SLP-76 sterile α motif (SAM) and individual H5 α helix mediate oligomer formation for microclusters and T-cell activation

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29539-29549

  Liu, Hebin ^a,b   Thaker, Youg Raj ^a   Stagg, Loren ^c   Schneider, Helga ^a   Ladbury, John E ^c   Rudd, Christopher E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b XI AN JIAOTONG LIVERPOOL UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

CO-PRECIPITATED; MICRO-CLUSTERS; N-TERMINALS; NUCLEAR FACTOR OF ACTIVATED T-CELLS; OLIGOMER FORMATIONS; SELF-ASSOCIATIONS; T CELL ACTIVATION; T-CELL RECEPTORS;

ASSOCIATION REACTIONS; CELL MEMBRANES; OLIGOMERS; TRANSCRIPTION;

T-CELLS;

ADAPTOR PROTEIN; CD3 ANTIGEN; DIMER; INTERLEUKIN 2; OLIGOMER; SLP 76 PROTEIN; T LYMPHOCYTE RECEPTOR; TETRAMER; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLUORESCENCE MICROSCALE THEROPHORESIS; GENETIC TRANSCRIPTION; H5 ALPHA HELIX; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LIGHT SCATTERING; LYMPHOCYTE FUNCTION; MICROCLUSTER; N TERMINAL STERILE ALPHA MOTIF; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS; BIOPHYSICS; IMMUNOLOGY; PROTEIN COMPLEXES; SAM DOMAIN; SIGNAL TRANSDUCTION; SLP-76; T-CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIGENS, CD3; BINDING SITES; CELLS, CULTURED; CIRCULAR DICHROISM; HUMANS; INTERLEUKIN-2; JURKAT CELLS; LIGHT; LYMPHOCYTE ACTIVATION; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; MUTATION; NFATC TRANSCRIPTION FACTORS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL; SCATTERING, RADIATION; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 84885624330     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.424846     Document Type: Article

References (61)

1. Rudd, C. E. (1999) Adaptors and molecular scaffolds in immune cell signaling. Cell 96, 5-8
2. Samelson, L. E. (2002) Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu. Rev. Immunol. 20, 371-394
3. Weiss, A. (2009) TCR signal transduction: opening the black box. J. Immunol. 183, 4821-4827
4. Wang, H., and Rudd, C. E. (2008) SKAP-55, SKAP-55-related and ADAP adaptors modulate integrin-mediated immune-cell adhesion. Trends Cell Biol. 18, 486-493
5. Jordan, M. S., Singer, A. L., and Koretzky, G. A. (2003) Adaptors as central mediators of signal transduction in immune cells. Nat. Immunol. 4, 110-116
6. Jackman, J. K., Motto, D. G., Sun, Q., Tanemoto, M., Turck, C. W., Peltz, G. A., Koretzky, G. A., and Findell, P. R. (1995) Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 inTcells. J. Biol. Chem. 270, 7029-7032
7. Yablonski, D., Kuhne, M. R., Kadlecek, T., and Weiss, A. (1998) Uncoupling of nonreceptor tyrosine kinases from PLC-γ1 in an SLP-76-deficient T cell. Science 281, 413-416
8. Pivniouk, V., Tsitsikov, E., Swinton, P., Rathbun, G., Alt, F. W., and Geha, R. S. (1998) Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell 94, 229-238
9. Clements, J. L., Yang, B., Ross-Barta, S. E., Eliason, S. L., Hrstka, R. F., Williamson, R. A., and Koretzky, G. A. (1998) Requirement for the leukocyte- specific adapter protein SLP-76 for normal T cell development. Science 281, 416-419
10. Baker, R. G., Hsu, C. J., Lee, D., Jordan, M. S., Maltzman, J. S., Hammer, D. A., Baumgart, T., and Koretzky, G. A. (2009) The adapter protein SLP-76 mediates "outside-in" integrin signaling and function in T cells. Mol. Cell. Biol. 29, 5578-5589
11. Kuhné, M. R., Lin, J., Yablonski, D., Mollenauer, M. N., Ehrlich, L. I., Huppa, J., Davis, M. M., and Weiss, A. (2003) Linker for activation of T cells, ζ-associated protein-70, and Src homology 2 domain-containing leukocyte protein-76 are required for TCR-induced microtubule-organizing center polarization. J. Immunol. 171, 860-866
12. Raab, M., da Silva, A. J., Findell, P. R., and Rudd, C. E. (1997) Regulation of Vav-SLP-76 binding by ZAP-70 and its relevance to TCRζ/CD3 induction of interleukin-2. Immunity 6, 155-164
13. Bubeck Wardenburg, J., Fu, C., Jackman, J. K., Flotow, H., Wilkinson, S. E., Williams, D. H., Johnson, R., Kong, G., Chan, A. C., and Findell, P. R. (1996) Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271, 19641-19644
14. Schneider, H., Guerette, B., Guntermann, C., and Rudd, C. E. (2000) Resting lymphocyte kinase (Rlk/Txk) targets lymphoid adaptor SLP-76 in the cooperative activation of interleukin-2 transcription in T-cells. J. Biol. Chem. 275, 3835-3840
15. Andreotti, A. H., Schwartzberg, P. L., Joseph, R. E., and Berg, L. J. (2010) T-cell signaling regulated by the Tec family kinase, Itk. Cold Spring Harb. Perspect. Biol. 2, a002287
16. Bunnell, S. C., Diehn, M., Yaffe, M. B., Findell, P. R., Cantley, L. C., and Berg, L. J. (2000) Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J. Biol. Chem. 275, 2219-2230
17. Berg, L. J., Finkelstein, L. D., Lucas, J. A., and Schwartzberg, P. L. (2005) Tec family kinases in T lymphocyte development and function. Annu Rev. Immunol. 23, 549-600
18. Ishiai, M., Kurosaki, M., Inabe, K., Chan, A. C., Sugamura, K., and Kurosaki, T. (2000) Involvement of LAT, Gads, and Grb2 in compartmentation of SLP-76 to the plasma membrane. J. Exp. Med. 192, 847-856
19. Yoder, J., Pham, C., Iizuka, Y. M., Kanagawa, O., Liu, S. K., McGlade, J., and Cheng, A. M. (2001) Requirement for the SLP-76 adaptor GADS in T cell development. Science 291, 1987-1991
20. Graham, L. J., Verí, M. C., DeBell, K. E., Noviello, C., Rawat, R., Jen, S., Bonvini, E., and Rellahan, B. (2003) 70Z/3 Cbl induces PLC γ 1 activation in T lymphocytes via an alternate Lat- and Slp-76-independent signaling mechanism. Oncogene 22, 2493-2503
21. Singer, A. L., Bunnell, S. C., Obstfeld, A. E., Jordan, M. S., Wu, J. N., Myung, P. S., Samelson, L. E., and Koretzky, G. A. (2004) Roles of the proline-rich domain in SLP-76 subcellular localization and T cell function. J. Biol. Chem. 279, 15481-15490
22. Berry, D. M., Nash, P., Liu, S. K., Pawson, T., and McGlade, C. J. (2002) A high-affinity Arg-X-X-Lys SH3 binding motif confers specificity for the interaction between Gads and SLP-76 in T cell signaling. Curr. Biol. 12, 1336-1341
23. Sanzenbacher, R., Kabelitz, D., and Janssen, O. (1999) SLP-76 binding to p56lck: a role for SLP-76 in CD4-induced desensitization of the TCR/CD3 signaling complex. J. Immunol. 163, 3143-3152
24. Yablonski, D., Kadlecek, T., and Weiss, A. (2001) Identification of a phospholipase C-γ1 (PLC-γ1) SH3 domain-binding site in SLP-76 required for T-cell receptor-mediated activation of PLC-γ1 and NFAT. Mol. Cell. Biol. 21, 4208-4218
25. Grasis, J. A., Guimond, D. M., Cam, N. R., Herman, K., Magotti, P., Lambris, J. D., and Tsoukas, C. D. (2010) In vivo significance of ITK-SLP-76 interaction in cytokine production. Mol. Cell. Biol. 30, 3596-3609
26. Sela, M., Bogin, Y., Beach, D., Oellerich, T., Lehne, J., Smith-Garvin, J. E., Okumura, M., Starosvetsky, E., Kosoff, R., Libman, E., Koretzky, G., Kambayashi, T., Urlaub, H., Wienands, J., Chernoff, J., and Yablonski, D. (2011) Sequential phosphorylation of SLP-76 at tyrosine 173 is required for activation of T and mast cells. EMBO J. 30, 3160-3172
27. Musci, M. A., Motto, D. G., Ross, S. E., Fang, N., and Koretzky, G. A. (1997) Three domains of SLP-76 are required for its optimal function in a T cell line. J. Immunol. 159, 1639-1647
28. da Silva, A. J., Li, Z., de Vera, C., Canto, E., Findell, P., and Rudd, C. E. (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. U.S.A. 94, 7493-7498
29. Di Bartolo, V., Montagne, B., Salek, M., Jungwirth, B., Carrette, F., Fourtane, J., Sol-Foulon, N., Michel, F., Schwartz, O., Lehmann, W. D., and Acuto, O. (2007) A novel pathway down-modulating T cell activation involves HPK-1-dependent recruitment of 14-3-3 proteins on SLP-76. J. Exp. Med. 204, 681-691
30. Sauer, K., Liou, J., Singh, S. B., Yablonski, D., Weiss, A., and Perlmutter, R. M. (2001) Hematopoietic progenitor kinase 1 associates physically and functionally with the adaptor proteins B cell linker protein and SLP-76 in lymphocytes. J. Biol. Chem. 276, 45207-45216
31. Shui, J. W., Boomer, J. S., Han, J., Xu, J., Dement, G. A., Zhou, G., and Tan, T. H. (2007) Hematopoietic progenitor kinase 1 negatively regulates T cell receptor signaling and T cell-mediated immune responses. Nat. Immunol. 8, 84-91
32. Raab, M., Wang, H., Lu, Y., Smith, X., Wu, Z., Strebhardt, K., Ladbury, J. E., and Rudd, C. E. (2010) T cell receptor "inside-out" pathway via signaling module SKAP1-RapL regulates T cell motility and interactions in lymph nodes. Immunity 32, 541-556
33. Raab, M., Smith, X., Matthess, Y., Strebhardt, K., and Rudd, C. E. (2011) SKAP1 protein PH domain determines RapL membrane localization and Rap1 protein complex formation for T cell receptor (TCR) activation of LFA-1. J. Biol. Chem. 286, 29663-29670
34. Dustin, M. L., Bivona, T. G., and Philips, M. R. (2004) Membranes as messengers in T cell adhesion signaling. Nat. Immunol. 5, 363-372
35. Yokosuka, T., Sakata-Sogawa, K., Kobayashi, W., Hiroshima, M., Hashimoto-Tane, A., Tokunaga, M., Dustin, M. L., and Saito, T. (2005) Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 6, 1253-1262
36. Bunnell, S. C., Singer, A. L., Hong, D. I., Jacque, B. H., Jordan, M. S., Seminario, M. C., Barr, V. A., Koretzky, G. A., and Samelson, L. E. (2006) Persistence of cooperatively stabilized signaling clusters drives T-cell activation. Mol. Cell. Biol. 26, 7155-7166
37. Liu, H., Purbhoo, M. A., Davis, D. M., and Rudd, C. E. (2010) SH2 domain containing leukocyte phosphoprotein of 76-kDa (SLP-76) feedback regulation of ZAP-70 microclustering. Proc. Natl. Acad. Sci. U.S.A. 107, 10166-10171
38. Purbhoo, M. A., Liu, H., Oddos, S., Owen, D. M., Neil, M. A., Pageon, S. V., French, P. M., Rudd, C. E., and Davis, D. M. (2010) Dynamics of subsynaptic vesicles and surface microclusters at the immunological synapse. Sci. Signal 3, ra36
39. Williamson, D. J., Owen, D. M., Rossy, J., Magenau, A., Wehrmann, M., Gooding, J. J., and Gaus, K. (2011) Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat. Immunol. 12, 655-662
40. Kim, C. A., and Bowie, J. U. (2003) SAM domains: uniform structure, diversity of function. Trends Biochem. Sci. 28, 625-628
41. Meruelo, A. D., and Bowie, J. U. (2009) Identifying polymer-forming SAM domains. Proteins 74, 1-5
42. Kim, C. A., Gingery, M., Pilpa, R. M., and Bowie, J. U. (2002) The SAM domain of polyhomeotic forms a helical polymer. Nat. Struct. Biol. 9, 453-457
43. Tran, H. H., Kim, C. A., Faham, S., Siddall, M. C., and Bowie, J. U. (2002) Native interface of the SAM domain polymer of TEL. BMC Struct. Biol. 2, 5
44. Thanos, C. D., Goodwill, K. E., and Bowie, J. U. (1999) Oligomeric structure of the human EphB2 receptor SAM domain. Science 283, 833-836
45. Serra-Pagès, C., Kedersha, N. L., Fazikas, L., Medley, Q., Debant, A., and Streuli, M. (1995) The LAR transmembrane protein tyrosine phosphatase and a coiled-coil LAR-interacting protein co-localize at focal adhesions. EMBO J. 14, 2827-2838
46. Schultz, J., Ponting, C. P., Hofmann, K., and Bork, P. (1997) SAM as a protein interaction domain involved in developmental regulation. Protein Sci. 6, 249-253
47. Qiao, F., and Bowie, J. U. (2005) The many faces of SAM. Sci STKE 2005, re7
48. Stapleton, D., Balan, I., Pawson, T., and Sicheri, F. (1999) The crystal structure of an Eph receptor SAM domain reveals a mechanism for modular dimerization. Nat. Struct. Biol. 6, 44-49
49. Shen, S., Lau, J., Zhu, M., Zou, J., Fuller, D., Li, Q. J., and Zhang, W. (2009) The importance of Src homology 2 domain-containing leukocyte phosphoprotein of 76 kilodaltons sterile-α motif domain in thymic selection and T-cell activation. Blood 114, 74-84
50. Barda-Saad, M., Shirasu, N., Pauker, M. H., Hassan, N., Perl, O., Balbo, A., Yamaguchi, H., Houtman, J. C., Appella, E., Schuck, P., and Samelson, L. E. (2010) Cooperative interactions at the SLP-76 complex are critical for actin polymerization. EMBO J. 29, 2315-2328
51. Schneider, H., Smith, X., Liu, H., Bismuth, G., and Rudd, C. E. (2008) CTLA-4 disrupts ZAP70 microcluster formation with reduced T cell/ APC dwell times and calcium mobilization. Eur. J. Immunol. 38, 40-47
52. Raab, M., Kang, H., da Silva, A., Zhu, X., and Rudd, C. E. (1999) FYN-TFYB- SLP-76 interactions define a T-cell receptor ζ/CD3-mediated tyrosine phosphorylation pathway that up-regulates interleukin 2 transcription in T-cells. J. Biol. Chem. 274, 21170-21179
53. Valk, E., Leung, R., Kang, H., Kaneko, K., Rudd, C. E., and Schneider, H. (2006) T cell receptor-interacting molecule acts as a chaperone to modulate surface expression of the CTLA-4 coreceptor. Immunity 25, 807-821
54. Bunnell, S. C., Hong, D. I., Kardon, J. R., Yamazaki, T., McGlade, C. J., Barr, V. A., and Samelson, L. E. (2002) T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158, 1263-1275
55. Jerabek-Willemsen, M., Wienken, C. J., Braun, D., Baaske, P., and Duhr, S. (2011) Molecular interaction studies using microscale thermophoresis. Assay Drug Dev. Technol. 9, 342-353
56. Ortega, A., Amorós, D., and García de la Torre, J. (2011) Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models. Biophys. J. 101, 892-898
57. Tovchigrechko, A., and Vakser, I. A. (2006) GRAMM-X public web server for protein-protein docking. Nucleic Acids Res. 34, W310-314
58. Tovchigrechko, A., and Vakser, I. A. (2005) Development and testing of an automated approach to protein docking. Proteins 60, 296-301
59. Bhattacharjya, S., Xu, P., Chakrapani, M., Johnston, L., and Ni, F. (2005) Polymerization of the SAM domain of MAPKKK Ste11 from the budding yeast: implications for efficient signaling through the MAPK cascades. Protein Sci. 14, 828-835
60. Varma, R., Campi, G., Yokosuka, T., Saito, T., and Dustin, M. L. (2006) T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity 25, 117-127
61. Houtman, J. C., Yamaguchi, H., Barda-Saad, M., Braiman, A., Bowden, B., Appella, E., Schuck, P., and Samelson, L. E. (2006) Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat. Struct. Mol. Biol. 13, 798-805