CD28 co-signaling in the adaptive immune response

Self/Nonself - Immune Recognition and Signaling

Volumn 1, Issue 3, 2010, Pages 231-240

  Riha, Pavel ^a   Rudd, Christopher E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

CD28; Co stimulation; Grb2; NfkB; PI3K; T cells

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD86 ANTIGEN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; T LYMPHOCYTE RECEPTOR;

ADAPTIVE IMMUNITY; AUTOIMMUNITY; HUMAN; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 78049310884     PISSN: 19382030     EISSN: 19382049     Source Type: Journal    
DOI: 10.4161/self.1.3.12968     Document Type: Review

References (129)

1. Bretscher P, Cohn M. A theory of self-nonself discrimination. Science 1970; 169:1042-9.
2. Lafferty KJ, Misko IS, Cooley MA. Allogeneic stimulation modulates the in vitro response of T cells to transplantation antigen. Nature 1974; 249:275-6.
3. Jenkins MK, Schwartz RH. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J Exp Med 1987; 165:302-19.
4. Rudd CE, Schneider H. Unifying concepts in CD28, ICOS and CTLA4 co-receptor signalling. Nat Rev Immunol 2003; 3:544-56.
5. Rudd CE. The reverse stop-signal model for CTLA4 function. Nat Rev Immunol 2008; 8:153-60.
6. Rudd CE, Taylor A, Schneider H. CD28 and CTLA-4 co-receptor expression and signal transduction. Immunol Rev 2009; 229:12-26.
7. Thangavelu G, Smolarchuk C, Anderson CC. Co-inhibitory molecules: Controlling the effectors or controlling the controllers? Self/Nonself 2010; 1:77-88.
8. Lee KP, Taylor C, Petryniak B, Turka LA, June CH, Thompson CB. The genomic organization of the CD28 gene. Implications for the regulation of CD28 mRNA expression and heterogeneity. J Immunol 1990; 145:344-52.
9. Gross JA, St. John T, Allison JP. The murine homologue of the T lymphocyte antigen CD28. Molecular cloning and cell surface expression. J Immunol 1990; 144:3201-10.
10. Freeman GJ, Borriello F, Hodes RJ, Reiser H, Gribben JG, Ng JW, et al. Murine B7-2, an alternative CTLA4 counter-receptor that costimulates T cell proliferation and interleukin 2 production. J Exp Med 1993; 178:2185-92.
11. Freeman GJ, Gribben JG, Boussiotis VA, Ng JW, Restivo VA Jr, Lombard LA, et al. Cloning of B7-2: a CTLA-4 counter-receptor that costimulates human T cell proliferation. Science 1993; 262:909-11.
12. Inaba K, Witmer-Pack M, Inaba M, Hathcock KS, Sakuta H, Azuma M, 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; 180:1849-60.
13. 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; 180:631-40.
14. Gmunder H, Lesslauer W. A 45 kDa human T-cell membrane glycoprotein functions in the regulation of cell proliferative responses. Eur J Biochem 1984; 142:153-60.
15. Lesslauer W, Koning F, Ottenhoff T, Giphart M, Goulmy E, van Rood JJ. T90/44 (9.3 antigen). A cell surface molecule with a function in human T cell activation. Eur J Immunol 1986; 16:1289-96.
16. Aruffo A, Seed B. Molecular cloning of a CD28 cDNA by a high-efficiency COS cell expression system. Proc Natl Acad Sci USA 1987; 84:8573-7.
17. Naluai AT, Nilsson S, Samuelsson L, Gudjonsdottir AH, Ascher H, Ek J, et al. The CTLA4/CD28 gene region on chromosome 2q33 confers susceptibility to celiac disease in a way possibly distinct from that of type 1 diabetes and other chronic inflammatory disorders. Tissue Antigens 2000; 56:350-5.
18. Howard TA, Rochelle JM, Seldin MF. Cd28 and Ctla-4, two related members of the Ig supergene family, are tightly linked on proximal mouse chromosome 1. Immunogenetics 1991; 33:74-6.
19. Shahinian A, Pfeffer K, Lee KP, Kundig TM, Kishihara K, Wakeham A, et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science 1993; 261:609-12.
20. + cells. Eur J Immunol 1995; 25:587-95.
21. Rulifson IC, Sperling AI, Fields PE, Fitch FW, Bluestone JA. CD28 costimulation promotes the production of Th2 cytokines. J Immunol 1997; 158:658-65.
22. Ferguson SE, Han S, Kelsoe G, Thompson CB. CD28 is required for germinal center formation. J Immunol 1996; 156:4576-81.
23. Borriello F, Sethna MP, Boyd SD, Schweitzer AN, Tivol EA, Jacoby D, et al. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 1997; 6:303-13.
24. Boise LH, Minn AJ, Noel PJ, June CH, Accavitti MA, Lindsten T, et al. CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity 1995; 3:87-98.
25. + helper T cells. A model for the long-term survival of memory cells. J Immunol 1996; 156:1764-71.
26. Kundig TM, Shahinian A, Kawai K, Mittrucker HW, Sebzda E, Bachmann MF, et al. Duration of TCR stimulation determines costimulatory requirement of T cells. Immunity 1996; 5:41-52.
27. Harper K, Balzano C, Rouvier E, Mattei MG, Luciani MF, Golstein P. 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 1991; 147:1037-44.
28. Collins AV, Brodie DW, Gilbert RJ, Iaboni A, Manso-Sancho R, Walse B, et al. The interaction properties of costimulatory molecules revisited. Immunity 2002; 17:201-10.
29. 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.
30. Freeman GJ, Gray GS, Gimmi CD, Lombard DB, Zhou LJ, White M, et al. Structure, expression and T cell costimulatory activity of the murine homologue of the human B lymphocyte activation antigen B7. J Exp Med 1991; 174:625-31.
31. Maxwell LJ, Singh JA. Abatacept for rheumatoid arthritis: a Cochrane systematic review. J Rheumatol 2010; 37:234-45.
32. St Clair EW. Novel targeted therapies for autoimmunity. Curr Opin Immunol 2009; 21:648-57.
33. Cruzado JM, Bestard O, Grinyo JM. New immunosuppressive protocols with the advent of novel biological drugs. Transplantation 2009; 88:20-3.
34. Kremer JM, Genant HK, Moreland LW, Russell AS, Emery P, Abud-Mendoza C, et al. Effects of abatacept in patients with methotrexate-resistant active rheumatoid arthritis: a randomized trial. Ann Intern Med 2006; 144:865-76.
35. Weaver TA, Charafeddine AH, Kirk AD. Costimulation blockade: towards clinical application. Front Biosci 2008; 13:2120-39.
36. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 2007; 27:111-22.
37. + T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009; 10:29-37.
38. Cefai D, Schneider H, Matangkasombut O, Kang H, Brody J, Rudd CE. CD28 receptor endocytosis is targeted by mutations that disrupt phosphatidylinositol 3-kinase binding and costimulation. J Immunol 1998; 160:2223-30.
39. Badour K, McGavin MK, Zhang J, Freeman S, Vieira C, Filipp D, et al. Interaction of the Wiskott-Aldrich syndrome protein with sorting nexin 9 is required for CD28 endocytosis and cosignaling in T cells. Proc Natl Acad Sci USA 2007; 104:1593-8.
40. Bluestone JA. New perspectives of CD28-B7-mediated T cell costimulation. Immunity 1995; 2:555-9.
41. Linsley PS. Distinct roles for CD28 and cytotoxic T lymphocyte-associated molecule-4 receptors during T cell activation? J Exp Med 1995; 182:289-92.
42. Noel PJ, Boise LH, Thompson CB. Regulation of T cell activation by CD28 and CTLA4. Adv Exp Med Biol 1996; 406:209-17.
43. + thymocytes by T cell receptor-induced apoptosis requires a costimulatory signal that can be provided by CD28. J Exp Med 1994; 179:709-13.
44. Prasad KV, Cai YC, Raab M, Duckworth B, Cantley L, Shoelson SE, et al. 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 1994; 91:2834-8.
45. August A, Dupont B. CD28 of T lymphocytes associates with phosphatidylinositol 3-kinase. Int Immunol 1994; 6:769-74.
46. Pages F, Ragueneau M, Rottapel R, Truneh A, Nunes J, Imbert J, et al. Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 1994; 369:327-9.
47. Truitt KE, Hicks CM, Imboden JB. Stimulation of CD28 triggers an association between CD28 and phosphatidylinositol 3-kinase in Jurkat T cells. J Exp Med 1994; 179:1071-6.
48. Raab M, Cai YC, Bunnell SC, Heyeck SD, Berg LJ, Rudd CE. p56lck and p59fyn regulate CD28 binding to phosphatidylinositol 3-kinase, growth factor receptorbound protein GRB-2 and T cell-specific protein-tyrosine kinase ITK: implications for T-cell costimulation. Proc Natl Acad Sci USA 1995; 92:8891-5.
49. Schneider H, Cai YC, Prasad KV, Shoelson SE, Rudd CE. T cell antigen CD28 binds to the GRB-2/SOS complex, regulators of p21ras. Eur J Immunol 1995; 25:1044-50.
50. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, et al. Function of PI3Kgamma in thymocyte development, T cell activation and neutrophil migration. Science 2000; 287:1040-6.
51. Garcon F, Patton DT, Emery JL, Hirsch E, Rottapel R, Sasaki T, et al. CD28 provides T-cell costimulation and enhances PI3K activity at the immune synapse independently of its capacity to interact with the p85/ p110 heterodimer. Blood 2008; 111:1464-71.
52. Soond DR, Bjorgo E, Moltu K, Dale VQ, Patton DT, Torgersen KM, et al. PI3K p110delta regulates T-cell cytokine production during primary and secondary immune responses in mice and humans. Blood 2010; 115:2203-13.
53. Lee KS, Lee HK, Hayflick JS, Lee YC, Puri KD. Inhibition of phosphoinositide 3-kinase delta attenuates allergic airway inflammation and hyperresponsiveness in murine asthma model. FASEB J 2006; 20:455-65.
54. Ward SG, Cantrell DA. Phosphoinositide 3-kinases in T lymphocyte activation. Curr Opin Immunol 2001; 13:332-8.
55. Ward SG, Ley SC, MacPhee C, Cantrell DA. Regulation of D-3 phosphoinositides during T cell activation via the T cell antigen receptor/CD3 complex and CD2 antigens. Eur J Immunol 1992; 22:45-9.
56. Deane JA, Trifilo MJ, Yballe CM, Choi S, Lane TE, Fruman DA. Enhanced T cell proliferation in mice lacking the p85beta subunit of phosphoinositide 3-kinase. J Immunol 2004; 172:6615-25.
57. Deane JA, Kharas MG, Oak JS, Stiles LN, Luo J, Moore TI, et al. T-cell function is partially maintained in the absence of class IA phosphoinositide 3-kinase signaling. Blood 2007; 109:2894-902.
58. Kang H, Schneider H, Rudd CE. Phosphatidylinositol 3-kinase p85 adaptor function in T-cells. Co-stimulation and regulation of cytokine transcription independent of associated p110. J Biol Chem 2002; 277:912-21.
59. Cai YC, Cefai D, Schneider H, Raab M, Nabavi N, Rudd CE. Selective CD28pYMNM mutations implicate phosphatidylinositol 3-kinase in CD86-CD28-mediated costimulation. Immunity 1995; 3:417-26.
60. Cefai D, Cai YC, Hu H, Rudd C. CD28 co-stimulatory regimes differ in their dependence on phosphatidylinositol 3-kinase: common co-signals induced by CD80 and CD86. Int Immunol 1996; 8:1609-16.
61. 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.
62. Okkenhaug K, Wu L, Garza KM, La Rose J, Khoo W, Odermatt B, et al. A point mutation in CD28 distinguishes proliferative signals from survival signals. Nat Immunol 2001; 2:325-32.
63. Burr JS, Savage ND, Messah GE, Kimzey SL, Shaw AS, Arch RH, et al. Cutting edge: distinct motifs within CD28 regulate T cell proliferation and induction of Bcl-XL. J Immunol 2001; 166:5331-5.
64. Harada Y, Tokushima M, Matsumoto Y, Ogawa S, Otsuka M, Hayashi K, et al. Critical requirement for the membrane-proximal cytosolic tyrosine residue for CD28-mediated costimulation in vivo. J Immunol 2001; 166:3797-803.
65. Radvanyi LG, Shi Y, Vaziri H, Sharma A, Dhala R, Mills GB, et al. CD28 costimulation inhibits TCR-induced apoptosis during a primary T cell response. J Immunol 1996; 156:1788-98.
66. Sperling AI, Auger JA, Ehst BD, Rulifson IC, Thompson CB, Bluestone JA. CD28/B7 interactions deliver a unique signal to naive T cells that regulates cell survival but not early proliferation. J Immunol 1996; 157:3909-17.
67. Kirchhoff S, Muller WW, Li-Weber M, Krammer PH. Upregulation of c-FLIPshort and reduction of activation-induced cell death in CD28-costimulated human T cells. Eur J Immunol 2000; 30:2765-74.
68. Yao R, Cooper GM. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 1995; 267:2003-6.
69. Jones RG, Elford AR, Parsons MJ, Wu L, Krawczyk CM, Yeh WC, et al. CD28-dependent activation of protein kinase B/Akt blocks Fas-mediated apoptosis by preventing death-inducing signaling complex assembly. J Exp Med 2002; 196:335-48.
70. Appleman LJ, van Puijenbroek AA, Shu KM, Nadler LM, Boussiotis VA. CD28 costimulation mediates downregulation of p27kip1 and cell cycle progression by activation of the PI3K/PKB signaling pathway in primary human T cells. J Immunol 2002; 168:2729-36.
71. Wood JE, Schneider H, Rudd CE. TcR and TcR-CD28 engagement of protein kinase B (PKB/AKT) and glycogen synthase kinase-3 (GSK-3) operates independently of guanine nucleotide exchange factor VAV-1. J Biol Chem 2006; 281:32385-94.
72. Schneider H, Valk E, Leung R, Rudd CE. CTLA-4 activation of phosphatidylinositol 3-kinase (PI 3-K) and protein kinase B (PKB/AKT) sustains T-cell anergy without cell death. PLoS One 2008; 3:3842.
73. Dodson LF, Boomer JS, Deppong CM, Shah DD, Sim J, Bricker TL, et al. Targeted knock-in mice expressing mutations of CD28 reveal an essential pathway for costimulation. Mol Cell Biol 2009; 29:3710-21.
74. Frauwirth KA, Riley JL, Harris MH, Parry RV, Rathmell JC, Plas DR, et al. The CD28 signaling pathway regulates glucose metabolism. Immunity 2002; 16:769-77.
75. Matthews SA, Cantrell DA. New insights into the regulation and function of serine/threonine kinases in T lymphocytes. Immunol Rev 2009; 228:241-52.
76. Okkenhaug K, Rottapel R. Grb2 forms an inducible protein complex with CD28 through a Src homology 3 domain-proline interaction. J Biol Chem 1998; 273:21194-202.
77. Arimura Y, Kato H, Dianzani U, Okamoto T, Kamekura S, Buonfiglio D, et al. A co-stimulatory molecule on activated T cells, H4/ICOS, delivers specific signals in T(h) cells and regulates their responses. Int Immunol 2002; 14:555-66.
78. Harada Y, Ohgai D, Watanabe R, Okano K, Koiwai O, Tanabe K, et al. A single amino acid alteration in cytoplasmic domain determines IL-2 promoter activation by ligation of CD28 but not inducible costimulator (ICOS). J Exp Med 2003; 197:257-62.
79. Ye ZS, Baltimore D. Binding of Vav to Grb2 through dimerization of Src homology 3 domains. Proc Natl Acad Sci USA 1994; 91:12629-33.
80. Schneider H, Rudd CE. CD28 and Grb-2, relative to Gads or Grap, preferentially co-operate with Vav1 in the activation of NFAT/AP-1 transcription. Biochem Biophys Res Commun 2008; 369:616-21.
81. Moller A, Dienz O, Hehner SP, Droge W, Schmitz ML. Protein kinase Ctheta cooperates with Vav1 to induce JNK activity in T-cells. J Biol Chem 2001; 276:20022-8.
82. Marinari B, Costanzo A, Viola A, Michel F, Mangino G, Acuto O, et al. Vav cooperates with CD28 to induce NFkappaB activation via a pathway involving Rac-1 and mitogen-activated kinase kinase 1. Eur J Immunol 2002; 32:447-56.
83. Bustelo XR. Regulatory and signaling properties of the Vav family. Mol Cell Biol 2000; 20:1461-77.
84. Fischer KD, Kong YY, Nishina H, Tedford K, Marengere LE, Kozieradzki I, et al. Vav is a regulator of cytoskeletal reorganization mediated by the T-cell receptor. Curr Biol 1998; 8:554-62.
85. Holsinger LJ, Graef IA, Swat W, Chi T, Bautista DM, Davidson L, et al. Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction. Curr Biol 1998; 8:563-72.
86. Krawczyk C, Oliveira-dos-Santos A, Sasaki T, Griffiths E, Ohashi PS, Snapper S, et al. Vav1 controls integrin clustering and MHC/peptide-specific cell adhesion to antigen-presenting cells. Immunity 2002; 16:331-43.
87. 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; 160:24-7.
88. Raab M, Pfister S, Rudd CE. CD28 signaling via VAV/ SLP-76 adaptors: regulation of cytokine transcription independent of TCR ligation. Immunity 2001; 15:921-33.
89. Rudd CE, Raab M. Independent CD28 signaling via VAV and SLP-76: a model for in trans costimulation. Immunol Rev 2003; 192:32-41.
90. Michel F, Mangino G, Attal-Bonnefoy G, Tuosto L, Alcover A, Roumier A, et al. CD28 utilizes Vav-1 to enhance TCR-proximal signaling and NF-AT activation. J Immunol 2000; 165:3820-9.
91. Acuto O, Michel F. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 2003; 3:939-51.
92. Annibaldi A, Sajeva A, Muscolini M, Ciccosanti F, Corazzari M, Piacentini M, et al. CD28 ligation in the absence of TCR promotes RelA/NFkappaB recruitment and trans-activation of the HIV-1 LTR. Eur J Immunol 2008; 38:1446-51.
93. Takeda K, Harada Y, Watanabe R, Inutake Y, Ogawa S, Onuki K, et al. CD28 stimulation triggers NFkappaB activation through the CARMA1-PKCtheta-Grb2/ Gads axis. Int Immunol 2008; 20:1507-15.
94. Holdorf AD, Green JM, Levin SD, Denny MF, Straus DB, Link V, 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; 190:375-84.
95. Tavano R, Contento RL, Baranda SJ, Soligo M, Tuosto L, Manes S, et al. CD28 interaction with filamin-A controls lipid raft accumulation at the T-cell immunological synapse. Nat Cell Biol 2006; 8:1270-6.
96. Hayashi K, Altman A. Filamin A is required for T cell activation mediated by protein kinase C-theta. J Immunol 2006; 177:1721-8.
97. Sanchez-Lockhart M, Graf B, Miller J. Signals and sequences that control CD28 localization to the central region of the immunological synapse. J Immunol 2008; 181:7639-48.
98. Yokosuka T, Kobayashi W, Sakata-Sogawa K, Takamatsu M, Hashimoto-Tane A, Dustin ML, et al. Spatiotemporal regulation of T cell costimulation by TCR-CD28 microclusters and protein kinase Ctheta translocation. Immunity 2008; 29:589-601.
99. Altman A, Villalba M. Protein kinase C-theta (PKCtheta): it's all about location. Immunol Rev 2003; 192:53-63.
100. 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; 15:935-45.
101. 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; 12:151-60.
102. 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; 91:9347-51.
103. Liu KQ, Bunnell SC, Gurniak CB, Berg LJ. T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J Exp Med 1998; 187:1721-7.
104. Liao XC, Littman DR. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity 1995; 3:757-69.
105. Kon-Kozlowski M, Pani G, Pawson T, Siminovitch KA. The tyrosine phosphatase PTP1C associates with Vav, Grb2 and mSos1 in hematopoietic cells. J Biol Chem 1996; 271:3856-62.
106. Taylor A, Akdis M, Joss A, Akkoc T, Wenig R, Colonna M, et al. IL-10 inhibits CD28 and ICOS costimulations of T cells via src homology 2 domain-containing protein tyrosine phosphatase 1. J Allergy Clin Immunol 2007; 120:76-83.
107. Sathish JG, Johnson KG, LeRoy FG, Fuller KJ, Hallett MB, Brennan P, et al. Requirement for CD28 costimulation is lower in SHP-1-deficient T cells. Eur J Immunol 2001; 31:3649-58.
108. Joss A, Akdis M, Faith A, Blaser K, Akdis CA. IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway. Eur J Immunol 2000; 30:1683-90.
109. Freeburn RW, Wright KL, Burgess SJ, Astoul E, Cantrell DA, Ward SG. Evidence that SHIP-1 contributes to phosphatidylinositol 3,4,5-trisphosphate metabolism in T lymphocytes and can regulate novel phosphoinositide 3-kinase effectors. J Immunol 2002; 169:5441-50.
110. Tarazona R, Borrego F, Galiani MD, Aguado E, Pena J, Coligan JE, et al. Inhibition of CD28-mediated natural cytotoxicity by KIR2DL2 does not require p56(lck) in the NK cell line YT-Indy. Mol Immunol 2002; 38:495-503.
111. Linsley PS. New look at an old costimulator. Nat Immunol 2005; 6:231-2.
112. Riley JL, Mao M, Kobayashi S, Biery M, Burchard J, Cavet G, et al. Modulation of TCR-induced transcriptional profiles by ligation of CD28, ICOS and CTLA-4 receptors. Proc Natl Acad Sci USA 2002; 99:11790-5.
113. Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 1999; 283:680-2.
114. Martin M, Schneider H, Azouz A, Rudd CE. Cytotoxic T lymphocyte antigen 4 and CD28 modulate cell surface raft expression in their regulation of T cell function. J Exp Med 2001; 194:1675-81.
115. Collins TL, Deckert M, Altman A. Views on Vav. Immunol Today 1997; 18:221-5.
116. Chiang YJ, Kole HK, Brown K, Naramura M, Fukuhara S, Hu RJ, et al. Cbl-b regulates the CD28 dependence of T-cell activation. Nature 2000; 403:216-20.
117. Paolino M, Penninger JM. Cbl-b in T-cell activation. Semin Immunopathol 2010; 32:137-48.
118. Marinari B, Costanzo A, Marzano V, Piccolella E, Tuosto L. CD28 delivers a unique signal leading to the selective recruitment of RelA and p52 NFkappaB subunits on IL-8 and Bcl-XL gene promoters. Proc Natl Acad Sci USA 2004; 101:6098-103.
119. Blanchet F, Cardona A, Letimier FA, Hershfield MS, Acuto O. CD28 costimulatory signal induces protein arginine methylation in T cells. J Exp Med 2005; 202:371-7.
120. Lee JY, Engelman JA, Cantley LC. Biochemistry. PI3K charges ahead. Science 2007; 317:206-7.
121. Harding FA, McArthur JG, Gross JA, Raulet DH, Allison JP. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 1992; 356:607-9.
122. Khoruts A, Mondino A, Pape KA, Reiner SL, Jenkins MK. A natural immunological adjuvant enhances T cell clonal expansion through a CD28-dependent, interleukin (IL)-2-independent mechanism. J Exp Med 1998; 187:225-36.
123. Bachmaier K, Pummerer C, Shahinian A, Ionescu J, Neu N, Mak TW, et al. Induction of autoimmunity in the absence of CD28 costimulation. J Immunol 1996; 157:1752-7.
124. Sansom DM, Walker LS. The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology. Immunol Rev 2006; 212:131-48.
125. Zhang J, Salojin KV, Delovitch TL. CD28 co-stimulation restores T cell responsiveness in NOD mice by overcoming deficiencies in Rac-1/p38 mitogenactivated protein kinase signaling and IL-2 and IL-4 gene transcription. Int Immunol 2001; 13:377-84.
126. + T cells require CD28 costimulation. J Immunol 2007; 179:6494-503.
127. + T cell differentiation by CD80/CD86-CD28 costimulation and restoration by IL-2 during the recall response. J Immunol 2008; 180:1148-57.
128. Donahue JG, Choo PW, Manson JE, Platt R. The incidence of herpes zoster. Arch Intern Med 1995; 155:1605-9.
129. Goronzy JJ, Weyand CM. Rheumatoid arthritis. Immunol Rev 2005; 204:55-73.