Molecular modifiers of T cell antigen receptor triggering threshold: The mechanism of CD28 costimulatory receptor

Immunological Reviews

Volumn 192, Issue , 2003, Pages 21-31

  Acuto, Oreste ^a   Mise Omata, Setsuko ^a   Mangino, Giorgio ^a   Michel, Frédérique ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; PROTEIN TYROSINE KINASE; T LYMPHOCYTE RECEPTOR;

AGING; ANTIGEN FUNCTION; ANTIGEN PRESENTING CELL; ENZYME ACTIVATION; HUMAN; IMMUNE RESPONSE; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD28; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0037564560     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-065X.2003.00034.x     Document Type: Review

References (112)

1. Lanzavecchia A, Sallusto F. Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science 2000;290:92-97.
2. Irvine DJ, Purbhoo MA, Krogsgaard M, Davis MM. Direct observation of ligand recognition by T cells. Nature 2002;419:845-849.
3. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol 2002;2:116-126.
4. Viola A, Lanzavecchia A. T cell activation determined by T cell receptor number and tunable thresholds. Science 1996;273:104-106.
5. Schweitzer AN, Sharpe AH. Studies using antigen-presenting cells lacking expression of both B7-1 (CD80) and B7-2 (CD86) show distinct requirements for B7 molecules during priming versus restimulation of Th2 but not Th1 cytokine production. J Immunol 1998;161:2762-2771.
6. Manickasingham SP, Anderton SM, Burkhart C, Wraith DC. Qualitative and quantitative effects of CD28/B7-mediated costimulation on naive T cells in vitro. J Immunol 1998;161:3827-3835.
7. Kündig TM, et al. Duration of TCR stimulation determines costimulatory requirements of T cells. Immunity 1996;5:41-52.
8. Michel F, Acuto O. CD28 costimulation: a source of Vav-1 for TCR signaling with the help of SLP-76? Sci STKE 2002;2002:E35.
9. Bikoue A, George F, Poncelet P, Mutin M, Janossy G, Sampol J. Quantitative analysis of leukocyte membrane antigen expression: normal adult values. Cytometry 1996;26:137-147.
10. Bromley SK, et al. The immunological synapse and CD28-CD80 interactions. Nat Immunol 2001;2:1159-1166.
11. Velazquez C, DiPaolo R, Unanue ER. Quantitation of lysozyme peptides bound to class II MHC molecules indicates very large differences in levels of presentation. J Immunol 2001;166:5488-5494.
12. Hathcock KS, Laszlo G, Pucillo C, Linsley P, Hodes RJ. Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J Exp Med 1994;180:631-640.
13. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 1994;179:1109-1118.
14. Inaba K, et al. 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 1994;180:1849-1860.
15. Giacomini E, et al. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J Immunol 2001;166:7033-7041.
16. Collins AV, et al. The interaction properties of costimulatory molecules revisited. Immunity 2002;17:201-210.
17. van der Merwe PA, Bodian DL, Daenke S, Linsley P, Davis SJ. CD80 (B7-1) binds both CD28 and CTLA-4 with a low affinity and very fast kinetics. J Exp Med 1997;185:393-403.
18. Davis MM, et al. Ligand recognition by alpha beta T cell receptors. Annu Rev Immunol 1998;16:523-544.
19. Shimaoka M, Takagi J, Springer TA. Conformational regulation of integrin structure and function. Annu Rev Biophys Biomol Struct 2002;31:485-516.
20. Anton van der Merwe P, Davis SJ, Shaw AS, Dustin ML. Cytoskeletal polarization and redistribution of cell-surface molecules during T cell antigen recognition. Semin Immunol 2000;12:5-21.
21. Linsley PS, Clark EA, Ledbetter JA. T-cell antigen CD28 mediates adhesion with B cells by interacting with activation antigen B7/BB-1. Proc Natl Acad Sci USA 1990;87:5031-5035.
22. Arulanandam AR, Kister A, McGregor MJ, Wyss DF, Wagner G, Reinherz EL. Interaction between human CD2 and CD58 involves the major beta sheet surface of each of their respective adhesion domains. J Exp Med 1994;180:1861-1871.
23. Hauss P, Selz F, Cavazzana-Calvo M, Fischer A. Characteristics of antigen-independent and antigen-dependent interaction of dendritic cells with CD4+ T cells. Eur J Immunol 1995;25:2285-2294.
24. Hwang I, et al. T cells can use either T cell receptor or CD28 receptors to absorb and internalize cell surface molecules derived from antigen-presenting cells. J Exp Med 2000;191:1137-1148.
25. Michel F, Attal-Bonnefoy G, Mangino G, Mise-Omata S, Acuto O. CD28 as a molecular amplifier extending TCR ligation and signaling capabilities. Immunity 2001;15:935-945.
26. Bachmann MF, Barner M, Kopf M. CD2 sets quantitative thresholds in T cell activation. J Exp Med 1999;190:1383-1392.
27. Green JM, Karpitskiy V, Kimzey SL, Shaw AS. Coordinate regulation of T cell activation by CD2 and CD28. J Immunol 2000;164:3591-3595.
28. Lenschow DJ, Walunas TL, Bluestone JA. CD28/B7 system of T cell costimulation. Annu Rev Immunol 1996;14:233-258.
29. Green JM, Noel PJ, Sperling AI, Gray GS, Bluestone JA, Thompson CB. Absence of B7-dependent responses in CD28-deficient mice. Immunity 1994;1:501-508.
30. Shahinian A, et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science 1993;261:609-612.
31. Tuosto L, Acuto O. CD28 affects the earliest signaling events generated by TCR engagement. Eur J Immunol 1998;28:2131-2142.
32. Wild MK, et al. Dependence of T cell antigen recognition on the dimensions of an accessory receptor-ligand complex. J Exp Med 1999;190:31-41.
33. Dustin ML, Springer TA. T-cell receptor crosslinking transiently stimulates adhesiveness through LFA-1. Nature 1989;341:619-624.
34. Hogg N, Henderson R, Leitinger B, McDowall A, Porter J, Stanley P. Mechanisms contributing to the activity of integrins on leuko-cytes. Immunol Rev 2002;186:164-171.
35. Rudd CE. Upstream-downstream: CD28 cosignal pathways and T cell function. Immunity 1996;4:527-534.
36. Samelson LE. Signal transduction mediated by the T cell antigen receptor. The role of adapter proteins. Annu Rev Immunol 2002;20:371-394.
37. Koretzky GA, Myung PS. Positive and negative regulation of T-cell activation by adaptor proteins. Nat Rev Immunol 2001;1:95-107.
38. Isakov N, Altman A. Protein kinase C (theta) in T cell activation. Annu Rev Immunol 2002;20:761-794.
39. Ellis JH, Ashman C, Burden MN, Kilpatrick KE, Morse MA, Hamblin PA. GRID: a novel Grb-2-related adapter protein that interacts with the activated T cell costimulatory receptor CD28. J Immunol 2000;164:5805-5814.
40. Chuang E, et al. The CD28 and CTLA-4 receptors associate with the serine/threonine phosphatase PP2A. Immunity 2000;13:313-322.
41. Marti F, et al. Negative-feedback regulation of CD28 costimulation by a novel mitogen-activated protein kinase phosphatase, MKP6. J Immunol 2001;166:197-206.
42. Michel F, Grimaud L, Tuosto L, Acuto O. Fyn and ZAP-70 are required for Vav phosphorylation in T cells stimulated by antigen-presenting cells. J Biol Chem 1998;273:31932-31938.
43. Heyeck SD, Wilcox HM, Bunnell SC, Berg LJ. Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J Biol Chem 1997;272:25401-25408.
44. Holdorf AD, et al. Proline residues in CD28 and the Src homology (SH) 3 domain of Lck are required for T cell costimulation. J Exp Med 1999;190:375-384.
45. Sadra A, Cinek T, Arellano JL, Shi J, Truitt KE, Imboden JB. Identification of tyrosine phosphorylation sites in the CD28 cytoplasmic domain and their role in the costimulation of Jurkat T cells. J Immunol 1999;162:1966-1973.
46. Burr JS, et al. Cutting edge: distinct motifs within CD28 regulate T cell proliferation and induction of Bcl-XL. J Immunol 2001;166:5331-5335.
47. August A, Gibson S, Kawakami Y, Kawakami T, Mills GB, Dupont B. CD28 is associated with and induces the immediate tyrosine phosphorylation and activation of the Tec family kinase ITK/EMT in the human Jurkat leukemic T-cell line. Proc Natl Acad Sci USA 1994;91:9347-9351.
48. Yang WC, et al. Role of Tec kinase in nuclear factor of activated T cells signaling. Int Immunol 2000;12:1547-1552.
49. Holdorf AD, Lee KH, Burack WR, Allen PM, Shaw AS. Regulation of Lck activity by CD4 and CD28 in the immunological synapse. Nat Immunol 2002;3:259-264.
50. Irles C, Symons A, Michel F, Bakker TR, van der Merwe PA, Acuto O. CD45 ectodomain controls interaction with GEMs and lck activity for optimal TCR signaling. Nat Immunol 2003;4:189-197.
51. Lemmon MA, Ferguson KM. Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 2000;350:1-18.
52. Appleman LJ, van Puijenbroek AA, Shu KM, Nadler LM, Boussiotis VA. CD28 costimulation mediates down-regulation of p27kip 1 and cell cycle progression by activation of the PI3K/PKB signaling pathway in primary human T cells. J Immunol 2002;168:2729-2736.
53. Diehn M, et al. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc Natl Acad Sci USA 2002;99:11796-11801.
54. Okkenhaug K, et al. A point mutation in CD28 distinguishes proliferative signals from survival signals. Nat Immunol 2001;2:325-332.
55. Harada Y, et al. Critical requirement for the membrane-proximal cytosolic tyrosine residue for CD28-mediated costimulation in vivo. J Immunol 2001;166:3797-3803.
56. Yang WC, Ghiotto M, Barbarat B, Olive D. The role of Tec protein-tyrosine kinase in T cell signaling. J Biol Chem 1999;214:607-617.
57. Miller AT, Berg LJ. New insights into the regulation and functions of Tec family tyrosine kinases in the immune system. Curr Opin Immunol 2002;14:331-340.
58. Crespo P, Schuebel KE, Ostrom AA, Gutkind JS, Bustelo XR. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature 1997;385:169-172.
59. Turner M, Billadeau DD. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat Rev Immunol 2002;2:476-486.
60. Klasen D, Pages F, Peyron J-F, Cantrell DA, Olive D. Two distinct regions of the CD28 intracytoplasmic domain are involved in the tyrosine phosphorylation of Vav and GTPase activating protein-associated p62 protein. Int Immunol 1998;10:481-489.
61. Kaga S, Ragg S, Rogers KA, Ochi A. Stimulation of CD28 with B7-2 promotes focal adhesion-like cell contacts where Rho family small G proteins accumulate in T cells. J Immunol 1998;160:24-27.
62. Michel F, et al. CD28 utilizes Vav-1 to enhance TCR-proximal signaling and NF-AT activation. J Immunol 2000;165:3820-3829.
63. Hehner SP, Hofmann TG, Dienz O, Droge W, Schmitz ML. Tyrosine-phosphorylated Vav1 as a point of integration for T-cell receptor-and CD28-mediated activation of JNK, p38, and interleukin-2 transcription. J Biol Chem 2000;275:18160-18171.
64. Marinari B, et al. Vav cooperates with CD28 to induce NF-kappaB activation via a pathway involving Rac-1 and mitogen-activated kinase kinase 1. Eur J Immunol 2002;32:447-456.
65. Costello PS, et al. The Rho-family GTP exchange factor Vav is a critical transducer of T cell receptor signals to the calcium, ERK, and NF-kappaB pathways. Proc Natl Acad Sci USA 1999;96:3035-3040.
66. Inabe K, Ishiai M, Scharenberg AM, Freshney N, Downward J, Kurosaki T. Vav3 modulates B cell receptor responses by regulating phosphoinositide 3-kinase activation. J Exp Med 2002;195:189-200.
67. Kim HH, Tharayil M, Rudd CE. Growth factor receptor-bound protein 2 SH2/SH3 domain binding to CD28 and its role in co-signaling. J Biol Chem 1998;273:296-301.
68. Han J, et al. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 1998;279:558-560.
69. Aghazadeh B, Lowry WE, Huang X-Y, Rosen MK. Structural basis for relief of autoinhibition of the Db1 homology domain of proto-oncogene Vav by tyrosine phosphorylation. Cell 2000;102:625-633.
70. Manetz TS, Gonzalez-Espinosa C, Arudchandran R, Xirasagar S, Tybulewicz V, Rivera J. Vav 1 regulates phospholipase C gamma activation and calcium responses in mast cells. Mol Cell Biol 2001;21:3763-3774.
71. Reynolds LF, et al. Vav1 transduces T cell receptor signals to the activation of phospholipase C-gamma1 via phosphoinositide 3-kinase-dependent and -independent pathways. J Exp Med 2002;195:1103-1114.
72. Genot EM, Arrienmerlou C, Ku G, Burgering BM, Weiss A, Kramer IM. The T-cell receptor regulates Akt (protein kinase B) via a pathway involving Rac1 and phosphatidylinositide 3-kinase. Mol Cell Biol 2000;20:5469-5478.
73. Iezzi G, Karjalainen K, Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 1998;8:89-95.
74. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998;395:82-86.
75. Grakoui A, et al. The immunological synapse: a molecular machine controlling T cell activation. Science 1999;285:221-227.
76. Krummel MF, Sjaastad MD, Wulfing C, Davis MM. Differential clustering of CD4 and CD3zeta during T cell recognition. Science 2000;289:1349-1352.
77. Wetzel SA, McKeithan TW, Parker DC. Live-cell dynamics and the role of costimulation in immunological synapse formation. J Immunol 2002;169:6092-6101.
78. Penninger JM, Crabtree GR. The actin cytoskeleton and lymphocyte activation. Cell 1999;96:9-12.
79. Wulfing C, Bauch A, Crabtree GR, Davis MM. The vav exchange factor is an essential regulator in actin-dependent receptor translocation to the lymphocyte-antigen-presenting cell interface. Proc Natl Acad Sci USA 2000;97:10150-10155.
80. Wulfing C, Sumen C, Sjaastad MD, Wu LC, Dustin ML, Davis MM. Costimulation and endogenous MHC ligands contribute to T cell recognition. Nat Immunol 2002;3:42-47.
81. Huang J, et al. CD28 plays a critical role in the segregation of PKCtheta within the immunologic synapse. Proc Natl Acad Sci USA 2002;99:9369-9373.
82. Wulfing C, Davis MM. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 1998;282:2266-2269.
83. Langlet C, Bernard AM, Drevot P, He HT. Membrane rafts and signaling by the multichain immune recognition receptors. Curr Opin Immunol 2000;12:250-255.
84. Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 1999;283:680-682.
85. Harder T, Simons K. Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur J Immunol 1999;29:556-562.
86. Villalba M, Bi K, Rodriguez F, Tanaka Y, Schoenberger S, Altman A. Vav1/Rac-dependent actin cytoskeleton reorganization is required for hpid raft clustering in T cells. J Cell Biol 2001;155:331-338.
87. Zaru R, Berrie CP, Iurisci C, Corda D, Valitutti S. CD28 co-stimulates TCR/CD3-induced phosphoinositide turnover in human T lymphocytes. Eur J Immunol 2001;31:2438-2447.
88. 2+ signaling pattern in CD4(+)CD8(+) thymocytes. J Exp Med 1999;190:943-952.
89. Dustin ML, Bromley SK, Kan Z, Peterson DA, Unanue ER. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc Natl Acad Sci USA 1997;94:3909-3913.
90. Turley SJ, et al. Transport of peptide - MHC class II complexes in developing dendritic cells. Science 2000;288:522-527.
91. Lee KH, Holdorf AD, Dustin ML, Chan AC, Allen PM, Shaw AS. T cell receptor signaling precedes immunological synapse formation. Science 2002;295:1539-1542.
92. van der Merwe PA. Formation and function of the immunological synapse. Curr Opin Immunol 2002;14:293-298.
93. Kupfer A, Mosmann TR, Kupfer H. Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc Natl Acad Sci USA 1991;88:775-779.
94. Hermiston ML, Xu Z, Majeti R, Weiss A. Reciprocal regulation of lymphocyte activation by tyrosine kinases and phosphatases. J Clin Invest 2002;109:9-14.
95. Raab M, Pfister S, Rudd CE. CD28 signaling via VAV/SLP-76 adaptors: regulation of cytokine transcription independent of TCR ligation. Immunity 2001;15:921-933.
96. Fowell DJ, et al. Impaired NFATc translocation and failure of Th2 development in Itk-deficient CD4+ T cells. Immunity 1999;11:399-409.
97. Beals CR, Sheridan CM, Turck CW, Gardner P, Crabtree GR. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 1997;275:1930-1934.
98. Kane LP, Lin J, Weiss A. It's all Rel-ative: NF-kappaB and CD28 costimulation of T-cell activation. Trends Immunol 2002;23:413-420.
99. Gaide O, et al. CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation. Nat Immunol 2002;3:836-843.
100. Kane LP, Andres PG, Howland KC, Abbas AK, Weiss A. Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-gaanma but not TH2 cytokines. Nat Immunol 2001;2:37-44.
101. Kane LP, Mollenauer MN, Xu Z, Turck CW, Weiss A. Akt-dependent phosphorylation specifically regulates Cot induction of NF-kappa B-dependent transcription. Mol Cell Biol 2002;22:5962-5974.
102. Arendt CW, Albrecht B, Soos TJ, Littman DR. Protein kinase C-theta: signaling from the center of the T-cell synapse. Curr Opin Immunol 2002;14:323-330.
103. Villalba M, et al. Translocation of PKC[theta] in T cells is mediated by a nonconventional, PI3-K- and Vav-dependent pathway, but does not absolutely require phospholipase C. J Cell Biol 2002;157:253-263.
104. Villalba M, Coudronniere N, Deckert M, Teixeiro E, Mas P, Altman A. A novel functional interaction between Vav and PKCtheta is required for TCR-induced T cell activation. Immunity 2000;12:151-160.
105. Rincon M, Flavell R. AP-1 transcriptional activity requires both T-cell receptor-mediated and co-stimulatory signals in primary T lymphocytes. EMBO J 1994;13:4370-4381.
106. Schaeffer EM, et al. Requirement for Tec kinases Rlk and Irk in T cell receptor signaling and immunity. Science 1999;284:638-641.
107. Su B, Jacinto E, Hibi M, Kallunki T, Karin M, Ben-Neriah Y. JNK is involved in signal integration during costimulation of T lymphocytes. Cell 1994;77:727-736.
108. Tzachanis D, et al. Tob is a negative regulator of activation that is expressed in anergic and quiescent T cells. Nat Immunol 2001;2:1174-1182.
109. Bonnevier JL, Mueller DL. Cutting edge: B7/CD28 interactions regulate cell cycle progression independent of the strength of TCR signaling. J Immunol 2002;169:6659-6663.
110. Gudmundsdottir H, Wells AD, Turka LA. Dynamics and requirements of T cell clonal expansion in vivo at the single-cell level: effector function is linked to proliferative capacity. J Immunol 1999;162:5212-5223.
111. Boise LH, et al. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 1993;74:597-608.
112. Plas DR, Rathmell JC, Thompson CB. Homeostatic control of lymphocyte survival potential origins and implication. Nat Immunol 2002;1:515-521.