Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation

Nature Cell Biology

Volumn 5, Issue 2, 2003, Pages 149-154

  Latour, Sylvain ^a,b   Roncagalli, Romain ^a,c   Chen, Riyan ^a   Bakinowski, Marcin ^a   Shi, Xiaochu ^a   Schwartzberg, Pamela L ^d   Davidson, Dominique ^a   Veillette, André ^a,c,e  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CD150 ANTIGEN; CELL RECEPTOR; CYTOKINE; CYTOPLASM PROTEIN; HYBRID PROTEIN; PHOSPHOTYROSINE; PROTEIN FYNT; PROTEIN TYROSINE KINASE; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE MUTATION; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; LYMPHOPROLIFERATIVE DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; T LYMPHOCYTE; TRANSGENIC MOUSE; VIRUS INFECTION; X CHROMOSOME LINKAGE;

ANIMALIA; HUMAN HERPESVIRUS 4; MUS MUSCULUS;

EID: 0037322612     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb919     Document Type: Article

References (29)

1. Sayos, J. et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395, 462-469 (1998).
2. Coffey, A.J. et al. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nature Genet. 20, 129-135 (1998).
3. Nicholdm K.E. et al. Inactivating mutations in an SH2 domain-encoding gene in X-linked lympho-proliferative syndrome. Proc. Natl. Acad. Sci. USa. 95, 13765-13770 (1998).
4. Veillette, A. The SAP family: a new class of adaptor-like molecules that regulates immune cell functions. Sci. STKE 2002, E8 (2002).
5. Morra, M. et al. X-linked lymphoproliferative disease: a progressive immunodeficiency. Annu. Rev. Immunol. 19, 657-682 (2001).
6. Parolini, S. et al. X-linked lymphoproliferative disease. 2B4 molecule displaying inhibitory rather than activating function are responsible for the inability of natural killer cells to kill Esptein-Barr virus-infected cells. J. Exp. Med. 192, 337-346 (2000).
7. Bottino, C. et al. NTB-A, a novel SH2D1A-associated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative disease. J. Exp. Med. 194, 235-246 (2001).
8. Latour, S. et al. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nature Immunol. 2, 681-690 (2001).
9. Tangye, S.G., Phillips, J.H., Lanier, L.L. & Nichols, K.E. Functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lyphoproliferative syndrome. J. Immunol. 165, 2932-2936 (2000).
10. Tangye, S.G. et al. Cutting edge: human 2B4, an activating NK cell receptor, recruits the protein tyrosine phosphatase SHP-2 and the adaptor signaling protein SAP. J. Immunol. 162, 6981-6985 (1999).
11. Wu, C. et al. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nature Immunol. 2, 410-414 (2001).
12. Czar, M.J. et al. Altered lymphocyte responses and cytokine production in mice deficient in X-linked lymphoproliferative disease gene. SH2D1A/DSHP/SAP. Proc. Natl. Acad. Sci. USA 98, 7449-7454 (2001).
13. Mikhalap, S.V. et al. CDw150 associated with src-homology 2-containing inositol phosphatase and modulates CD95-mediated apoptosis. J. Immunol. 162, 5719-5727 (1999).
14. Sicheri, F. & Kuriyan, J. Structure of Src-family tyrosine kinases. Curr. Opin. Struct. Biol. 7, 777-785 (1997).
15. Thompson, A.D. et al. EAT-2 is a novel SH2 domain containing protein that is up regulated by Ewing's sarcoma EWS/FLI1 fusion gene. Oncogene 13, 2649-2658 (1996).
16. Poy, F. et al. Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol. Cell 4, 555-561 (1999).
17. Li, S.C. et al. Novel mode of ligand binding by the SH2 domain of the human XLP disease gene product SAP/SH2D1A. Curr. Biol. 9, 1355-1362 (1999).
18. Hwang, P.M. et al. A "three-pronged" binding mechanism for the SAP/SH2D1A SH2 domain: structural basis and relevance to the XLP syndrome. EMBO J. 21, 314-323 (2002).
19. Rotin, D. et al. SH2 domain prevent tyrosine dephosphorylation of the EGF receptor: identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma. EMBO J. 11, 559-567 (1992).
20. Yu, J. et al. Synergistic regulation of immunoreceptor signaling by slp-76-related adaptor clnk and serine/threonine protein kinase hpk-1. Mol. Cell Biol. 21, 6102-6112 (2001).
21. Moarefi, I. et al. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385, 650-653 (1997).
22. Lerner, E.C. & Smithgall, T.E. SH3-dependent stimulation of Src-family kinase autophosphorylation without tail release fron the SH domain in vivo. Nature Struct. Biol. 9, 365-369 (2002).
23. Anafi, M., Rosen, M.K., Gish, G.D., Kay, L.E. & Pawson, T. A potential SH3 domain-binding site in the Crk SH2 domain. J. Biol. Chem. 271, 21365-21374 (1996).
24. kk. Nature 350, 62-66 (1991).
25. Latour, S., Fournel, M. & Veillette, A. Regulation of T-cell antigen receptor signalling by Syk tyrosine protein kinase. Mol. Cell. Biol. 17, 4434-4441 (1997).
26. fyn. J. Exp. Med. 175 1483-1492, (1992).
27. Cloutier, J.F. & Veillette, A. Cooperative inhibition of T-cell antigen receptor signaling by a complex between a kinase and a phosphatase. J. Exp. Med. 189, 111-121 (1999).
28. Gregorieff, A., Pyronnet, S., Sonenberg, N. & Veillette, A. Regulation of SOCS-1 expression by translational repression. J. Biol. Chem. 275, 21596-21604 (2000).
29. kk. Cell 55, 301-308