (1991a) Binding of the B cell activation antigen B7 to CD28 costimulates T-cell proliferation and interleukin 2 mRNA accumulation. J. Exp. Med. 173, 721.
48. Linsley, P. S., Brady, W., Urnes, M., Grosmaire, L. S., Damle, N. K. & Ledbetter, J. A. (1991b) CTLA-4 is a second receptor for the B cell activation antigen B7. J. Exp. Med. 174, 561.
49. Linsley, P. S., Greene, J. L., Tan, P., Bradshaw, J., Ledbetter, J. A., Anasetti, C. & Damle, N. K. (1992a) Coexpression and functional cooperativity of CTLA-4 and CD28 on activated T lymphocytes. J. Exp. Med. 176, 1595.
50. Linsley, P. S., Wallace, P. M., Johnson, J., Gibson, M. G., Greene, J. L., Ledbetter, J. A., Singh, C. & Tepper, M. A. (1992b) Immunosuppression in vivo by a soluble form of the CTLA-4 T cell activation molecule. Science 257, 792.
51. Linsley, P. S., Greene, J. L., Brady, W., Bajorath, J., Ledbetter, J. A. & Peach, R. (1994) Human B7-1 (CD80) and B7-2 (CD86) bind with similar avidities but distinct kinetics to CD28 and CTLA-4-receptors. Immunity 1, 793.
52. Lucas, P. J., Negishi, I., Nakayama, K., Fields, L. E. & Loh, D. Y. (1995) Naive CD28-deficient T-cells can initiate but not sustain an in vitro antigen-specific immune response. J. Immunol. 154, 5757.
53. Mamalaki, C., Norton, T., Tanaka, Y., Townsend, A. R., Chandler, P., Simpson, E. & Kioussis, D. (1992) Thymic depletion and peripheral activation of Class I MHC restricted T-cells by soluble peptide in TcR transgenic mice. Proc. Natl. Acad. Sci. USA 89, 11342.
54. Miller, S. D., Vanderlugt, C. L., Lenschow, D. J., Pope, J. G., Karandikar, N. J., Dal Canto, M. C. & Bluestone, J. A. (1995) Blockade of CD28/B7-1 interaction prevents epitope spreading and clinical relapses of murine EAE. Immunity 3, 739.
55. Mueller, D. L., Jenkins, M. K. & Schwartz, R. H. (1989) Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annu. Rev. Immunol. 7, 445.
56. + helper T-cells. J. Immunol. 156, 1764.
57. Murphy, E. E., Terres, G., Macatonia, S. E., Hsieh, C. S., Mattson, J., Lanier, L. L., Wysocka, M., Trinchieri, G., Murphy, K. & O'Garra, A. (1994) B7 and interleukin-12 cooperate for proliferation and IFN-γ production by mouse Th1 clones that are unresponsive to B7 costimulation. J. Exp. Med. 180, 223.
58. Nagata, S. & Golstein, P. (1995) The Fas death factor. Science 267, 1449.
59. Pages, F., Ragueneau, M., Rottapel, R., Truneh, A., Nunes, J., Imbert, J. & Olive, D. (1994) Binding of phosphatidyl-inositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 369, 327.
60. Pawson, T. (1995) Protein modules and signalling networks. Nature 373, 573.
61. Peach, R. J., Bajorath, J., Brady, W., Leytze, G., Greene, J., Naemura, J. & Linsley, P. S. (1994) Complementarity determining region 1 (CDR1)- and CDR3-analogous regions in CTLA-4 and CD28 determine binding to B7-1. J. Exp. Med. 180, 2049.
62. Prasad, K. V., Cai, Y.C., Raab, M., Duckworth, B., Cantley, L., Shoelson, S. E. & Rudd, C. E. (1994) T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc. Natl. Acad. Sci. USA 91, 2834.
63. Reiser, H., Freeman, G. J., Razi-Wolf, Z., Gimmi, C. D., Benacerraf, B. & Nadler, L. M. (1992) Murine B7 antigen provides an efficient costimulatory signal for activation of murine T lymphocytes via the T-cell receptor/CD3 complex. Proc. Natl. Acad. Sci. USA 89, 271.
64. Schneider, H., Cai, Y. C., Prasad, K. V. S., Shoelson, S. E. & Rudd, C. E. (1995a) T-cell antigen CD28 binds to the GRB-2/SOS complex, regulators of p21ras. Eur. J. Immunol. 25, 1044.
65. Schneider, H., Prasad, V. S., Shoelson, S. E. & Rudd, C. E. (1995b) CTLA-4 binding to the lipid kinase phosphatidylinositol 3-kinase in T cells. J. Exp. Med. 181, 351.
66. Shahinian, A., Pfeffer, K., Lee, K. P., Kundig, T. M., Kishihara, K., Wakeham, A., Kawai, K., Ohashi, P. S. Thompson, C. B. & Mak, T. (1993) Differential T cell costimulatory requirements in CD28-deficient mice. Science 261, 609.
67. Shultz, L. D., Schweitzer, P. A., Rajan, T. V., Yi, T., Ihle, J. N., Matthews, R. J., Thomas, M. L. & Beier, D. R. (1993) Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 73, 1445.
68. Songyang, Z., Shoelson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. G., King, F., Roberts, T., Ratnofsky, S., Lechleider, R. J., Neel, B. G., Birge, R. B., Fajardo, J. E., Chou, M. M., Hanafusa, H., Schaffhausen, B. & Cantley, L. C. (1993) SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767.
69. Stein, P. H., Fraser, J. D. & Weiss, A. (1994) The cytoplasmic domain of CD28 is both necessary and sufficient for costimulation of interleukin-2 secretion and association with phosphatidylinositol 3′-kinase. Mol. Cell. Biol. 14, 3392.
70. Su, B., Jacinto, E., Hibi, M., Kallunki, T., Karin, M. & Ben-Neriah, Y. (1994) JNK is involved in signal integration during costimulation of T lymphocytes. Cell 77, 727.
71. Thomas, M. L. (1995) Of ITAMS and ITIMS: turning on and off the B cell antigen receptor. J. Exp. Med. 181, 1953.
72. Thompson, C. B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456.
73. Tivol, E. A., Borriello, F., Schweitzer, A. N., Lynch, W. P., Bluestone, J. A. & Sharpe, A. H. (1995) Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3, 541.
74. + T-cells by B7-transfected melanoma cells. Science 259, 368.
75. Truitt, K. E., Hicks, C. M. & Imboden, J. B. (1994) Stimulation of CD28 triggers an association between CD28 and phosphatidylinositol 3-kinase in Jurkat T-cells. J. Exp. Med. 179, 1071.
76. Tsui, H. W. S., de Sousa, L. & Tsui, F. W. L. (1993) Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nature Genet. 4, 124.
77. Walunas, T. L., Lenschow, D. J., Bakker, C. Y., Linsley, P. S., Freeman, G. J., Green, J. M., Thompson, C. B. & Bluestone, J. A. (1994) CTLA-4 can function as a negative regulator of T-cell activation. Immunity 1, 405.
78. Ward, S. G., Westwick, J., Hall, N. D. & Sansom, D. M. (1993) Ligation of CD28 receptor by B7 induces formation of D-3 phosphoinositides in T lymphocytes independently of T cell receptor activation. Eur. J. Immunol. 23, 2572.
79. Ward, S. G., Wilson, A., Turner, L., Westwick, J. & Sansom, D. M. (1995) Inhibition of CD28-mediated T cell costimulation by the phosphoinositide 3-kinase inhibitor wortmannin. Eur. J. Immunol. 25, 526.
80. Waterhouse, P., Penninger, J. M., Timms, E., Wakeham, A., Shahinian, A., Lee, K. P., Thompson, C. B., Griesser, H. & Mak, T. W. (1995) Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 270, 985.
81. Zhang, Y. & Allison, J. P. (1996) Identification of a conserved amino acid sequence motif in the CD28 cytoplasmic domain that is required for CD28 signaling. Manuscript submitted.