The complexities of T-Cell Co-stimulation: CD28 and beyond

Immunological Reviews

Volumn , Issue 153, 1996, Pages 155-182

  Sperling, Anne I ^a   Bluestone, Jeffrey A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; ABATACEPT; ANTIBODY CONJUGATE; CD86 ANTIGEN; CD86 PROTEIN, MOUSE; CYTOTOXIC T-LYMPHOCYTE ANTIGEN 4; DIFFERENTIATION ANTIGEN; IMMUNOSUPPRESSIVE AGENT; LEUKOCYTE ANTIGEN; LIGAND; MEMBRANE PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; AUTOIMMUNITY; CELL SURVIVAL; ETIOLOGY; GRAFT REJECTION; HELPER CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE ACTIVATION; ANIMAL; AUTOIMMUNE DISEASE; BIOLOGICAL MODEL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; PROTEIN BINDING; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD28; ANTIGENS, CD80; ANTIGENS, CD86; ANTIGENS, DIFFERENTIATION; AUTOIMMUNE DISEASES; GRAFT REJECTION; IMMUNOCONJUGATES; IMMUNOSUPPRESSIVE AGENTS; LIGANDS; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MODELS, IMMUNOLOGICAL; PROTEIN BINDING; T-LYMPHOCYTES;

EID: 0030300154     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065x.1996.tb00924.x     Document Type: Review

References (93)

1. Azuma, M., Ito, D., Yagita, H., Okumura, K., Phillips, J. H., Lanier, L. L. & Somoza, C. (1993) B70 antigen is a second ligand for CTLA-4 and CD28. Nature 366, 76.
2. Balzano, C., Buonavista, N., Rouvier, E. & Golstein, P. (1992) CTLA-4 and CD28: similar proteins, neighboring genes. Int. J. Cancer Suppl. 7, 28.
3. 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. U. S. A. 90, 5687.
4. + T cells. J. Exp. Med. 166, 823.
5. L. Immunity 3, 87.
6. Boussiotis, V. A., Freeman, G. J., Gribben, J. G., Daley, J., Gray, G. & Nadler, L. M. (1993) Activated human B lymphocytes express three CTLA-4 counterreceptors that costimulate T-cell activation. Proc. Natl. Acad. Sci. U. S. A. 90, 11059.
7. Bretscher, P. & Cohn, M. (1970) A theory of self-nonself discrimination. Science 169, 1042.
8. Brunet, J. F., Denizot, F., Luciani, M. F., Roux-Dosseto, M., Suzan, M., Mattei, M. G. & Golstein, P. (1987) A new member of the immunoglobulin superfamily - CTLA-4. Nature 328, 267.
9. Corry, D. B., Reiner, S. L., Linsley, P. S. & Locksley, R. M. (1994) Differential effects of blockade of CD28-B7 on the development of Th1 or Th2 effector cells in experimental leishmaniasis. J. Immunol. 153, 4142.
10. + T lymphocytes. J. Immunol. 148, 1985.
11. Debray-Sachs, M., Carnaud, C., Boitard, C., Cohen, H., Gresser, I., Bedossa, P. & Bach, J. F. (1991) Prevention of diabetes in NOD mice treated with antibody to murine IFN gamma. J. Autoimmun. 4, 237.
12. + thymocytes. J. Immunol. 152, 3254.
13. Dent, A. L., Matis, L. A., Hooshmand, F. H., Widacki, S. M., Bluestone, J. A. & Hedrick, S. M. (1990) Self-reactive γδ T cells are eliminated in the thymus. Nature 343, 714.
14. Ferguson, S. E., Han, S., Kelsoe, G. & Thompson, C. B. (1996) CD28 is required for germinal center formation. J. Immunol. (in press).
15. Finck, B. K., Linsley, P. S. & Wofsy, D. (1994) Treatment of murine lupus with CTLA4Ig. Science 265, 1225.
16. Fraser, J. D., Irving, B. A., Crabtree, G. R. & Weiss, A. (1991) Regulation of interleukin-2 gene enhancer activity by the T cell accessory molecule CD28. Science 251, 313.
17. Freeman, G. J., Borriello, F., Hodes, R. J., Reiser, H., Gribben, J. G., Ng, J. W., Kim, J., Goldberg, J. M., Hathcock, K., Laszlo, G., Lombard, L. A., Wang, S., Gray, G. S., Nadler, L. M. & Sharpe, A. H. (1993a) Murine B7-2, an alternative CTLA-4 counter-receptor that costimulates T cell proliferation and interleukin-2 production. J. Exp. Med. 178, 2185.
18. Freeman, G. J., Borriello, F., Hodes, R. J., Reiser, H., Hathcock, K. S., Laszlo, G., McKnight, A. J., Kim, J., Du, L., Lombard, D. B., Gray, G. S., Nadler, L. M. & Sharpe, A. H. (1993b) Uncovering of functional alternative CTLA-4 counter-receptor in B7-deficient mice. Science 262, 907.
19. 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.
20. Freeman, G. J., Gribben, J. G., Boussiotis, V. A., Ng, J. W., Restivo, V. A., Jr, Lombard, L. A., Gray, G. S. & Nadler, L. M. (1993c) Cloning of B7-2: a CTLA-4 counter-receptor that costimulates human T cell proliferation. Science 262, 909.
21. Gelber, C., Paborsky, L., Singer, S., McAteer, D., Tisch, R., Jolicoeur, C., Buelow, R., McDevitt, H. & Fathman, C. G. (1994) Isolation of nonobese diabetic mouse T-cells that recognize novel autoantigens involved in the early events of diabetes. Diabetes 43, 33.
22. 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.
23. Guerder, S., Meyerhoff, J. & Flavell, R. (1994a) The role of the T cell costimulator B7-1 in autoimmunity and the induction and maintenance of tolerance to peripheral antigen. Immunity 1, 155.
24. Guerder, S., Picarella, D. E., Linsley, P. S. & Flavell, R. A. (1994b) Costimulator B7-1 confers antigen-presenting-cell function to parenchymal tissue and in conjunction with tumor necrosis factor alpha leads to autoimmunity in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 91, 5138.
25. Han, S., Hathcock, K., Zheng, B., Kepler, T. B., Hodes, R. & Kelsoe, G. (1995) Cellular interaction in germinal centers: roles of CD40 ligand and B7-2 in established germinal centers. J. Immunol. 155, 556.
26. Harding, F. A., McArthur, J. G., Gross, J. A., Raulet, D. H. & Allison, J. P. (1992) CD28-mediated signaling co-stimulates murine T cells and prevents induction of anergy in T cell clones. Nature 356, 607.
27. Harlan, D. M., Hengartner, H., Huang, M. L., Kang, Y. H., Abe, R., Moreadith, R. W., Pircher, H., Gray, G. S., Ohashi, P. S. & Freeman, G. J. (1994) Mice expressing both B7-1 and viral glycoprotein on pancreatic beta cells along with glycoprotein-specific transgenic T cells develop diabetes due to a breakdown of T-lymphocyte unresponsiveness. Proc. Natl. Acad. Sci. U. S. A. 91, 3137.
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. Jenkins, M. K., Mueller, D., Schwartz, R. H., Carding, S., Bottomley, K., Stadecker, M. J., Urdahl, K. B. & Norton, S. D. (1991a) Induction and maintenance of anergy in mature T cells. Adv. Exp. Med. Biol. 292, 167.
31. Jenkins, M. K., Taylor, P. S., Norton, S. D. & Urdahl, K. B. (1991b) CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J. Immunol. 147, 2461.
32. Jones, L. A., Izon, D. J., Nieland, J. D., Linsley, P. S. & Kruisbeek, A. M. (1993) CD28-B7 interactions are not required for intrathymic clonal deletion. Int. Immunol. 5, 503.
33. Karandikar, N. J., Vanderlugt, C. L., Walunas, T. L., Miller, S. D. & Bluestone, J. A. (1996) CTLA-4: a negative regulator of autoimmune disease. J. Exp. Med. 184 (in press).
34. Kawai, K., Shahinian, A., Mak, T. W. & Ohashi, P. S. (1996) Skin allograft rejection in CD28-deficient mice. Transplantation 61, 352.
35. Kearney, E. R., Walunas, T. L., Karr, R. W., Morton, P. A., Loh, D. Y., Bluestone, J. A. & Jenkins, M. K. (1995) Antigen-dependent clonal expansion of a trace population of antigen-specific CD4+ T cells in vivo is dependent on CD28 costimulation and inhibited by CTLA-4. J. Immunol. 155, 1032.
36. 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 activate differentially the Th1/Th2 developmental pathways: application to autoimmune disease therapy. Cell 80, 707.
37. Lafferty, K. J. & Gill, R. G. (1993) The maintenance of self-tolerance. Immunol. Cell Biol. 71, 209.
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. Larsen, C. P., Ritchie, S. C., Pearson, T. C., Linsley, P. S. & Lowry, R. P. (1992) Functional expression of the costimulatory molecule, B7/BB1, on murine dendritic cell populations. J. Exp. Med. 176, 1215.
40. Leach, D.R., Krummel, M. F. & Allison, J. P (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734.
41. Lenschow, D. J., Zeng, Y., Thistlethwaite, 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.
42. Lenschow, D. J., Su, G. H.-T., Zuckerman, L. A., Nabavi, N., Jellis, C. L., Gray, G. S., Miller, J. & Bluestone, J. A. (1993) Expression and functional significance of an additional ligand for CTLA-4. Proc. Natl. Acad. Sci. U. S. A. 90, 11054.
43. Lenschow, D. J., Sperling, A. I., Cooke, M. P., Freeman, G., Rhee, L., Decker, D. C., Gray, G., Nadler, L. M., Goodnow, C. C. & Bluestone, J. A. (1994) Differential up-regulation of the B7-1 and B7-2 costimulatory molecules after Ig receptor engagement by antigen. J. Immunol. 153, 1990.
44. Lenschow, D. J., Ho, S. C., Sattar, H., Rhee, L., Gray, G., Nabavi, N., Herold, K. C. & Bluestone, J. A. (1995a) Differential effects of anti-B7-1 and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J. Exp. Med. 181, 1145.
45. Lenschow, D. J., Zeng, Y., Hathcock, K. S., Zuckerman, L. A., Freeman, G., Thistlethwaite, J. R., Gray, G. S., Hodes, R. J. & Bluestone, J. A. (1995b) Inhibition of transplant rejection following treatment with anti-B7-2 and anti-B7-1 antibodies. Transplantation 60, 1711.
46. Lenschow, D. J., Walunas, T. L. & Bluestone, J. A. (1996a) CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14, 233.
47. Lenschow, D., Herold, K., Rhee, L., Patel, B., Koons, A., Qin, H.-Y., Fuchs, E., Singh, B., Thompson, C. B. & Bluestone, J. A. (1996b) CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity 5, 285.
48. 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.
49. Levine, B. L., Ueda, Y., Craighead, N., Huang, M. L. & June, C. H. (1995) CD28 ligands CD80 (B7-1) and CD86 (B7-2) induce long term autocrine growth of CD4+ T cells and induce similar patterns of cytokine secretion in vitro. Int. Immunol. (in press).
50. Lin, H., Boiling, S. F., Linsley, P. S., Wei, R.-Q., Gordon, D., Thompson, C. B. & Turka, L. A. (1993) Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4Ig plus donor-specific transfusion. J. Exp. Med. 178, 1801.
51. Lindsten, T., June, C. H., Ledbetter, J. A., Stella, G. & Thompson, C. B. (1989) Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244, 339.
52. Lindsten, T., Lee, K. P., Harris E. S., Petryniak, B., Craighead, N., Reynolds, P. J., Lombard, B. D., 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.
53. Linsley, P. S., Brady, W., Urnes, M., Grosmaire, L. S., Damle, N. K. & Ledbetter, J. A. (1991) CTLA-4 is a second receptor for the B-cell activation antigen B7. J. Exp. Med. 174, 561.
54. Linsley, P. S., Clark, E. A. & Ledbetter, J. A. (1990) T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1. Proc. Natl. Acad. Sci. U. S. A. 87, 5031.
55. Linsley, P. S., Greene, J. L., Tan, P., Bradshaw, J., Ledbetter, J. A., Anasetti, C. & Damle, N. K. (1992a) Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. J. Exp. Med. 176, 1595.
56. Linsley, P. S., Wallace, P. M., Johnson, J., Gibson, M. G., Greene, J., 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.
57. Liu, Y., Jones, B., Aruffo, A., Sullivan, K. M., Linsley, P. S. & Janeway, C. A., Jr. (1992) Heat-stable antigen is a costimulatory molecule for CD4 T cell growth. J. Exp. Med. 175, 437.
58. Lu, P., di Zhou, X., Chen, S.-J., Moorman, M., Morris, S. C., Finkelman, F. D., Linsley, P., Urban, J. F. & Gause, W. C. (1994) CTLA-4 ligands are required to induce an in vivo interleukin 4 response to a gastrointestinal nematode parasite. J. E.xp. Med. 180, 693.
59. + T lymphocytes from TCR transgenic mice. J. Immunol. 152, 5220.
60. McRae, B. L., Kennedy, M. K., Tan, L. J., Dal Canto, M. C., Pich, K. S. & Miller, S. D. (1992) Induction of active and adoptive relapsing experimental autoimmune encephalomyelitis (EAE) using an encephalitogenic epitope of proteolipid protein. J. Neuroimmunol. 38, 229.
61. Migliorati, G., Nicoletti, I., Pagliacci, M. C., D''Adamio, L. & Riccardi, C. (1993) IL-4 protects double-negative and CD4 single-positive thymocytes from dexamethasone-induced apoptosis. Blood 81, 1352.
62. Miller, S. D., McRae, B. L., Vanderlugt, C. L., Nikcevich, K. M., Pope, J. G., Pope, L. & Karpus, W. J. (1995a) Evolution of the T-cell repertoire during the course of experimental immunemediated demyelinating diseases. Immunol. Rev. 144, 225.
63. Miller, S. D., Vanderlugt, C. L., Lenschow, D. J., Dal Canto, M. C. & Bluestone, J. A. (1995b) Blockade of CD28/B7-1 interaction prevents epitope spreading and clinical relapses of murine EAE. Immunity 3, 739.
64. Murohy, K. M., Weaver, C. T., Elish, M., Allen, P. M. & Loh, D. Y. (1989) Peripheral tolerance to allogeneic class II histocompatibility antigens expressed in transgenic mice: evidence against a clonal-deletion mechanism. Proc. Natl. Acad. Sci. U. S. A. 86, 10034.
65. Naujokas, M. F., Morin, M., Anderson, M. S., Peterson, M. & Miller, J. (1993) The chondroitin sulfate form of invariant chain can enhance stimulation of T cell responses through interaction with CD44. Cell 74, 257.
66. Nelson, A. J., Hosier, S., Brady, W., Linsley, P. S. & Farr, A. G. (1993) Medullary thymic epithelium expresses a ligand for CTLA4 in situ and in vitro. J. Immunol. 151, 2453.
67. + thymocytes. J. Immunol. 151, 1868.
68. Pawlowski, T., Elliot, J. D., Loh, D. Y. & Staerz, U. D. (1993) Positive selection of T lymphocytes on fibroblasts. Nature 364, 642.
69. 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 the binding to B7-1. J. Exp. Med. 180, 2049.
70. Perrin, P. J., Scott, D., Quigley, L., Albert, P. S., Feder, O., Gray, G. S., Abe, R., June, C. H. & Racke, M. K. (1995) Role of B7:CD28/CTLA-4 in the induction of chronic relapsing experimental allergic encephalomyelitis. J. Immunol. 154, 1481.
71. Prabhu Das, M. R., Zamvil, S. S., Borriello, F., Weiner, H. L., Sharpe, A. H. & Kuchroo, V.K. (1995) Reciprocal expression of co-stimulatory molecules, B7-1 and B7-2, on murine T cells following activation. Eur. J. Immunol. 25, 207.
72. Punt, J. A., Osborne, B. A., Takahama, Y., Sharrow, S. O. & Singer, A. (1994) Negative selection of CD4+CD8+ thymocytes by T cell receptor-induced apoptosis requires a costimulatory signal that can be provided by CD28. J. Exp. Med. 179, 709.
73. Ramarathinam, L., Castle, M., Wu, Y. & Liu, Y. (1994) T cell costimulation by B7/BB1 induces CD8 T cell-dependent tumor rejection: an important role of B7/BB 1 in the induction, recruitment, and effector function of antitumor T cells. J. Exp. Med. 179, 1205.
74. Rapoport, M. J., Jararmillo, A., Zipris, D., Lazarus, A. H., Serreze, D. V., Leiter, E. H., Cyopick, P., Danska, J. S. & Delovitch, T.L. (1993) Interleukin 4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice. J. Exp. Med. 178, 87.
75. Rulifson, I. C., Sperling, A. I., Fields, P. E., Fitch, F. W. & Bluestone, J. A. (1997) CD28 costimulation promotes the production of Th2 cytokines. J. Immunol. (in press).
76. Sayegh, M. H., Akalin, E., Hancock, W. W., Russell, M. E., Carpenter, C. B., Linsley, P. S. & Turka, L.A. (1995) CD28-B7 blockade after alloantigenic challenge in vivo inhibits Th1 cytokines but spares Th2. J. Exp. Med. 181, 1869.
77. Seder, R. A., Germain, R. N., Linsley, P. S. & Paul, W. E. (1994) CD28-mediated costimulation of interleukin 2 (IL-2) production plays a critical role in T cell priming for IL-4 and interferon gamma production. J. Exp. Med. 179, 299.
78. Serreze, D. V. & Leiter, E. H. (1994) Genetic and pathogenic basis of autoimmune diabetes in NOD mice. Curr. Opin. Immunol. 6, 900.
79. Sethna, M. P., van Parijs, L., Sharpe, A. H., Abbas, A. K. & Freeman, G. J. (1994) A negative reculatory function of B7 revealed in B7-1 transgenic mice. Immunity. 1, 415.
80. Sha, W. C., Nelson, C. A., Newberry, R. D., Kranz, D. M., Russell, J. H. & Loh, D. Y. (1988) Selective expression of an antigen receptor on CD8-bearing T lymphocytes in transgenic mice. Nature 335, 271.
81. Shahinian, A., Pfeffer, K., Lee, K. P., Kundig, T. M., Kishihara, K., Wakeham, A., Kawai, K., Ohashi, P. S., Thompson, C. B. & Mak, T. W. (1993) Differential T cell costimulatory requirements in CD28-deficient mice. Science 261, 609.
82. Shehadeh, N. N., LaRosa, F. & Lafferty, K. J. (1993) Altered cytokine activity in adjuvant inhibition of autoimmune diabetes. J. Autoimmun. 6, 291.
83. Sperling, A. I., Green, J. M., Mosley, R. L., Smith, P. L., DiPaolo, R. J., Klein, J. R., Bluestone. J. A. & Thompson, C. B. (1995) CD43 is a murine T cell costimulatory receptor that functions independently of CD28. J. Exp. Med. 182, 139.
84. Sperling, A. I., Auger, J. A., Ehst, B. D., Rulifson, I. C., Thompson, C. B. & Bluestone, J. A. (1996) CD28/B7 interactions deliver a unique signal to naive T cells that regulates cell survival but not early proliferation. J. Immunol. 157, 3909.
85. Tivol, E. A., Borriello, F., Schwetzer, 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.
86. Townsend, S. E., Su, F.W., Atherton, J. M. & Allison, J. P. (1994) Specificity and longevity of antitumor immune responses induced by B7-transfected tumors. Cancer Res. 54, 6477.
87. Trembleau, S., Penna, G., Bosi, E., Mortara, A., Gately, M. K. & Adorini, L. (1995) Interleuin 12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J. Exp. Med. 181, 817.
88. Vukmanovic, S., Stella, G., King, P. D., Dyall, R., Hogquist, K. A., Harty, J. T., Nikolic-Zugic, J. & Bevan, M. J. (1994) A positively selecting thymic epithelial cell line lacks costimulatory activity. J. Immunol. 152, 3814.
89. Walunas, T. L., Bakker, C. Y. & Bluestone, J. A. (1996) CTLA-4 ligation blocks CD28-dependent T cell activation. J. Exp. Med. (in press).
90. 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.
91. Walunas, T. L., Sperling, A. I., Khattri, R., Thompson, C. B. & Bluestone, J. A. (1995) CD28 expression is not essential for positive and negative selection of thymocytes or peripheral T cell tolerance. J. Immunol. 156, 1006.
92. Windhagen, A., Newcombe, J., Dangond, F., Strand, C., Woodroofe, M. N., Cuzner, M. L. & Hafler, D. A. (1996) Expression of costimulatory molecules B7-1(CD80), B7-2(CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J. Exp. Med. 182, 1985.
93. Zubiaga, A. M., Munoz, E. & Huber, B. T. (1992) IL-4 and IL-2 selectively rescue The cell subsets from glucocorticoid-induced apoptosis. J. Immunol. 149, 107.