Ligation of CD28 stimulates the formation of a multimeric signaling complex involving Grb-2-associated binder 2 (Gab2), Src homology phosphatase-2, and phosphatidylinositol 3-kinase: Evidence that negative regulation of CD28 signaling requires the Gab2 pleckstrin homology domain

Journal of Immunology

Volumn 176, Issue 1, 2006, Pages 594-602

  Parry, Richard V ^a   Whittaker, Gillian C ^a   Sims, Martin ^c   Edmead, Christine E ^b   Welham, Melanie J ^b   Ward, Stephen G ^a,b  

^a UNIVERSITY OF BATH   (United Kingdom)

^b University of Bath   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; B7 ANTIGEN; CD28 ANTIGEN; GROWTH FACTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PLECKSTRIN; PROTEIN GRB2 ASSOCIATED BINDER 2; PROTEIN TYROSINE PHOSPHATASE SHP 2; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL STIMULATION; CHO CELL; COMPLEX FORMATION; DELETION MUTANT; ENZYME REGULATION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; LEUKEMIA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; T LYMPHOCYTE ACTIVATION;

EID: 29644432549     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.1.594     Document Type: Article

References (60)

1. June, C. H., J. A. Bluestone, L. M. Nadler, and C. B. Thompson. 1994. The B7 and CD28 receptor families, Immunol. Today 15: 321-331.
2. Ward, S. G. 1996. CD28: a signalling perspective. Biochem. J. 318: 361-377.
3. Saito, T., and S. Yamasaki. 2003. Negative feedback of T cell activation through inhibitory adapters and costimulatory receptors, Immunol. Rev. 192: 143-160.
4. Prasad, K. V., Y. C. Cai, M. Raab, B. Duckworth, L. Cantley, S. E. Shoelson, and C. E. Rudd. 1994. 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 91: 2834-2838.
5. Vanhaesebroeck, B., S. J. Leevers, K. Ahmadi, J. Timms, R. Katso, P. C. Driscoll, R. Woscholski. P. J. Parker, and M. D. Waterfield. 2001. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70: 535-602.
6. Cullen, P. J., G. E. Cozier, G. Banting, and H. Mellor. 2001. Modular phosphoinositide-binding domains: their role in signalling and membrane trafficking. Curr. Biol. 11: R882-R893.
7. Dowler, S., R. A. Currie. D. G. Campbell, M. Deak, G. Kular. C. P. Downes. and D. R. Alessi. 2000. Identification of pleckstrin-homology-domain- containing proteins with novel phosphoinositide-binding specificities. Biochem. J. 351: 19-31.
8. DiNitto, J. P., T. C. Cronin, and D. G. Lambright. 2003. Membrane recognition and targeting by lipid-binding domains. Sci. STKE 2003: re16-re19.
9. Togni, M., J. Lindquist, A. Gerber, U. Kölsch, A. Hamm-Baarke, S. Kliche, and B. Schraven. 2004. The role of adaptor proteins in lymphocyte activation. Mol. Immunol. 41: 615-630.
10. Gu, H., and B. G. Neel. 2003. The "Gab" in signal transduction. Trends Cell Biol. 13: 122-130.
11. Nishida, K., and T. Hirano. 2003. The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci. 94: 1029-1033.
12. Isakoff, S. J., T. Cardozo, J. Andreev, Z. Li, K. M. Ferguson, R. Abagyan, M. A. Lemmon, A. Aronheim, and E. Y. Skolnik. 1998. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17: 5374-5387.
13. Rodrigues, G. A., M. Falasca, Z. Zhang, S. H. Ong, and J. Schlessinger. 2000. A novel positive feedback loop mediated by the docking protein Gab 1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell. Biol. 20: 1448-1459.
14. Gu. H., K. Saito, L. D. Klaman, J. Shen, T. Fleming, Y. Wang, J. C. Pratt, G. Lin, B. Lim, J. P. Kinet, and B. G. Neel. 2001. Essential role for Gab2 in the allergic response. Nature 412: 186-190.
15. Itoh, M., Y. Yoshida, K. Nishida, M. Narimatsu, M. Hibi, and T. Hirano. 2000. Role of Gab 1 in heart, placenta, and skin development and growth factor- and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol. Cell. Biol. 20: 3695-3704.
16. Seiffert, M., J. M. Custodio, I. Wolf, M. Harkey, Y. Liu, J. N. Blattman, P. D. Greenberg, and L. R. Rohrschneider. 2003. Gab3-deficient mice exhibit normal development and hematopoiesis and are immunocompetent. Mol. Cell. Biol. 23: 2415-2424.
17. Nishida, K., L. Wang, E. Morii, S. J. Park, M. Narimatsu, S. Itoh, S. Yamasaki, M. Fujishima, K. Ishihara, M. Hibi. et al. 2002. Requirement of Gab2 for mast cell development and KitL/c-Kit signaling. Blood 99: 1866-1869.
18. Nishida, K., Y. Yoshida. M. Itoh. T. Fukada, T. Ohtani, T. Shirogane, T. Atsumi, M. Takahashi-Tezuka, K. Ishihara, M. Hibi, and T. Hirano. 1999. Gab-family adapter proteins act downstream of cytokine and growth factor receptors and T- and B-cell antigen receptors. Blood 93: 1809-1816.
19. Gu, H., J. C. Pratt, S. J. Burakoff, and B. G. Neel. 1998. Cloning of p97/Gab2, the major SHP2-binding protein in hematopoietic cells, reveals a novel pathway for cytokine-induced gene activation. Mol. Cell 2: 729-740.
20. Gadina, M., C. Sudarshan. R. Visconti. Y. J. Zhou, H. Gu, B. G. Neel, and J. J. O'Shea. 2000. The docking molecule Gab2 is induced by lymphocyte activation and is involved in signaling by interleukin-2 and interleukin-15 but not other common γ chain-using cytokines. J. Biol. Chem. 275: 26959-26966.
21. Yamasaki, S., K. Nishida, M. Hibi, M. Sakuma. R. Shiina, A. Takeuchi, H. Ohnishi, T. Hirano, and T. Saito. 2001. Docking protein Gab2 is phosphorylated by ZAP-70 and negatively regulates T cell receptor signaling by recruitment of inhibitory molecules. J. Biol. Chem. 276: 45175-45183.
22. Pratt, J. C., V. E. Igras, H. Maeda, S. Baksh, E. W. Gelfand, S. J. Burakoff, B. G. Neel, and H. Gu. 2000. Cutting edge: Gab2 mediates an inhibitory phosphatidylinositol 3′-kinase pathway in T cell antigen receptor signaling. J. Immunol. 165: 4158-4163.
23. Frearson, J. A., and D. R. Alexander. 1998. The phosphotyrosine phosphatase SHP-2 participates in a multimeric signaling complex and regulates T cell receptor (TCR) coupling to the Ras/mitogen-activated protein kinase (MAPK) pathway in Jurkat T cells. J. Exp. Med. 187: 1417-1426.
24. Ward, S. G., A. Wilson, L. Turner, J. Westwick, and D. M. Sansom. 1995. Inhibition of CD28-mediated T cell costimulation by the phosphoinositide 3-kinase inhibitor wortmannin. Eur. J. Immunol. 25: 526-532.
25. Gu, H., H. Maeda, J. J. Moon, J. D. Lord, M. Yoakim, B. H. Nelson, and B. G. Neel. 2000. New role for She in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol. Cell. Biol. 20: 7109-7120.
26. Craddock, B. L., and M. J. Welham. 1997. Interleukin-3 induces association of the protein-tyrosine phosphatase SHP2 and phosphatidylinositol 3-kinase with a 100-kDa tyrosine-phosphorylated protein in hemopoietic cells. J. Biol. Chem. 272: 29281-29289.
27. Welham, M. J., V. Duronio, and J. W. Schrader. 1994. Interleukin-4- dependent proliferation dissociates p44erk-1, p42erk-2, and p21ras activation from cell growth. J. Biol. Chem. 269: 5865-5873.
28. Craddock, B. L., E. A. Orchiston, H. J. Hinton, and M. J. Welham. 1999. Dissociation of apoptosis from proliferation, protein kinase B activation, and BAD phosphorylation in interleukin-3-mediated phosphoinositide 3-kinase signaling. J. Biol. Chem. 274: 10633-10640.
29. Ward, S. 2000. Measurement of phosphoinositide 3-kinase activity. Methods Mol. Biol. 138: 163-172.
30. Nunes, J. A., Y. Collette, A. Truneh, D. Olive, and D. A. Cantrell. 1994. The role of p21ras in CD28 signal transduction: triggering of CD28 with antibodies, but not the ligand B7-1, activates p21ras. J. Exp. Med. 180: 1067-1076.
31. Carlberg, K., and L. R. Rohrschneider. 1997. Characterization of a novel tyrosine phosphorylated 100-kDa protein that binds to SHP-2 and phosphatidylinositol 3′-kinase in myeloid cells. J. Biol. Chem. 272: 15943-15950.
32. Gu, H.. J. D. Griffin, and B. G. Neel. 1997. Characterization of two SHP-2-associated binding proteins and potential substrates in hematopoietic cells. J. Biol. Chem. 272: 16421-16430.
33. McGuire, K. L., and M. Iacobelli. 1997. Involvement of Rel, Fos, and Jun proteins in binding activity to the IL-2 promoter CD28 response element/AP-1 sequence in human T cells. J. Immunol. 159: 1319-1327.
34. Astoul, E., C. Edmunds, D. A. Cantrell, and S. G. Ward. 2001. PI3K and T cell activation: limitations of leukemic cell lines as signalling molecules. Trends Immunol 22: 490-496.
35. Freeburn, R. W., K. L. Wright, S. J. Burgess, E. Astoul, D. A. Cantrell, and S. G. Ward. 2002. 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. 169: 5441-5450.
36. Thompson, C. B., T. Lindsten, J. A. Ledbetter, S. L. Kunkel, H. A. Young, S. G. Emerson, J. M. Leiden, and C. H. June. 1989. CD28 activation pathway regulates the production of multiple T-cell-derived lymphokines/cytokines. Proc. Natl. Acad. Sci. USA 86: 1333-1337.
37. Fraser, J. D., B. A. Irving, G. R. Crabtree, and A. Weiss. 1991. Regulation of interleukin-2 gene enhancer activity by the T cell accessory molecule CD28. Science 251: 313-316.
38. Shapiro, V. S., K. E. Truitt, J. B. Imboden, and A. Weiss. 1997. CD28 mediates transcriptional up-regulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF-IL-2B AP-1 sites. Mol. Cell. Biol. 17: 4051-4058.
39. Wilkinson, B., H. Wang, and C. E. Rudd. 2004. Positive and negative adaptors in T-cell signalling. Immunology 111: 368-374.
40. Zhao, C., D. H. Yu, R. Shen, and G. S. Feng. 1999. Gab2, a new pleckstrin homology domain-containing adapter protein, acts to uncouple signaling from ERK kinase to Elk-1. J. Biol. Chem. 274: 19649-19654.
41. Zhu, Q. S., L. J. Robinson, V. Roginskaya, and S. J. Corey. 2004. G-CSF-induced tyrosine phosphorylation of Gab2 is Lyn kinase dependent and associated with enhanced Akt and differentiative, not proliferative, responses. Blood 103: 3305-3312.
42. 1-integrin signaling pathway-mediated hematopoietic cell adhesion and migration. Blood 99: 2351-2359.
43. Podar, K., G. Mostoslavsky, M. Sattler, Y. T. Tai, T. Hayashi, L. P. Catley, T. Hideshima, R. C. Mulligan, D. Chauhan, and K. C. Anderson. 2004. Critical role for hematopoietic cell kinase (Hck)-mediated phosphorylation of Gab1 and Gab2 docking proteins in interleukin 6-induced proliferation and survival of multiple myeloma cells. J. Biol. Chem. 279: 21658-21665.
44. Liu, Y., B. Jenkins, J. L. Shin, and L. R. Rohrschneider. 2001. Scaffolding protein Gab2 mediates differentiation signaling downstream of Fms receptor tyrosine kinase. Mol. Cell. Biol. 21: 3047-3047.
45. Xie, Z. H., I. Ambudkar, and R. P. Siraganian. 2002. The adapter molecule Gab2 regulates FcεRI-mediated signal transduction in mast cells. J. Immunol. 168: 4682-4691.
46. Arnaud, M., R. Mzali, F. Gesbert, C. Crouin, C. Guenzi, C. Vermot-Desroches, J. Wijdenes, G. Courtois, O. Bernard, and J. Bertoglio. 2004. Interaction of the tyrosine phosphatase SHP-2 with Gab2 regulates Rho-dependent activation of the c-fos serum response element by interleukin-2. Biochem. J. 382: 545-556.
47. Ward, S. G., C. H. June, and D. Olive. 1996. PI 3-kinase: a pivotal pathway in T cell activation, Immunol. Today 17: 187-197.
48. Harada, Y., M. Tokushima, Y. Matsumoto, S. Ogawa, M. Otsuka, K. Hayashi, B. Weiss, C. H. June, and R. Abe. 2001. Critical requirement for the membrane proximal cytosolic tyrosine residue for CD28-mediated costimulation in vivo. J. Immunol. 166: 3797-3803.
49. Okkenhaug, K., L. Wu, K. M. Garza, J. La Rose, W. Khoo, B. Odermatt, T. W. Mak, P. S. Ohashi, and R. Rottapel. 2001. A point mutation in CD28 distinguishes proliferative signals from survival signals. Nat. Immunol. 2: 325-332.
50. Andres P. G., K. C. Howland, A. Nirula, L. P. Kane, L. Barron, D. Dresnek, A. Sadra, J. Imboden, A. Weiss, and A. K. Abbas. 2004. Distinct regions in the CD28 cytoplasmic domain are required for T helper type 2 differentiation. Nat. Immunol. 5: 435-442.
51. L. J. Immunol. 166: 5331-5335.
52. Reif, K., S. Lucas, and D. Cantrell. 1997. A negative role for phosphoinositide 3-kinase in T-cell antigen receptor function. Curr. Biol. 7: 285-293.
53. Lynch, D. K., and R. J. Daly. 2002. PKB-mediated negative feedback tightly regulates mitogenic signalling via Gab2. EMBO J. 21: 72-82.
54. Parry, R. V., D. Olive, J. Westwick, D. M. Sansom, and S. G. Ward. 1997. Evidence that a kinase distinct from protein kinase C and phosphatidylinositol 3-kinase mediates ligation-dependent serine/threonine phosphorylation of the T-lymphocyte co-stimulatory molecule CD28. Biochem. J. 326: 249-257.
55. Reif, K., I. Gout, M. D. Waterfield, and D. A. Cantrell. 1993. Divergent regulation of phosphatidylinositol 3-kinase p85α and p85β isoforms upon T cell activation. J. Biol. Chem. 268: 10780-10788.
56. Ward, S. G. 1996. Phosphoinositide 3-kinase and CD28-mediated T-cell co-stimulation. Biochem. Soc. Trans. 24: 240-245.
57. Ueda, Y., B. L. Levine, M. L. Huang, G. J. Freeman, L. M. Nadler, C. H. June, and S. G. Ward. 1995. Both CD28 ligands CD80 (B7-1) 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.
58. Edmead, C. E., B. C. Fox, C. Stace, N. Ktistakis, and M. J. Welham. 2006. The pleckstrin homology domain of Gab-2 is required for optimal interleukin-3 signalsome-mediated responses. Cell Signal. In press.
59. Pluskey, S., T. J. Wandless, C. T. Walsh, and S. E. Shoelson. 1995. Potent stimulation of SH-PTP2 phosphatase activity by simultaneous occupancy of both SH2 domains. J. Biol. Chem. 270: 2897-2900.
60. Hof, P., S. Pluskey, S. Dhe-Paganon, M. J. Eck, and S. E. Shoelson. 1998. Crystal structure of the tyrosine phosphatase SHP-2. Cell 92: 441-450.