The SH3 Domain of Itk/Emt Binds to Proline-Rich Sequences in the Cytoplasmic Domain of the T Cell Costimulatory Receptor CD28

Journal of Immunology

Volumn 159, Issue 7, 1997, Pages 3220-3229

  Marengère, Luc E M ^a,c   Okkenhaug, Klaus ^b,d   Clavreul, Anne ^e   Couez, Dominique ^e   Gibson, Spencer ^f   Mills, Gordon B ^f   Mak, Tak W ^a,c   Rottapel, Robert ^b,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c AMGEN INSTITUTE   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

^e INSERM   (France)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; DIPEPTIDE; EMT PROTEIN TYROSINE KINASE; EMT PROTEIN-TYROSINE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE 11; MIXED LINEAGE KINASE 3; PEPTIDE; PROLINE; PROLINE RICH PROTEIN; PROLINE-RICH POLYPEPTIDE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TUMOR PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL CULTURE; CHEMISTRY; CYTOPLASM; ENZYMOLOGY; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MACROMOLECULE; METABOLISM; MOLECULAR GENETICS; MOUSE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; SRC HOMOLOGY DOMAIN; THYMOMA;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD28; CYTOPLASM; DIPEPTIDES; HUMANS; LYMPHOCYTE ACTIVATION; MACROMOLECULAR SUBSTANCES; MAP KINASE KINASE KINASES; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NEOPLASM PROTEINS; PEPTIDES; PHOSPHORYLATION; PROLINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SRC HOMOLOGY DOMAINS; THYMOMA; TUMOR CELLS, CULTURED;

EID: 0031255110     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Bluestone, J. A. 1995. New perspectives of CD28-B7-mediated T cell costimulation. Immunity 2:555.
2. Linsley, P. S., and J. A. Ledbetter. 1993. The role of the CD28 receptor during T cell responses to antigen. Annu. Rev. Immunol. 11:191.
3. Schwartz, R. H. 1992. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 71: 1065.
4. Aruffo, A., and B. Seed. 1987. Molecular cloning of a CD28 cDNA by a high efficiency COS cell expression system. Proc. Natl. Acad. Sci. USA 84:8573.
5. Harding, F. A., J. G. McArthur, J. A. Gross, D. H. Daulet, and J. P. Allison. 1992. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356:607.
6. Jenkins, M. K., and R. H. Schwartz. 1987. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J. Exp. Med. 165:302.
7. Schwartz, R. H. 1991. A cell culture model of T lymphocyte clonal anergy. Science 248:1349.
8. Chan, A. C., B. A. Irving, J. D. Fraser, and A. Weiss. 1991. The zeta chain is associated with a tyrosine kinase and upon T-cell antigen receptor stimulation associates with ZAP-70, a 70-kDa tyrosine phosphoprotein. Proc. Natl. Acad. Sci. USA 88:9166.
9. Rudd, C. E., J. M. Trevillyan, J. D. Dasgupta, L. L. Wong, and S. F. Schlossman. 1988. The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc. Natl. Acad. Sci. USA 85:5190.
10. Samelson, L. E., A. F. Philips, E. T. Luong, and R. D. Klausner. 1990. Association of the Fyn protein-tyrosine kinase with the T-cell antigen receptor. Proc. Natl. Acad. Sci. USA 87:4358.
11. fyn. Cell 70:751.
12. LcK. Nature 357:161.
13. Fyn mutant mice display differential signalling in lhymocytes and peripheral T cells. Cell 70: 741.
14. Negishi I., N. Motoyama, K. Nakayama, K. Nakayama, S. Senju, S. Hatakeyama, Q. Zhang, A. C. Chan, and D. Y. Loh. 1995. Essential role for ZAP-70 in both positive and negative selection of thymocytes. Nature 376:435.
15. August, A., S. Gibson, Y. Kawakami, T. Kawakami, G. B. Mills, and B. Dupont. 1994. 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 91:9347.
16. Lu, Y., A. Granelli-Piperno, J. M. Bjorndahl, C. A. Phillips, and J. M. Trevillyan. 1992. CD28-induced T cell activation: evidence for a protein-tyrosine kinase signal transduction pathway. J. Immunol. 149:24.
17. Pages, F., M. Ragueneau, R. Rottapel, A. Truneh, J. Nunes, J. Imbert, and D. Olive. 1994. Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 369:327.
18. Prasad, K. V. S., 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.
19. Stein, P. H., J. D. Fraser, and A. Weiss. 1994. The cytoplasmic domain of CD28 is both necessary and sufficient for costimulation of interleukin-2 secretion and association with phosphatidylinositol 3′-kinase. Mol. Cell. Biol. 14:3392.
20. Siliciano, J. D., T. A. Morrow, and S. V. Desiderio. 1992. itk, a T-cell-specific tyrosine kinase gene inducible by interleukin-2. Proc. Natl. Acad. Sci. USA 89: 11194.
21. Gibson, S., B. Leung, J. Squire, M. Hill, N. Arima, P. Goss, D. Hogg, and G. Mills. 1993. Identification, cloning, and characterization of a novel human T-cell-specific tyrosine kinase located at the hematopoietin complex on chromosome 5q. Blood 82:1561.
22. Heyeck, S. D., and L. J. Berg. 1993. Developmental regulation of a murine T-cell-specific tyrosine kinase gene, Tsk. Proc. Natl. Acad. Sci. USA 90:669.
23. Couez, D., F. Pages, M. Ragueneau, J. Nunes, S. Klasen, C. Mawas, A. Truneh, and D. Olive. 1994. Functional expression of human CD28 in murine T cell hybridomas. Mol. Immunol. 31:47.
24. Hutchcroft, J. E., D. P. Franklin, B. Tsai, D. Harrison-Findik, L. Varticovski, and B. E. Bierer. 1995. Phorbol ester treatment inhibits phosphatidylinositol 3-kinase activation by, and association with, CD28, a T-lymphocyte surface receptor. Proc. Natl. Acad. Sci. USA 92:8808.
25. Gibson, S., A. August, D. Branch, B. Dupont, and G. M. Mills. 1996. Functional LCK is required for optimal CD28-mediated activation of the TEC family tyrosine kinase EMT/ITK. J. Biol. Chem. 271:7079.
26. Marengere, L. E. M., Z. Songyang, G. D. Gish, M. D. Schaller, J. T. Parsons, M. J. Stern, L. C. Cantley, and T. Pawson. 1994. SH2 domain specificity and activity modified by a single residue. Nature 369:502.
27. August, A., and B. Dupont. 1994. Activation of src family kinase lck following CD28 cross-linking in the Jurkal leukemic cell line. Biochem. Biophys. Res. Com-mun. 199:1466.
28. Hutchcroft, J. E., and B. E. Bierer. 1994. Activation-dependent phosphorylation of the T-lymphocyte surface receptor CD28 and associated proteins. Proc. Natl. Acad. Sci. USA 91:3260.
29. King, P. D., A. Sadra, J. M. Teng, R. L. Xiao, A. Han, A. Selvakumar, A. August, and B. Dupont. 1997. Analysis of CD28 cytoplasmic tail tyrosine residues as regulators and substrates for the protein tyrosine kinases, EMT and LCK. J. Immunol. 158:580.
30. Fyn regulate CD28 binding to phosphatidylinositol 3-kinase, growth factor receptor-bound protein GRB-2, and T cell-specific prolein-tyrosine kinase ITK: implications for T-cell costimulation. Proc Natl. Acad. Sci. USA 92:8891.
31. Kapeller, R., K. V. Prasad, O. Jansen, W. Hou, B. S. Schaffhausen, C. E. Rudd, and L. C. Cantley. 1994. Identification of two SH3-binding motifs in the regulatory subunit of phosphatidylinositol 3′-kinase. J. Biol. Chem. 269:1927.
32. Karnitz, L. M., S. L. Sutor, and R. T. Abraham 1994. The Src-family kinase, Fyn, regulates the activation of phosphatidylinositol 3-kinase in an interleukin 2-responsive line. J. Exp. Med. 179:1799.
33. Liu, X., L. M. Marengere, C. A. Koch, and T. Pawson. 1993. The v-Src SH3 domain binds phosphatidylinositol 3′-kinase. Mol. Cell. Biol 11:2511.
34. Chen, J. K., W. S. Lane, A. W. Brauer, A. Tanaka, and S. L. Schreiber. 1993. Biased combinatorial libraries: novel ligands for the SH3 domain of phosphatidylinositol 3′-kinase. J. Am. Chem. Soc. 115:12591.
35. Yu, H., J. K. Chen, S. Feng, D. C. Dalgarno, A. W. Brauer, and S. L. Schreiber. 1994. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76:933.
36. Bunnell, S. C., P. A. Henry, R. Kolluri, T. Kirchhausen, R. J. Rickles, and L. J. Berg. 1996. Identification of Itk/Tsk Src homology 3 domain ligands. J. Biol. Chem. 271:25646.
37. c-src. Mol. Cell. Biol. 10:1307.
38. Jackson, P., and D. Baltimore. 1989. N-terminal mutations activate the leukemogenic potential of the myristoylated form of c-abl. EMBO J. 8:449.
39. Mayer, B. J., and D. Baltimore. 1994. Mutagenic analysis of the roles of SH2 and SH3 domains in regulation of the Abl tyrosine kinase. Mol. Cell. Biol. 14:2883.
40. Okada, M., B. W. Howell, M. A. Broome, and J. A. Cooper. 1993. Deletion of the SH3 domain of Src interferes with regulation by the phosphorylated carboxyl-terminal tyrosine. J. Biol. Chem. 268:18070.
41. Seidel-Dugan, C., B. E. Meyer, S. M. Thomas, and J. S. Brugge. 1992. Effects of SH2 and SH3 deletions on the functional activities of wild-type and transforming variants of c-Src. Mol. Cell. Biol. 12:1835.
42. Boussiotis, V. A., D. L. Barber, B. J. Lee, J. G. Gribben, G. J. Freeman, and L. M. Nadler. 1996. Differential association of protein tyrosine kinases with the T cell receptor is linked to the induction of anergy and its prevention by B7 family-mediated costimulation. J. Exp. Med. 184:365.
43. Campbell, M. A., and B. M. Sefton. 1992. Association between B-lymphocyte membrane immunoglobulin and multiple members of the Src family of protein tyrosine kinases. Mol. Cell. Biol. 12:2315.
44. Burkhardt, A. L., M. Brunswick, J. B. Bolen, and J. J. Mond. 1991. Anti-immu-noglobulin stimulation of B lymphocytes activates .vrr-rclated prolein-tyrosine kinases. Proc. Natl. Acad. Sci. USA 88:7410.
45. Yamanashi, Y., T. Kakiuchi, J. Mizuguchi, T. Yamamoto, and K. Toyoshima. 1991. Association of B cell antigen receptor with protein lyrosine kinase Lyn. Science 251:192.
46. lck. Cell 55:301.
47. Narazaki, M., B. A. Witthuhn, K. Yoshida, O. Silvennoinen, K. Yasukawa, J. N. Ihle, T. Kishimoto, and T. Taga. 1994. Activation of Jak2 kinase mediated by the IL-6 signal transducer, gp130. Proc. Natl. Acad. Sci. USA 91:2285.
48. Schaller, M. D., C. A. Borgman, B. S. Cobb, R. R. Vines, A. B. Reynolds, and J. T. Parsons. 1992. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89:5192.
49. Springer, T. A., M. L. Dustin, T. K. Kishimoto, and S. D. Marlin. 1987. The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system. Annu. Rev. Immunol. 5:233.
50. Bierer, B., A. Peterson, J. C. Gorga, S. H. Herman, and S. J. Burakoff. 1988. Synergistic T cell activation via the physiological ligands for CD2 and the T cell receptor. J. Exp. Med. 168:1145.
51. lck binds to proline-rich sequences in the cytoplasmic domain of CD2. J. Exp. Med. 183:169.
52. Xu, W., S. C. Harrison, and M. J. Eck. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385:595.
53. Sichert, F., I. Moarefi, and J. Kuriyan. 1997. Crystal structure of the Src family tyrosine kinase Hck. Nature 385:602.
54. c-src. Nature 351:69.
55. Cooper, J. A., and B. Howell. 1993. The when and how of Src regulation. Cell 73:1051.
56. Andreoui, A. H., S. C. Bunnell, S. Feng, L. J. Berg, and S. L. Schreiber 1997. Regulatory intramolecular association in a tyrosine kinase of the Tec family. Nature 385:93.
57. Moarefi, I., M. LaFevre-Bernt, F. Sicheri, M. Huse, C. H. Lee, J. Kuriyan, and W. T. Miller. 1997. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385:650.
58. Yang, W., S. N. Malek, and S. Desiderio. 1995. An SH3-binding site conserved in Bruton's tyrosine kinase and related tyrosine kinase mediates specific protein interactions in vitro and in vivo. J. Biol. Chem. 270:20832.
59. Park, H., M. I. Wahl, D. E. H. Afar, C. W. Turck, D. J. Rawlings, C. Tam, A. M. Scharenberg, J. Kinet, and O. N. Witte. 1996. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity 4:515.
60. Mahajan, S., J. Fargnoli, A. L. Burkhardt, S. A. Kut, S. J. Saouaf, and J. B. Bolen. 1995. Src family protein tyrosine kinases induce autoactivation of Bruton's tyrosine kinase. Mol. Cell. Biol. 15:5304.
61. Saouaf, S. J., S. A. Kut, J. Fargnoli, R. B. Rowley, J. B. Bolen, and S. Mahajan. 1995. Reconstitution of the B cell antigen receptor signaling components in COS cells. J. Biol. Chem. 270:27072.
62. Saouaf, S. J., S. Mahajan, R. B. Rowley, S. Kut, J. Fargnoh, A. L. Burkhardt, S. Tsukada, O. N. Witte, and J. B. Bolen. 1994. Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinase following B cell antigen receptor surface engagement. Proc. Natl. Acad. Sci. USA 91:9524.
63. Rawlings, D. J., A. M. Scharenberg, H. Park, M. I. Wahl, S. Lin, R. M. Kato, A. Fluckiger, O. N. Witte, and J. Kinet. 1996. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science 271:822.
64. Salim, K., M. J. Bottomley, E. Querfurth, M. J. Zvelebil, I. Gout, R. Scaife, R. L. Margolis, R. Gigg, C. I. E. Smith, P. C. Driscoll, M. D. Waterfield, and G. Panayotou. 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15:6241.
65. Franke, T. F., D. R. Kaplan, L. C. Cantley, and A. Toker. 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3, 4-biosphate. Science 275:665.