SLP-76 binding to p56(lck): A role for SLP-76 in CD4-induced desensitization of the TCR/CD3 signaling complex

Journal of Immunology

Volumn 163, Issue 6, 1999, Pages 3143-3152

  Sanzenbacher, Ralf ^a   Kabelitz, Dieter ^a   Janssen, Ottmar ^a,b  

^a PAUL EHRLICH INSTITUT   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; T LYMPHOCYTE RECEPTOR;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DESENSITIZATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIBODIES, MONOCLONAL; ANTIGENS, CD4; BINDING SITES; CLONE CELLS; HUMANS; KINETICS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MODELS, BIOLOGICAL; ONCOGENE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-VAV; RECEPTOR-CD3 COMPLEX, ANTIGEN, T-CELL; SRC HOMOLOGY DOMAINS; T-LYMPHOCYTES; TYROSINE;

EID: 0033568459     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. Russell, J., C. L. White, D. Y. Loh, and P. Meleedy-Rey. 1992. Receptor-stimulated death pathway is opened by antigen in mature T cells. Proc. Natl. Acad. Sci. USA 88:2151.
2. + T cells. J. Immunol. 146:35.
3. + antigen-presenting cells. Int. Immunol. 4:1381.
4. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267:1449.
5. Dhein, J., H. Walczak, C. Baeumler, K. M. Debatin, and P. H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373:438.
6. Brunner, T., R. J. Mogil, D. LaFace, N. J. Yoo, A. Mahboubi, F. Echeverri, S. J. Martin, W. R. Force, D. H. Lynch, C. F. Ware, and D. R. Green. 1995. Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373:441.
7. Ju, S. T., D. J. Panka, H. Cui, R. Ettinger, M. el-Khatib, D. H. Sherr, B. Z. Stanger, and A. Marshak-Rothstein. 1995. Fas(CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 373:444.
8. Alderson, M. R., T. W. Tough, T. Davis-Smith, S. Braddy, B. Falk, K. A. Schooley, R. G. Goodwin, C. A. Smith, F. Ramsdell, and D. H. Lynch. 1995. Fas ligand mediates activation-induced cell death in human T lymphocytes. J. Exp. Med. 181:71.
9. Radvanyi, L. G., Y. Shi, H. Vaziri, A. Sharma, R. Dhala, G. B. Mills, and R. G. Miller. 1996. CD28 costimulation inhibits TCR-induced apoptosis during a primary T cell response. J. Immunol. 156:1788.
10. + T cells from human immunodeficiency virus-infected asymptomatic individuals. J. Exp. Med. 175:331.
11. Oberg, H.-H., R. Sanzenbacher, B. Lengl-Janßen, T. Dobmeyer, S. Flindt, O. Janssen, and D. Kabelitz. 1997. Ligation of cell surface CD4 inhibits activation-induced cell death of human T lymphocytes at the level of Fas-ligand expression. J. Immunol. 159:5742.
12. Katzav, S., D. Martin-Zanca, and M. Barbacid. 1989. Vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells. EMBO J. 8:2283.
13. vav associates with tyrosine-phosphorylated SLP-76 in antigen-stimulated T cells. J. Exp. Med. 184:1161.
14. Jackman, J. K., D. G. Motto, Q. Sun, M. Tanemoto, C. W. Turck, G. A. Peltz, G. A. Koretzky, and P. R. Findell. 1995. Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 in T cells. J. Biol. Chem. 270: 7029.
15. Motto, D. G., S. E. Ross, J. Wu, L. R. Hendricks-Taylor, and G. A. Koretzky. 1996. Implication of the Grb2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J. Exp. Med. 183:1937.
16. Pivniouk, V., E. Tsitsikov, P. Swinton, G. Rathbun, F. W. Alt, and R. S. Geha. 1998. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell 94:229.
17. Clements, J. L., B. Yang, S. E. Ross-Barta, S. L. Eliason, R. F. Hrstka, R. A. Williamson, and G. A. Koretzky. 1998. Requirement for the leukocyte-specific adapter protein SLP-76 for normal T cell development. Science 281:416.
18. Yablonski, D., M. R. Kuhne, T. Kadlecek, and A. Weiss. 1998. Uncoupling of nonreceptor tyrosine kinases from PLCγ1 in a SLP-76-deficient T cell. Science 281:413.
19. Wienands, J., J. Schweikert, B. Wollscheid, H. Jumaa, P. J. Nielsen, and M. Reth. 1998. SLP-65: a new signaling component in B lymphocytes which requires expression of the antigen receptor for phosphorylation. J. Exp. Med. 188:791.
20. Fu, C., C. W. Turck, T. Kurosaki, and A. C. Chan. 1998. BLNK: a central linker protein in B cell activation. Immunity 9:93.
21. fyn mediates binding to phosphatidylinositol 3-kinase in T cells. Proc. Natl. Acad. Sci. USA 90:7366.
22. lck SH3 domain mediates binding to PI-3 kinase but not to PI-4 kinase. Mol. Cell. Biol. 13:7708.
23. Wu, J., D. G. Motto, G. A. Koretzky, and A. Weiss. 1996. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4:593.
24. Wardenburg, J. B., C. Fu, J. K. Jackman, H. Flotow, S. E. Wilkinson, D. H. Williams, R. Johnson, G. Kong, A. C. Chan, and P. R. Findell. 1996. Phosphorylation of SLP-76 by the ZAP-70 protein tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271:19641.
25. Raab, M., A. J. da Silva, P. R. Findell, and C. E. Rudd. 1997. Regulation of Vav-SLP-76 binding by ZAP-70 and its relevance to TCRζ/CD3 induction of interleukin-2. Immunity 6:155.
26. Musci, M. A., D. G. Motto, S. E. Ross, N. Fang, and G. A. Koretzky. 1997. Three domains of SLP-76 are required for its optimal function in a T cell line. J. Immunol. 159:1639.
27. Koretzky, G. A. 1997. The role of Grb2-associated proteins in T cell activation. Immunol. Today 8:401.
28. Ren, R., B. J. Mayer, P. Cicchetti, and D. Baltimore. 1993. Identification of a ten-amino acid proline-rich SH3 binding site. Science 259:1157.
29. 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.
30. Blake, T. J., M. Shapiro, H. C. Morse III, and W. Y. Langdon. 1991. The sequences of the human and mouse c-cbl protooncogenes show v-cbl was generated by a large truncation encompassing a proline-rich domain and a leucine zipper-like motif. Oncogene 6:653.
31. Fukazawa, T., K. A. Reedquist, T. Trub, S. Soltoff, G. Panchamoorthy, B. Druker, L. Cantley, S. E. Schoelson, and H. Band. 1995. The SH3 domain-binding T cell tyrosyl phosphoprotein p120: demonstration of its identity with the c-cbl protooncogene product and in vivo complexes with Fyn, Grb-2 and phosphatidylinositol 3-kinase. J. Biol. Chem. 270:19141.
32. Taylor, S. J., and D. Shalloway. 1994. An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature 368:867.
33. Fumagalli, S., N. F. Totty, J. J. Hsuan, and S. A. Courtneidge. 1994. A target for Src in mitosis. Nature 368:871.
34. Lock, P., S. Fumagalli, P. Polakis, F. McCormick, and S. A. Courtneidge. 1996. The human p62 cDNA encodes Sam68 and not the RasGAP-associated p62 protein. Cell 84:23.
35. Rudd, C. E., O. Janssen, Y.-C. Cai, A. J. da Silva, M. Raab, and K. V. S. Prasad. 1994 Two-step TCRζ/CD3-CD4 and CD28 signaling in T cells: SH2/SH3 domains, protein-tyrosine kinases and lipid kinases. Immunol. Today 15:225.
36. Alberola-Ila, J., S. Takaki, J. D. Kerner, and R. Perlmutter. 1997. Differential signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 15:125.
37. lck in T-cell receptor/CD3-mediated apoptosis and Fas-ligand induction in Jurkat cells. Biochem. Biophys. Res. Commun. 213:994.
38. lck plays a key role in transducing apoptotic signals in T cells. FEBS Lett. 363:101.
39. Gonzalez-Garcia, A., L. R.-Borlado, E. Leonardo, I. Mérida, C. Martinez-A., and A. C. Carrera. 1997. Lck is necessary and sufficient for Fas-ligand expression and apoptotic cell death in mature cycling T cells. J. Immunol 158:4104.
40. June, C. H., M. C. Fletcher, J. A. Ledbetter, G. L. Schieven, J. N. Siegel, A. F. Phillips, and L. E. Samelson. 1990. Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction. Proc. Natl. Acad. Sci. USA 87:7722.
41. Migita, K., K. Eguchi, Y. Kawabe, A. Mizokami, T. Tsukada, and S. Nagataki. 1994. Prevention of anti-CD3 monoclonal antibody-induced thymic apoptosis by protein tyrosine kinase inhibitors. J. Immunol. 153:3457.
42. Oberg, H.-H., B. Lengl-Janßen, M. J. Robertson, D. Kabelitz, and O. Janssen. 1997. Differential role of tyrosine phosphorylation in the induction of apoptosis in T cell clones via CD95 or the TCR/CD3-complex. Cell Death Differ. 4:403.
43. Collins, T. L., M. Deckert, and A. Altman. 1997. Views on Vav. Immunol. Today 18:221.
44. Bustelo, X. R., J. A. Ledbetter, and M. Barbacid. 1992. Product of vav protooncogene defines a new class of tyrosine protein kinase substrates. Nature 356:68.
45. Margolis, B., P. Hu, S. Katzav, W. Li, J. M. Oliver, A. Ullrich, A. Weiss, and J. Schlessinger. 1992. Tyrosine phosphorylation of vav protooncogene product containing SH2 domain and transcription factor motifs. Nature 356:71.
46. Jabado, N., A. Pallier, F. Le Deist, F. Bernard, A. Fischer, and C. Hivroz. 1997. CD4 ligands inhibit the formation of multifunctional transduction complexes involved in T cell activation. J. Immunol. 158:94.
47. lck by gp120, a model for TCR desensitization. J. Immunol. 158:2017.
48. Onodera, H., D. G. Motto, G. A. Koretzky, and D. M. Rothstein. 1996. Differential regulation of activation-induced tyrosine phosphorylation and recruitment of SLP-76 to Vav by distinct isoforms of the CD45 protein-tyrosine phosphatase. J. Biol. Chem. 271:22225.
49. Musci, M. A., L. R. Hendricks-Taylor, D. G. Motto, M. Paskind, J. Kamens, C. W. Turck, and G. A. Koretzky. 1997. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272:11674.
50. da Silva, A. J., Z. Li, C. De Vera, E. Canto, P. Findell, and C. E. Rudd. 1997. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production. Proc. Natl. Acad. Sci. USA 94:7493.
51. Clements, J. L., S. E. Ross-Barta, L. T. Tygrett, T. J. Waldschmidt, and G. A. Koretzky. 1998. SLP-76 expression is restricted to hemopoietic cells of monocyte, granulocyte, and T lymphocyte lineage and is regulated during T cell maturation and activation. J. Immunol. 161: 3880.
52. Feng, S., J. K. Cheng, H. Yu, J. A. Simon, and S. L. Schreiber. 1994. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266:1241.
53. Lim, W. A., F. M. Richards, and R. O. Fox. 1994. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 372:375.
54. Morton, C. J., D. J. R. Pugh, E. L. J. Brown, J. D. Kahmann, D. A. C. Renzoni, and I. D. Campbell. 1996. Solution structure and peptide binding of the SH3 domain from human fyn. Structure 4:705.
55. lck tyrosine kinase. J. Biomol. NMR 8:105.
56. Ledbetter, J. A., C. H. June, P. S. Rabinovitch, A. Grossmann, T. T. Tsu, and J. B. Imboden. 1988. Signal transduction through CD4 receptors: stimulatory vs inhibitory activity is regulated by CD4 proximity to the CD3/TCR receptor. Eur. J. Immunol. 18:525.
57. Farber, D. L., M. Luqman, O. Acuto, and K. Bottomly. 1995. Control of memory CD4 T cell activation: MHC class II molecules on APCs and CD4 ligation inhibit memory but not naive CD4 T cells. Immunity 2:249.
58. + cells by CD4. Science 249: 1558.
59. Cruikshank, W. W., D. M. Center, N. Nisar, M. Wu, B. Natke, A. C. Theodore, and H. Kornfeld. 1994. Molecular and functional analysis of a lymphocyte chemoattractant factor: association of biologic function with CD4 expression. Proc. Natl. Acad. Sci. USA 91:5109.
60. Center, D. M., H. Kornfeld, and W. W. Cruikshank. 1996. Interleukin 16 and its function as a CD4 ligand. Immunol. Today 17:476.
61. Cruikshank, W. W., K. Lim, A. C. Theodore, J. Cook, G. Fine, P. F. Weller, and D. M. Center. 1996. IL-16 inhibition of CD3-dependent lymphocyte activation and proliferation. J. Immunol. 157:5240.
62. Baier, M., A. Werner, N. Bannert, K. Metzner, and R. Kurth. 1995. HIV suppression by interleukin-16. Nature 378:563.
63. + cells transfected with IL-16 cDNA are resistant to HIV-1 infection: inhibition of mRNA expression. Nat. Med. 3:659.
64. Idziorek, T., J. Khalife, O. Billaut-Mulot, E. Hermann, M. Aumencier, Y. Mouton, A. Capron, and G. M. Bahr. 1998. Recombinant human IL-16 inhibits HIV-1 replication and protects against activation-induced cell death (AICD). Clin. Exp. Immunol. 112:84.
65. Anderson, P., M.-L. Blue, C. Morimoto, and S. F. Schlossman. 1987. Cross-linking of T3 (CD3) with T4 (CD4) enhances the proliferation of resting T lymphocytes. J. Immunol. 139:678.
66. Oravecz, T., and M. A. Norcross. 1993. Costimulatory properties of the human CD4 molecule: enhancement of CDS-induced T cell activation by human immunodeficiency virus type 1 through viral envelope glycoprotein gp120. AIDS Res. Hum. Retroviruses 9:945.
67. Newell, M. K., L. J. Haughn, C. R. Maroun, and M. H. Julius. 1990. Death of mature T cells by separate ligation of CD4 and the T cell receptor for antigen. Nature 347:286.
68. Banda, N. K., J. Bernier, D. K. Kurahara, R. Kurrle, N. Haigwood, R.-P. Sekaly, and T. H. Finkel. 1992. Cross-linking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J. Exp. Med. 176:1099.
69. Choy, E. H. S., J. Adjave, L. Forrest, G. H. Kingsley, and G. S. Panayi. 1993. Chimeric anti-CD4 monoclonal antibody cross-linked by monocyte Fcγ receptor mediates apoptosis of human CD4 lymphocytes. Eur. J. Immunol. 23:2676.
70. Algeciras, A., D. H. Dockrell, D. H. Lynch, and C. V. Paya. 1998. CD4 regulates susceptibility to Fas ligand- and tumor necrosis factor-mediated apoptosis. J. Exp. Med. 187:711.
71. Oyaizu, N., T. W. McCloskey, M. Coronesi, N. Chirmule, V. S. Kalyanaraman, and S. Pahwa. 1993. Accelerated apoptosis in peripheral blood mononuclear cells (PBMCs) from human immunodeficiency virus type-1 infected patients and in CD4 cross-linked PBMCs from normal individuals. Blood 82:3392.
72. Wang, Z.-Q., A. Dudhane, T. Orlikowsky, K. Clarke, X. Li, Z. Darzynkiewicz, and M. K. Hoffmann. 1994. CD4 engagement induces Fas antigen-dependent apoptosis of T cells in vivo. Eur. J. Immunol. 24:1549.
73. + T cells. Proc. Natl. Acad. Sci. USA 93:11014.
74. - and 'activating' memory T cells. Clin. Exp. Immunol. 95:195.
75. + T cells in the absence of TCR co-stimulation. Int. Immunol. 8:65.
76. lck. J. Exp. Med. 183:39.
77. Bank, I., and L. Chess. 1985. Perturbation of the T4 molecule transmits a negative signal to T cells. J. Exp. Med. 162:1294.
78. Mittler, R. S., and M. K. Hoffmann. 1989. Synergism between HIV gp120 and gp120-specific antibody in blocking human T cell activation. Science 245: 1380.
79. Dianzani, U., A. Shaw, M. Fernandez-Cabezuda, and C. A. Janeway Jr. 1992. Extensive CD4 cross-linking inhibits T cell activation by anti-receptor antibody but not by antigen. Int. Immunol. 4:995.
80. Liegler, T. J., and D. P. Stites. 1994. HIV-1 gp120 and anti-gp120 induce reversible unresponsiveness in peripheral CD4 T lymphocytes. J. Acquired Immune Defic. Syndr. 7:340.
81. Baldari, C. T., E. Milia, M. M. Di Somma, F. Baldoni, S. Valitutti, and J. L. Telford. 1995. Distinct signaling properties identify functionally different CD4 epitopes. Eur. J. Immunol. 25:1843.