Title: The Complexities of T‐Cell Co‐stimulation: CD28 and Beyond
Abstract: Immunological ReviewsVolume 153, Issue 1 p. 155-182 The Complexities of T-Cell Co-stimulation: CD28 and Beyond Anne I. Sperling, Anne I. Sperling Ben May Institute for Cancer Research, Department of Pathology and the Committee on Immunology, University of Chicago, Chicago, Illinois, USA.Search for more papers by this authorJeffrey A. Bluestone, Corresponding Author Jeffrey A. Bluestone Ben May Institute for Cancer Research, Department of Pathology and the Committee on Immunology, University of Chicago, Chicago, Illinois, USA.Dr Jeffrey Bluestone, Charles B. Huggins Professor, Ben May Insitute for Cancer Research, MC 1089, University of Chicago, 5841 S. Maryland Ave., Chicago, IL 60637, USA.Search for more papers by this author Anne I. Sperling, Anne I. Sperling Ben May Institute for Cancer Research, Department of Pathology and the Committee on Immunology, University of Chicago, Chicago, Illinois, USA.Search for more papers by this authorJeffrey A. Bluestone, Corresponding Author Jeffrey A. Bluestone Ben May Institute for Cancer Research, Department of Pathology and the Committee on Immunology, University of Chicago, Chicago, Illinois, USA.Dr Jeffrey Bluestone, Charles B. Huggins Professor, Ben May Insitute for Cancer Research, MC 1089, University of Chicago, 5841 S. Maryland Ave., Chicago, IL 60637, USA.Search for more papers by this author First published: October 1996 https://doi.org/10.1111/j.1600-065X.1996.tb00924.xCitations: 126Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat REFERENCES 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. Balzano, C., Buonavista, N., Rouvier, E. & Golstein, P. (1992) CTLA-4 and CD28: similar proteins, neighboring genes. Int. J. Cancer Suppl. 7, 28. 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. Bendelac, A., Carnaud, C., Boitard, C. & Bach, J. F.(1987) Syngeneic transfer of autoimmune diabetes from diabetic NOD mice to healthy neonates. Requirement for both L3T4+ and Lyt-2+ T cells, J. Exp. Med 166, 823. Boise, L. H., Minn, A. J., Noel, P. J., June, C. H., Accavitti, M., Lindsten, T & Thompson, C. B. (1995) CD28 costimulation can promote T cell survival by enhancing the expression of BC1-XL. Immunity 3, 87. Boussiotis, Y. 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. Bretscher, P & Cohn, M. (1970) A theory of self-nonself discrimination. Science 169, 1042. 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. Corry, D. B., Reiner, S. L., Linsley, P. S. & Locksley, R. M. (1994) Differential effects of blockade of CD28-B7 on the development of Thl or Th2 effector cells in experimental leish-maniasis. Immunol. 153, 4142. Damle, N.K., Klussman, K., Linsley, P & Aruffo, A. (1992) Differential costimulatory effects of adhesion molecules B7, ICAM-1,LFA-3 and VCAM-1 on resting and antigen-primed CD4+ T lymphocytes, J. Immunol. 148, 1985. 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. Degermann, S., Surh, C. D, Glimcher, L. H., Sprent, J. & Lo, D (1996) B7 expression on thymic medullary epithelium correlates with epithelium-mediated deletion of V-beta 5+ thymocytes. J. Immunol. 152, 3254. Dent, A. L., Matis, L. A., Hooshmand, F. H., Widacki, S. M., Bluestone, J. A. & Hedrick, S. M. (1990) Self-reactive βδ T cells are eliminated in the thymus. Nature. 343, 714. Ferguson, S. E., Han, S., Kelsoe, G. & Thompson, C. B. (1996) CD28 is required for germinal center formation. J. Immunol.(in press). Finck, B. K., Linsley, P. S. & Wofsy, D. (1994) Treatment of murine lupus with CTLA4Ig. Science 265, 1225. 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. 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. Freeman, G. J., Borriello, F., Hodes, R. J., Reiser, H., Hathcock, K. S., Lasziol, 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. 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. 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. Gelber, C., Paborsky, L., Singer, S., McAteer, D., Tisch, R., Jolicoeur, C., Buelow, R., McDev-itt, 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. 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. 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. Guerder, S., Picarella, D. E., Linsley, P. S. & Flavell, R. A. (1994b) Costimulator B7-1 confers antigen-presenting-cell function to parcnchymal tissue and in conjunction with tumor necrosis factor alpha leads to autoimmunity in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 91, 5138. 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. 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. 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-lympbocyte unresponsiveness. Proc. Natl. Acad. Sci. U. S. A. 91, 3137. 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. Hathcock, K. S., Laszlo, G., Pucillo, C., Linsley, P & Hodes, R. J. (1994) Comparative analysis ofB7-l and B7-2 costimulatory ligands: expression and function. J. Exp. Med. 180, 631. 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. Bioi. 292, 167. 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. 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. 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). Kawai, K., Shahinian, A., Mak, T. W & Ohashi, P. S. (1996) Skin allograft rejection in CD28-deficient mice. Transplantation 61, 352. 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. 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 Thl/Th2 developmental pathways: application to autoimmune disease therapy. Cell 80, 707. Lafferty, K. J. & Gill, R. G. (1993) The maintenance of self-tolerance. Immunol. Cell Biol. 71, 209. Lanier, L. L., Öfallon, 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. 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. Leach, D.R., Krummel, M. F. & Allison, J. P. (1996) Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734. Lenschow, D. J., Zeng, Y., Thistietbwaite, 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 CrLA4Ig. Science 257, 789. Lenscbow, 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. 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. Lenschow, D. J., Ho, S. C., Sattar, H., Rhee, L., Gray, G., Nabavi, N., Herold, K. C. & Blue-stone, J. A. (1995a) Differential effects of anti-B7-I and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J. Exp. Med. 181, 1145. 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. Lenschow, D. J., Walunas, T. L. & Bluestone, J. A. (1996a) CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14, 233. 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 Thl and Th2 subsets in the development of autoimmune diabetes. Immunity 5, 285. 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 intra-cellular localization motif in its cytoplasmic tail. J. Biol. Chem. 270, 25107. 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 vivo. Int. Immunol. (in press). 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. 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. Lindsten, T., Lee, K. P., Harris E. S., Petryniak, B., Craighead, N., Reynolds, P. J., Lombard, B. U, 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. 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. 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. 87, 5031. 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. 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. 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. 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. Exp. Med. 180, 693. McKnight, A. J., Perez, V. L., Shea, C. M., Gray, G. S. & Abbas, A.K. (1994) Costimulator dependence of lymphokine secretion by naive and activated CD4+ T lymphocytes from TCR transgenic mice. J. Immunol. 152, 5220. 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. 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. 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. 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. 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. Naujokas, M. E, 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. 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. Page, D. M., Kane, L. P, Allison, J. P & Hedrick, S. M. (1993) Two signals are required for negative selection of CD4+ CD8+ thymocytes. J. Immunol. 151, 1868. Pawlowski, T. Elliot, J. D., Loh, D. Y. & Staerz, U. D. (1993) Positive selection of T lymphocytes on fibroblasts. Nature 364, 642. Peach, R. J., Bajorath, J., Brady, W., Leytze, G., Greene, J., Naemura, J. & Linsley, P.S. (1994) Complementarity determining region 1 (CDRl)- and CDR3-analogous regions in CTLA-4 and CD28 determine the binding to B7-1. J. Exp. Med 180, 2049. 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. Prabhu Das, M. R., Zamvil, S.S., Borriello, F., Weiner, H. L., Sharpe, A. H. & Kuchroo, VK. (1995) Reciprocal expression of co-stimulatory molecules, B7-1 and B7-2, on murine T cells following activation. Eur. J. Immunol. 25, 207. 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. 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. Rapoport, M. J., Jaramillo, 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. Rulifson, I.C. Sperling, A. I., Fieids, P.E., Fitch, F. W. & Bluestone, J. A. (1997) CD28 costimulation promotes the production of Th2 cytokines. J. Immunol. (in press). 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. 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. Serreze, D. V. & Leiter, E. H. (1994) Genetic and pathogenic basis of autoimmune diabetes in NOD mice. Curr. Opin. Immunol. 6, 900. 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. 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. 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. Shehadeh, N. N., LaRosa, F. & Lafferty, K. J. (1993) Altered cytokine activity in adjuvant inhibition of autoimmune diabetes. J. Autoimmun. 6, 291. 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. Sperling, A. L, Auger, J. A., Ehst, B. D, Rulifson, L. 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. 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. Townsend, S. E., Su, F.W., Atherton, J. M. & Allison, J. P (1994) Specificity and longevity of anti tumor immune responses induced by B7-transfected tumors. Cancer Res. 54, 6477. Trembleau, S., Penna, G., Bosi, E., Mortara, A., Gately, M. K. & Adorini, L. (1995) Interleukin 12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J. Exp. Med. 181, 817. 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. Immunol. 152, 3814. Walunas, T. L., Bakker, C. Y. & Bluestone, J. A. (1996) CTLA-4 ligation blocks CD28-dependent T cell activation. J. Exp. Med.,(in press). 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) CrLA-4 can function as a negative regulator of T cell activation. Immunity 1, 405. 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. Windhagen, A., Newcombe, J., Dangond, F., Strand, C., Woodroofe, M. N., Cuzner, M. L. & Hafler, D. A. (1996) Expression of costimulatory molecules B7-I(CD80), B7-2(CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J. Exp. Med. 182, 1985. 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. Citing Literature Volume153, Issue1October 1996Pages 155-182 ReferencesRelatedInformation
Publication Year: 1996
Publication Date: 1996-10-01
Language: en
Type: review
Indexed In: ['crossref', 'pubmed']
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