GRB2-mediated recruitment of THEMIS to LAT is essential for thymocyte development

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3749-3756

  Paster, Wolfgang ^a   Brockmeyer, Claudia ^a,e   Fu, Guo ^b   Simister, Philip C ^c   De Wet, Ben ^a   Martinez Riaño, Ana ^a,f   Hoerter, John A H ^b   Feller, Stephan M ^c   Wülfing, Christoph ^d   Gascoigne, Nicholas R J ^b   Acuto, Oreste ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LAT PROTEIN; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; PROTEIN SH3; REGULATOR PROTEIN; THYMOCYTE EXPRESSED MOLECULE INVOLVED IN SELECTION; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MATURATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENETIC TRANSFECTION; IMAGE ANALYSIS; IMMUNOLOGICAL SYNAPSE; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; THYMOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CELL ADHESION MOLECULES; CELL LINE; GRB2 ADAPTOR PROTEIN; HUMANS; IMMUNOLOGICAL SYNAPSES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE ALIGNMENT; THYMOCYTES; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84875444226     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203389     Document Type: Article

References (30)

1. Fu, G., S. Vallée, V. Rybakin, M. V. McGuire, J. Ampudia, C. Brockmeyer, M. Salek, P. R. Fallen, J. A. Hoerter, A. Munshi, et al. 2009. Themis controls thymocyte selection through regulation of T cell antigen receptor-mediated signaling. Nat. Immunol. 10: 848-856.
2. Johnson, A. L., L. Aravind, N. Shulzhenko, A. Morgun, S. Y. Choi, T. L. Crockford, T. Lambe, H. Domaschenz, E. M. Kucharska, L. Zheng, et al. 2009. Themis is a member of a new metazoan gene family and is required for the completion of thymocyte positive selection. Nat. Immunol. 10: 831-839.
3. Lesourne, R., S. Uehara, J. Lee, K. D. Song, L. Li, J. Pinkhasov, Y. Zhang, N. P. Weng, K. F. Wildt, L. Wang, et al. 2009. Themis, a T cell-specific protein important for late thymocyte development. Nat. Immunol. 10: 840-847.
4. Gascoigne, N. R., and E. Palmer. 2011. Signaling in thymic selection. Curr. Opin. Immunol. 23: 207-212.
5. Patrick, M. S., H. Oda, K. Hayakawa, Y. Sato, K. Eshima, T. Kirikae, S. Iemura, M. Shirai, T. Abe, T. Natsume, et al. 2009. Gasp, a Grb2-associating protein, is critical for positive selection of thymocytes. Proc. Natl. Acad. Sci. USA 106: 16345-16350.
6. Chabod, M., C. Pedros, L. Lamouroux, C. Colacios, I. Bernard, D. Lagrange, D. Balz-Hara, J. F. Mosnier, C. Laboisse, N. Vergnolle, et al. 2012. A spontaneous mutation of the rat Themis gene leads to impaired function of regulatory T cells linked to inflammatory bowel disease. PLoS Genet. 8: e1002461.
7. Brockmeyer, C., W. Paster, D. Pepper, C. P. Tan, D. C. Trudgian, S. McGowan, G. Fu, N. R. Gascoigne, O. Acuto, and M. Salek. 2011. T cell receptor (TCR)-induced tyrosine phosphorylation dynamics identifies THEMIS as a new TCR signalosome component. J. Biol. Chem. 286: 7535-7547.
8. Trudgian, D. C., B. Thomas, S. J. McGowan, B. M. Kessler, M. Salek, and O. Acuto. 2010. CPFP: a central proteomics facilities pipeline. Bioinformatics 26: 1131-1132.
9. Trudgian, D. C., R. Singleton, M. E. Cockman, P. J. Ratcliffe, and B. M. Kessler. 2012. ModLS: Post-translational modification localization scoring with automatic specificity expansion. J. Proteomics Bioinform. 5: 283-289.
10. Beausoleil, S. A., J. Villén, S. A. Gerber, J. Rush, and S. P. Gygi. 2006. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24: 1285-1292.
11. Singleton, K. L., K. T. Roybal, Y. Sun, G. Fu, N. R. Gascoigne, N. S. van Oers, and C. Wülfing. 2009. Spatiotemporal patterning during T cell activation is highly diverse. Sci. Signal. 2: ra15.
12. Lewitzky, M., C. Kardinal, N. H. Gehring, E. K. Schmidt, B. Konkol, M. Eulitz, W. Birchmeier, U. Schaeper, and S. M. Feller. 2001. The C-terminal SH3 domain of the adapter protein Grb2 binds with high affinity to sequences in Gab1 and SLP-76 which lack the SH3-typical P-x-x-P core motif. Oncogene 20: 1052-1062.
13. 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: 933-945.
14. Harkiolaki, M., T. Tsirka, M. Lewitzky, P. C. Simister, D. Joshi, L. E. Bird, E. Y. Jones, N. O'Reilly, and S. M. Feller. 2009. Distinct binding modes of two epitopes inGab2 that interactwith the SH3Cdomain of Grb2. Structure 17: 809-822.
15. Lewitzky, M., M. Harkiolaki, M. C. Domart, E. Y. Jones, and S. M. Feller. 2004. Mona/Gads SH3C binding to hematopoietic progenitor kinase 1 (HPK1) combines an atypical SH3 binding motif, R/KXXK, with a classical PXXP motif embedded in a polyproline type II (PPII) helix. J. Biol. Chem. 279: 28724-28732.
16. Balagopalan, L., N. P. Coussens, E. Sherman, L. E. Samelson, and C. L. Sommers. 2010. The LAT story: a tale of cooperativity, coordination, and choreography. Cold Spring Harb. Perspect. Biol. 2: a005512.
17. Lin, T. A., K. W. McIntyre, J. Das, C. Liu, K. D. O'Day, B. Penhallow, C. Y. Hung, G. S. Whitney, D. J. Shuster, X. Yang, et al. 2004. Selective Itk inhibitors block T-cell activation and murine lung inflammation. Biochemistry 43: 11056-11062.
18. Brdicka, T., T. A. Kadlecek, J. P. Roose, A. W. Pastuszak, and A. Weiss. 2005. Intramolecular regulatory switch in ZAP-70: analogy with receptor tyrosine kinases. Mol. Cell. Biol. 25: 4924-4933.
19. Blom, N., S. Gammeltoft, and S. Brunak. 1999. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294: 1351-1362.
20. Xue, Y., F. Zhou, M. Zhu, K. Ahmed, G. Chen, and X. Yao. 2005. GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res. 33(Web Server issue): W184-W187.
21. Lesourne, R., E. Zvezdova, K. D. Song, D. El-Khoury, S. Uehara, V. A. Barr, L. E. Samelson, and P. E. Love. 2012. Interchangeability of Themis1 and Themis2 in thymocyte development reveals two related proteins with conserved molecular function. J. Immunol. 189: 1154-1161.
22. Nika, K., C. Soldani, M. Salek, W. Paster, A. Gray, R. Etzensperger, L. Fugger, P. Polzella, V. Cerundolo, O. Dushek, et al. 2010. Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity 32: 766-777.
23. Acuto, O., V. Di Bartolo, and F. Michel. 2008. Tailoring T-cell receptor signals by proximal negative feedback mechanisms. Nat. Rev. Immunol. 8: 699-712.
24. Terasawa, H., D. Kohda, H. Hatanaka, S. Tsuchiya, K. Ogura, K. Nagata, S. Ishii, V. Mandiyan, A. Ullrich, J. Schlessinger, et al. 1994. Structure of the Nterminal SH3 domain of GRB2 complexed with a peptide from the guanine nucleotide releasing factor Sos. Nat. Struct. Biol. 1: 891-897.
25. Tashiro, K., T. Tsunematsu, H. Okubo, T. Ohta, E. Sano, E. Yamauchi, H. Taniguchi, and H. Konishi. 2009. GAREM, a novel adaptor protein for growth factor receptor-bound protein 2, contributes to cellular transformation through the activation of extracellular signal-regulated kinase signaling. J. Biol. Chem. 284: 20206-20214.
26. Aghazadeh, B., W. E. Lowry, X. Y. Huang, and M. K. Rosen. 2000. Structural basis for relief of autoinhibition of the Dbl homology domain of proto-oncogene Vav by tyrosine phosphorylation. Cell 102: 625-633.
27. Kortum, R. L., C. L. Sommers, C. P. Alexander, J. M. Pinski, W. Li, A. Grinberg, J. Lee, P. E. Love, and L. E. Samelson. 2011. Targeted Sos1 deletion reveals its critical role in early T-cell development. Proc. Natl. Acad. Sci. USA 108: 12407-12412.
28. Daniels, M. A., E. Teixeiro, J. Gill, B. Hausmann, D. Roubaty, K. Holmberg, G. Werlen, G. A. Holländer, N. R. Gascoigne, and E. Palmer. 2006. Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444: 724-729.
29. Kortum, R. L., C. L. Sommers, J. M. Pinski, C. P. Alexander, R. K. Merrill, W. Li, P. E. Love, and L. E. Samelson. 2012. Deconstructing Ras signaling in the thymus. Mol. Cell. Biol. 32: 2748-2759.
30. Jang, I. K., J. Zhang, Y. J. Chiang, H. K. Kole, D. G. Cronshaw, Y. Zou, and H. Gu. 2010. Grb2 functions at the top of the T-cell antigen receptor-induced tyrosine kinase cascade to control thymic selection. Proc. Natl. Acad. Sci. USA 107: 10620-10625.