Multipoint Binding of the SLP-76 SH2 Domain to ADAP Is Critical for Oligomerization of SLP-76 Signaling Complexes in Stimulated T Cells

REFERENCES

• Balagopalan L, Coussens NP, Sherman E, Samelson LE, Sommers CL. 2010. The LAT story: a tale of cooperativity, coordination, and choreography. Cold Spring Harb. Perspect. Biol. 2:a005512. doi:10.1101/cshperspect.a005512.
   PubMed Web of Science ®Google Scholar
• Bartelt RR, Houtman JC. 2013. The adaptor protein LAT serves as an integration node for signaling pathways that drive T cell activation. Wiley Interdiscip. Rev. Syst. Biol. Med. 5:101–110.
   PubMedGoogle Scholar
• Barda-Saad M, Shirasu N, Pauker MH, Hassan N, Perl O, Balbo A, Yamaguchi H, Houtman JC, Appella E, Schuck P, Samelson LE. 2010. Cooperative interactions at the SLP-76 complex are critical for actin polymerization. EMBO J. 29:2315–2328.
   PubMed Web of Science ®Google Scholar
• Sangani D, Venien-Bryan C, Harder T. 2009. Phosphotyrosine-dependent in vitro reconstitution of recombinant LAT-nucleated multiprotein signalling complexes on liposomes. Mol. Membr. Biol. 26:159–170.
   PubMed Web of Science ®Google Scholar
• Houtman JC, Higashimoto Y, Dimasi N, Cho S, Yamaguchi H, Bowden B, Regan C, Malchiodi EL, Mariuzza R, Schuck P, Appella E, Samelson LE. 2004. Binding specificity of multiprotein signaling complexes is determined by both cooperative interactions and affinity preferences. Biochemistry 43:4170–4178.
   PubMed Web of Science ®Google Scholar
• Bunnell SC, Hong DI, Kardon JR, Yamazaki T, McGlade CJ, Barr VA, Samelson LE. 2002. T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 158:1263–1275.
   PubMedGoogle Scholar
• Barda-Saad M, Braiman A, Titerence R, Bunnell SC, Barr VA, Samelson LE. 2005. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immunol. 6:80–89.
   PubMed Web of Science ®Google Scholar
• Bunnell SC, Singer AL, Hong DI, Jacque BH, Jordan MS, Seminario MC, Barr VA, Koretzky GA, Samelson LE. 2006. Persistence of cooperatively stabilized signaling clusters drives T-cell activation. Mol. Cell. Biol. 26:7155–7166.
   PubMed Web of Science ®Google Scholar
• Houtman JC, Yamaguchi H, Barda-Saad M, Braiman A, Bowden B, Appella E, Schuck P, Samelson LE. 2006. Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat. Struct. Mol. Biol. 13:798–805.
   PubMed Web of Science ®Google Scholar
• Nguyen K, Sylvain NR, Bunnell SC. 2008. T cell costimulation via the integrin VLA-4 inhibits the actin-dependent centralization of signaling microclusters containing the adaptor SLP-76. Immunity 28:810–821.
   PubMed Web of Science ®Google Scholar
• Sylvain NR, Nguyen K, Bunnell SC. 2011. Vav1-mediated scaffolding interactions stabilize SLP-76 microclusters and contribute to antigen-dependent T cell responses. Sci. Signal. 4:ra14. doi:10.1126/scisignal.2001178.
   PubMedGoogle Scholar
• Yokosuka T, Sakata-Sogawa K, Kobayashi W, Hiroshima M, Hashimoto-Tane A, Tokunaga M, Dustin ML, 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.
   PubMed Web of Science ®Google Scholar
• Campi G, Varma R, Dustin ML. 2005. Actin and agonist MHC-peptide complex-dependent T cell receptor microclusters as scaffolds for signaling. J. Exp. Med. 202:1031–1036.
   PubMed Web of Science ®Google Scholar
• Hashimoto-Tane A, Yokosuka T, Ishihara C, Sakuma M, Kobayashi W, Saito T. 2010. T-cell receptor microclusters critical for T-cell activation are formed independently of lipid raft clustering. Mol. Cell. Biol. 30:3421–3429.
   PubMedGoogle Scholar
• da Silva AJ, Li Z, de Vera C, Canto E, Findell P, Rudd CE. 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.
   PubMedGoogle Scholar
• Musci MA, Hendricks-Taylor LR, Motto DG, Paskind M, Kamens J, Turck CW, Koretzky GA. 1997. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272:11674–11677.
   PubMed Web of Science ®Google Scholar
• Yablonski D, Kadlecek T, Weiss A. 2001. Identification of a phospholipase C-gamma1 (PLC-gamma1) SH3 domain-binding site in SLP-76 required for T-cell receptor-mediated activation of PLC-gamma1 and NFAT. Mol. Cell. Biol. 21:4208–4218.
   PubMedGoogle Scholar
• Burns JC, Corbo E, Degen J, Gohil M, Anterasian C, Schraven B, Koretzky GA, Kliche S, Jordan MS. 2011. The SLP-76 Src homology 2 domain is required for T cell development and activation. J. Immunol. 187:4459–4466.
   PubMed Web of Science ®Google Scholar
• Peterson EJ, Woods ML, Dmowski SA, Derimanov G, Jordan MS, Wu JN, Myung PS, Liu QH, Pribila JT, Freedman BD, Shimizu Y, Koretzky GA. 2001. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 293:2263–2265.
   PubMed Web of Science ®Google Scholar
• Griffiths EK, Krawczyk C, Kong YY, Raab M, Hyduk SJ, Bouchard D, Chan VS, Kozieradzki I, Oliveira-Dos-Santos AJ, Wakeham A, Ohashi PS, Cybulsky MI, Rudd CE, Penninger JM. 2001. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293:2260–2263.
   PubMed Web of Science ®Google Scholar
• Geng L, Raab M, Rudd CE. 1999. Cutting edge: SLP-76 cooperativity with FYB/FYN-T in the up-regulation of TCR-driven IL-2 transcription requires SLP-76 binding to FYB at Tyr595 and Tyr651. J. Immunol. 163:5753–5757.
   PubMed Web of Science ®Google Scholar
• Boerth NJ, Judd BA, Koretzky GA. 2000. Functional association between SLAP-130 and SLP-76 in Jurkat T cells. J. Biol. Chem. 275:5143–5152.
   PubMed Web of Science ®Google Scholar
• Lange S, Sylvester M, Schumann M, Freund C, Krause E. 2010. Identification of phosphorylation-dependent interaction partners of the adapter protein ADAP using quantitative mass spectrometry: SILAC vs (18)O-labeling. J. Proteome Res. 9:4113–4122.
   PubMed Web of Science ®Google Scholar
• Sylvester M, Kliche S, Lange S, Geithner S, Klemm C, Schlosser A, Grossmann A, Stelzl U, Schraven B, Krause E, Freund C. 2010. Adhesion and degranulation promoting adapter protein (ADAP) is a central hub for phosphotyrosine-mediated interactions in T cells. PLoS One 5:e11708. doi:10.1371/journal.pone.0011708.
   PubMed Web of Science ®Google Scholar
• Brown PH, Balbo A, Schuck P. 2008. Characterizing protein-protein interactions by sedimentation velocity analytical ultracentrifugation. Curr. Protoc. Immunol. Chapter 18:Unit 18.15. doi:10.1002/0471142735.im1815s81.
   Google Scholar
• Schuck P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78:1606–1619.
   PubMed Web of Science ®Google Scholar
• Zhao H, Brown PH, Schuck P. 2011. On the distribution of protein refractive index increments. Biophys. J. 100:2309–2317.
   PubMedGoogle Scholar
• Cohn EJ, Edsall JT. 1943. Density and apparent specific volume of proteins. Van Nostrand-Reinhold, Princeton, NJ.
   Google Scholar
• Brautigam CA. 2011. Using Lamm-equation modeling of sedimentation velocity data to determine the kinetic and thermodynamic properties of macromolecular interactions. Methods 54:4–15.
   PubMedGoogle Scholar
• Dam J, Velikovsky CA, Mariuzza RA, Urbanke C, Schuck P. 2005. Sedimentation velocity analysis of heterogeneous protein-protein interactions: Lamm equation modeling and sedimentation coefficient distributions c(s). Biophys. J. 89:619–634.
   PubMedGoogle Scholar
• Keller S, Vargas C, Zhao H, Piszczek G, Brautigam CA, Schuck P. 2012. High-precision isothermal titration calorimetry with automated peak-shape analysis. Anal. Chem. 84:5066–5073.
   PubMed Web of Science ®Google Scholar
• Houtman JC, Brown PH, Bowden B, Yamaguchi H, Appella E, Samelson LE, Schuck P. 2007. Studying multisite binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: application to adaptor protein complexes in cell signaling. Protein Sci. 16:30–42.
   PubMed Web of Science ®Google Scholar
• Zacharias DA, Violin JD, Newton AC, Tsien RY. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913–916.
   PubMed Web of Science ®Google Scholar
• Yablonski D, Kuhne MR, Kadlecek T, Weiss A. 1998. Uncoupling of nonreceptor tyrosine kinases from PLC-gamma1 in an SLP-76-deficient T cell. Science 281:413–416.
   PubMedGoogle Scholar
• Bunnell SC, Barr VA, Fuller CL, Samelson LE. 2003. High-resolution multicolor imaging of dynamic signaling complexes in T cells stimulated by planar substrates. Sci. STKE 2003:PL8. doi:10.1126/stke.2003.177.pl8.
   PubMedGoogle Scholar
• Pauker MH, Reicher B, Fried S, Perl O, Barda-Saad M. 2011. Functional cooperation between the proteins Nck and ADAP is fundamental for actin reorganization. Mol. Cell. Biol. 31:2653–2666.
   PubMed Web of Science ®Google Scholar
• Wang H, Wei B, Bismuth G, Rudd CE. 2009. SLP-76-ADAP adaptor module regulates LFA-1 mediated costimulation and T cell motility. Proc. Natl. Acad. Sci. U. S. A. 106:12436–12441.
   PubMedGoogle Scholar
• Wang H, McCann FE, Gordan JD, Wu X, Raab M, Malik TH, Davis DM, Rudd CE. 2004. ADAP-SLP-76 binding differentially regulates supramolecular activation cluster (SMAC) formation relative to T cell-APC conjugation. J. Exp. Med. 200:1063–1074.
   PubMed Web of Science ®Google Scholar
• Baker RG, Hsu CJ, Lee D, Jordan MS, Maltzman JS, Hammer DA, Baumgart T, Koretzky GA. 2009. The adapter protein SLP-76 mediates “outside-in” integrin signaling and function in T cells. Mol. Cell. Biol. 29:5578–5589.
   PubMedGoogle Scholar
• Wang H, Rudd CE. 2008. SKAP-55, SKAP-55-related and ADAP adaptors modulate integrin-mediated immune-cell adhesion. Trends Cell Biol. 18:486–493.
   PubMed Web of Science ®Google Scholar
• Bradshaw JM, Mitaxov V, Waksman G. 1999. Investigation of phosphotyrosine recognition by the SH2 domain of the Src kinase. J. Mol. Biol. 293:971–985.
   PubMedGoogle Scholar
• Spuches AM, Argiros HJ, Lee KH, Haas LL, Pero SC, Krag DN, Roller PP, Wilcox DE, Lyons BA. 2007. Calorimetric investigation of phosphorylated and non-phosphorylated peptide ligand binding to the human Grb7-SH2 domain. J. Mol. Recognit. 20:245–252.
   PubMedGoogle Scholar
• Long YQ, Voigt JH, Lung FD, King CR, Roller PP. 1999. Significant compensatory role of position Y-2 conferring high affinity to non-phosphorylated inhibitors of Grb2-SH2 domain. Bioorg. Med. Chem. Lett. 9:2267–2272.
   PubMedGoogle Scholar
• Li P, Zhang M, Peach ML, Zhang X, Liu H, Nicklaus M, Yang D, Roller PP. 2003. Structural basis for a non-phosphorus-containing cyclic peptide binding to Grb2-SH2 domain with high affinity. Biochem. Biophys. Res. Commun. 307:1038–1044.
   PubMedGoogle Scholar
• Lung FD, Chang CW, Chong MC, Liou CC, Li P, Peach ML, Nicklaus MC, Lou BS, Roller PP. 2005. Small nonphosphorylated Grb2-SH2 domain antagonists evaluated by surface plasmon resonance technology. Biopolymers 80:628–635.
   PubMedGoogle Scholar
• Barr VA, Balagopalan L, Barda-Saad M, Polishchuk R, Boukari H, Bunnell SC, Bernot KM, Toda Y, Nossal R, Samelson LE. 2006. T-cell antigen receptor-induced signaling complexes: internalization via a cholesterol-dependent endocytic pathway. Traffic 7:1143–1162.
   PubMedGoogle Scholar
• Braiman A, Barda-Saad M, Sommers CL, Samelson LE. 2006. Recruitment and activation of PLCgamma1 in T cells: a new insight into old domains. EMBO J. 25:774–784.
   PubMedGoogle Scholar
• Sauer K, Liou J, Singh SB, Yablonski D, Weiss A, Perlmutter RM. 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.
   PubMedGoogle Scholar
• Lasserre R, Cuche C, Blecher-Gonen R, Libman E, Biquand E, Danckaert A, Yablonski D, Alcover A, Di Bartolo V. 2011. Release of serine/threonine-phosphorylated adaptors from signaling microclusters down-regulates T cell activation. J. Cell Biol. 195:839–853.
   PubMed Web of Science ®Google Scholar
• Zhang W, Trible RP, Zhu M, Liu SK, McGlade CJ, Samelson LE. 2000. Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell antigen receptor-mediated signaling. J. Biol. Chem. 275:23355–23361.
   PubMed Web of Science ®Google Scholar
• Zhu M, Janssen E, Zhang W. 2003. Minimal requirement of tyrosine residues of linker for activation of T cells in TCR signaling and thymocyte development. J. Immunol. 170:325–333.
   PubMedGoogle Scholar
• Nag A, Monine MI, Faeder JR, Goldstein B. 2009. Aggregation of membrane proteins by cytosolic cross-linkers: theory and simulation of the LAT-Grb2-SOS1 system. Biophys. J. 96:2604–2623.
   PubMedGoogle Scholar