Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-γ but not TH2 cytokines

Nature Immunology

Volumn 2, Issue 1, 2001, Pages 37-44

  Kane, Lawrence P ^a   Andres, Pietro G ^b   Howland, Kimberly C ^a   Abbas, Abul K ^a   Weiss, Arthur ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT1 PROTEIN, HUMAN; CD28 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 2; LYMPHOCYTE ANTIGEN RECEPTOR; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL LINE; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; MOUSE MUTANT; PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH2 CELL; TRANSGENIC MOUSE; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD28; CELL LINE; CYTOKINES; HUMANS; INTERFERON TYPE II; INTERLEUKIN-2; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TH2 CELLS; UP-REGULATION;

EID: 0035221568     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/83144     Document Type: Article

References (75)

1. Lenschow, D. J., Walunas, T. L. & Bluestone, J. A. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14, 233-258 (1996).
2. Noel, P. J., Boise, L. H. & Thompson, C. B. Regulation of T cell activation by CD28 and CTLA4. Adv. Exp. Med. Biol. 406, 209-217 (1996).
3. Howland, K. C., Ausubel, L. J., London, C. A. & Abbas, A. K. The roles of CD28 and CD40 ligand in T cell activation and tolerance. J. Immunol. 164, 4465-4470 (2000).
4. King, C. L., Xianli, J., June, C. H., Abe, R. & Lee, K. P. CD28-deficient mice generate an impaired Th2 response to Schistosoma mansoni infection. Eur. J. Immunol. 26, 2448-2455 (1996).
5. Villegas, E. N., Elloso, M. M., Reichmann, G., Peach, R. & Hunter, C. A. Role of CD28 in the generation of effector and memory responses required for resistance to Toxoplasma gondii. J. Immunol. 163, 3344-3353 (1999).
6. Dahl, A. M. et al. Expression of Bcl-XL restores cell survival, but not proliferation and effector differentiation, in CD28-deficient T lymphocytes. J. Exp. Med. 191, 2031-2038 (2000).
7. Lucas, P. J., Negishi, I., Nakayama, K., Fields, L. E. & Loh, D.Y. Naive CD28-deficient T cells can initiate but not sustain an in vitro antigen-specific immune response. J. Immunol. 154, 5757-5768 (1995).
8. Shahinian, A. et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science 261, 609-612 (1993).
9. Wülfing, C. & Davis, M. M. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282, 2266-2269 (1998).
10. Ward, S. G. CD28: a signaling perspective. Biochem J. 318, 361-377 (1996).
11. Viola, A., Schroeder, S., Sakakibara, Y. & Lanzavecchia, A.T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283, 680-682 (1999).
12. Shapiro, V. S., Truitt, K. E., Imboden, J. B. & Weiss, A. CD28 mediates transcriptional upregulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF-1L-2B AP-1 sites. Mol. Cell Biol. 17, 4051-4058 (1997).
13. Hutchcroft, J. E. & Bierer, B. E. Signaling through CD28/CTLA-4 family receptors. J. Immunol. 156, 4071-4074 (1996).
14. June, C. H., Bluestone, J. A., Nadler, L. M. & Thompson, C. B. The B7 and CD28 receptor families. Immunol. Today 15, 321-331 (1994).
15. Crabtree, G. R. & Clipstone, N. A. Signal transduction between the plasma membrane and nuclues of T lymphocytes. Annu. Rev. Biochem. 63, 1045-1083 (1994).
16. Jain, J., Loh, C. & Rao, A. Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol. 7, 333-342 (1995).
17. Civil, A., Geerts, M., Aarden, L. A. & Verweij, C. L. Evidence for a role of CD28RE as a response element for distinct mitogenic T cell activation signals. Eur. J. Immunol. 22, 3041-3043 (1992).
18. Fraser, J. D., Irving, B. A., Crabtree, G. R. & Weiss, A. Regulation of Interleukin-2 gene enhancer activity by the T cell accessory molecule CD28. Science 251, 313-316 (1991).
19. McGuire, K. L. & Iacobelli, M. Involvement of Rel, Fos, and Jun proteins in binding activity to the IL-2 promoter CD28 element/AP-1 sequence in human T cells. J. Immunol. 159, 1319-1327 (1997).
20. Verweij, C. L., Geerts, M. & Aarden, L. A. Activation of interleukin-2 gene transcription via the T-cell surface molecule CD28 is mediated through an NF-κB-like response element. J. Biol. Chem. 266, 14179-14182 (1991).
21. Butscher, W. G., Powers, C., Olive, M., Vinson, C. & Gardner, K. Coordinate transactivation of the interleukin-2 CD28 response element by c-Rel and ATF-1/CREB2. J. Biol. Chem. 273, 552-560 (1998).
22. Curtiss, V. E., Smilde, R. & McGuire, K. L. Requirements for interleukin 2 promoter transactivation by the Tax protein of human T-cell leukemia virus type I. Mol. Cell Biol. 16, 3567-3575 (1996).
23. Fraser, J. D. & Weiss, A. Regulation of T-cell lymphokine gene transcription by the accessory molecule CD28. Mol. Cell Biol. 12, 4357-4363 (1992).
24. Cerdan, C. et al. Prolonged IL-2 receptor α/CD25 expression after T cell activation via the adhesion molecules CD2 and CD28. J. Immunol. 149, 2255-2261 (1992).
25. Thompson, C. B. et al. CD28 activation pathway regulates the production of multiple T-cell-derived lymphokines/cytokines. Proc. Natl. Acad. Sci. USA 86, 1333-1337 (1989).
26. Wechsler, A. S., Gordon, M. C., Dendorfer, U. & LeClair, K. P. Induction of IL-8 expression in T cells uses the CD28 costimulatory pathway. J. Immunol. 153, 2515-2523 (1994).
27. Ghosh, P., Tan, T.-H., Rice, N. R., Sica, A. & Young, H. A. The interleukin 2 CD28-responsive complex contains at least three members of the NF-κB family: c-Rel, p50, and p65. Proc. Natl Acad. Sci. USA 90, 1696-1700 (1993).
28. Maggirwar, S. B., Harhaj, E. W. & Sun, S.-C. Regulation of the interleukin-2 CD28-responsive element by NF-ATp and various NF-κB/Rel transcription factors. Mol. Cell Biol. 17, 2605-2614 (1997).
29. Bryan, R. G. et al. Effect of CD28 signal transduction on c-Rel in human peripheral blood T cells. Mol. Cell Biol. 14, 7933-7942 (1994).
30. Lai, J.-H. & Tan, T.-H. CD28 signaling causes a sustained down-regulation of IκBα which can be prevented by the immunosuppressant rapamycin. J. Biol. Chem. 269, 30077-30080 (1994).
31. Kontgen, F. et al. Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Dev. 9, 1965-1977 (1995).
32. Parry, R.V. et al. Ligation of the T cell co-stimulatory receptor CD28 activates the serine-threonine protein kinase protein kinase B. Eur J. Immunol. 27, 2495-2501 (1997).
33. Fruman, D.A. et al. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 283, 393-397 (1999).
34. Ueda, Y. et al. Both CD28 ligands CD80 (B7-2) and CD86 (B7-2) activate phosphatidylinositol 3-kinase, and wortmannin reveals heterogeneity in the regulation of T cell IL-2 secretion. Int. Immunol. 7, 957-966 (1995).
35. Kane, L. P., Shapiro, V. S. S., Stokoe, D. & Weiss, A. Induction of NF-κB by the Akt/PKB kinase. Curr. Biol. 9, 601-604 (1999).
36. Jones, R. G. et al. Protein Kinase B Regulates T Lymphocyte Survival, Nuclear Factor κB Activation, and Bcl-X(L) Levels In vivo. J. Exp. Med. 191, 1721-1734 (2000).
37. Eder, A. M., Dominguez, L., Franke, T. F. & Ashwell, J. D. Phosphoinositide 3-kinase regulation of T cell receptor-mediated interleukin-2 gene expression in normal T cells. J. Biol. Chem. 273, 28025-28031 (1998).
38. Vanhaesebroeck, B. & Alessi, D. R. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346, 561-576 (2000).
39. Manger, B., Weiss, A., Imboden, J., Laing, T. & Stobo, J. D. The role of protein kinase C in transmembrane signaling by the T cell antigen receptor complex. Effects of stimulation with soluble or immobilized CD3 antibodies. J. Immunol. 139, 2755-2760 (1987).
40. Weiss, A., Manger, B. & Imboden, J. Synergy between the T3/antigen receptor complex and Tp44 in the activation of human T cells. J. Immunol. 137, 819-625 (1986).
41. Shapiro, V. S., Mollenauer, M. N. & Weiss, A. Nuclear factor of activated T cells and AP-1 are insufficient for IL-2 promoter activation: requirement for CD28 up-regulation of RE/AP. J. Immunol. 161, 6455-6458 (1998).
42. Fraser, J. D., Newton, M. E. & Weiss, A. CD28 and T cell antigen receptor signal transduction coordinately regulate interleukin 2 gene expression in response to superantigen stimulation. J. Exp. Med. 175, 1131-1134 (1992).
43. Alessi, D. R. et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15, 6541-6551 (1996).
44. Lin, X., O'Mahony, A., Mu, Y., Geleziunas, R. & Greene, W. C. Protein kinase C-θ participates in NF-κB activation induced by CD3-CD28 costimulation through selective activation of IκB kinase β. Mol. Cell Biol. 20, 2933-2940 (2000).
45. Coudronniere, N., Villalba, M., Englund, N. & Altman, A. NF-κ B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-θ. Proc. Natl Acad. Sci. USA 97, 3394-3399 (2000).
46. Monks, C. R., Kupfer, H., Tamir, I., Barlow, A. & Kupfer, A. Selective modulation of protein kinase C-θ during T-cell activation. Nature 385, 83-86 (1997).
47. Wilkinson, S. E., Parker, P. J. & Nixon, J. S. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem. J. 294, 335-337 (1993).
48. Van Parijs, L. et al. Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11, 281-288 (1999).
49. Stokoe, D. et al. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277, 567-570 (1997).
50. Khattri, R., Auger, J.A., Griffin, M. D., Sharpe, A. H. & Bluestone, J.A. Lymphoproliferative disorder in CTLA-4 knockout mice is characterized by CD28-regulated activation of Th2 responses. J. Immunol. 162, 5784-5791 (1999).
51. Kubo, M. et al. CD28 costimulation accelerates IL-4 receptor sensitivity and IL-4- mediated Th2 differentiation. J. Immunol. 163, 2432-2442 (1999).
52. Rulifson, I. C., Sperling, A. I., Fields, P. E., Fitch, F.W. & Bluestone, J.A. CD28 costimulation promotes the production of Th2 cytokines. J. Immunol. 158, 658-665 (1997).
53. Ronchese, F., Hausmann, B., Hubele, S. & Lane, P. Mice transgenic for a soluble form of murine CTLA-4 show enhanced expansion of antigen-specific CD4+ T cells and defective antibody production in vivo. J. Exp. Med. 179, 809-817 (1994).
54. Lenschow, D. J. et al. CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity 5, 285-293 (1996).
55. Peterson, R.T. & Schreiber, S. L. Kinase phosphorylation: Keeping it all in the family. Curr. Biol. 9, R521-524 (1999).
56. Li-Weber, M., Giasi, M. & Krammer, P. H. Involvement of Jun and Rel proteins in up-regulation of interleukin-4 gene activity by the T cell accessory molecule CD28. J. Biol. Chem. 273, 32460-32466 (1998).
57. Stack, R. M., Thompson, C. B. & Fitch, F.W. IL-4 enhances long-term survival of CD28-deficient T cells. J. Immunol. 160, 2255-2262 (1998).
58. Chan, T. O., Rittenhouse, S. E. & Tsichlis, P. N. Akt/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu. Rev. Biochem. 68, 965-1014 (1999).
59. Parekh, D. B., Ziegler, W. & Parker, P. J. Multiple pathways control protein kinase C phosphorylation. EMBO J. 19, 496-503 (2000).
60. Ott, M. et al. Immune hyperactivation of HIV-1-infected T cells mediated by Tat and the CD28 pathway. Science 275, 1481-1485 (1997).
61. Borgatti, P. et al. Extracellular HIV-I Tat protein activates phosphatidylinositol 3- and Akt/PKB kinases in CD4+ T lymphoblastoid Jurkat cells. Eur J. Immunol. 27, 2805-2811 (1997).
62. Reif, K., Lucas, S. & Cantrell, D. A negative role for phosphoinositide 3-kinase in T-cell antigen receptor function. Curr. Biol. 7, 285-293 (1997).
63. Crooks, M. E. et al. CD28-mediated costimulation in the absence of phosphatidylinositol 3-kinase association and activation. Mol. Cell Biol. 15, 6820-6828 (1995).
64. Ward, S. G., Wilson, A., Turner, L., Westwick, J. & Sansom, D. M. Inhibition of CD28-mediated T cell costimulation by the phosphoinositide 3-kinase inhibitor wortmannin. Eur. J. Immunol. 25, 526-532 (1995).
65. Ward, S. G., June, C. H. & Olive, D. P1 3-kinase: a pivotal pathway in T-cell activation? Immunol. Today 17, 187-197 (1996).
66. Shan, X. et al. Deficiency of PTEN in jurkat T cells causes constitutive localization of itk to the plasma membrane and hyperresponsiveness to CD3 stimulation. Mol. Cell Biol. 20, 6945-6957 (2000).
67. Hehner, S. P. et al. Mixed-lineage kinase 3 delivers CD3/CD28-derived signals into the IκB kinase complex. Mol. Cell Biol. 20, 2556-2568 (2000).
68. Lin, X., Cunningham, E.T., Mu, Y., Geleziunas, R. & Greene, W. C. The proto-oncogene Cot kinase participates in CD3/CD28 induction of NF-κB acting through the NF-κB-inducing kinase and IκB kinases. Immunity 10, 271-280 (1999).
69. Tsatsanis, C., Patriotis, C. & Tsichlis, P. N. Tp1-2 induces IL-2 expression in T-cell lines by triggering multiple signaling pathways that activate NFAT and NF-κB. Oncogene 17, 2609-2618 (1998).
70. Tuosto, L. et al. Mitogen-activated kinase kinase kinase I regulates T cell receptor-and CD28-mediated signaling events which lead to NF-κB activation. Eur. J. Immunol. 30, 2445-2454 (2000).
71. Tsatsanis, C., Patriotis, C., Bear, S. E. & Tsichlis, P. N. The Tp1-2 protooncoprotein activates the nuclear factor of activated T cells and induces interleukin 2 expression in T cell lines. Proc. Natl Acad. Sci. USA 95, 3827-3832 (1998).
72. Ballester, A., Tobena, R., Lisbona, C., Calvo, V. & Alemany, S. Cot kinase regulation of IL-2 production in Jurkat T cells. J. Immunol. 159, 1613-1618 (1997).
73. Durand, D. B., Bush, M. R., Morgan, J. G., Weiss, A. & Crabtree, G. R. A 275 basepair fragment at the 5′ end of the interleukin 2 gene enhances expression from a heterologous promoter in response to signals from the T cell antigen receptor. J. Exp. Med. 165, 395-407 (1987).
74. Refaeli, Y., Van Parijs, L., London, C.A., Tschopp, J. & Abbas, A. K. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 8, 615-623 (1998).
75. Naviaux, R. K., Costanzi, E., Haas, M. & Verma, I. M. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol.. 70, 5701-5705 (1996).