Tyrosine-phosphorylation of the scaffold protein ADAP and its role in T cell signaling

References

• Abram CL, Lowell CA. The ins and outs of leukocyte integrin signaling. Annu Rev Immunol. 2009;27:339–362.
   PubMed Web of Science ®Google Scholar
• Hogg N, Patzak I, Willenbrock F. The insider’s guide to leukocyte integrin signalling and function. Nat Rev Immunol. 2011;11(6):416–426.
   PubMed Web of Science ®Google Scholar
• Moser M, Legate KR, Zent R, et al. The tail of integrins, talin, and kindlins. Science. 2009;324(5929):895–899.
   PubMed Web of Science ®Google Scholar
• Springer TA, Dustin ML. Integrin inside-out signaling and the immunological synapse. Curr Opin Cell Biol. 2012;24(1):107–115.
   PubMed Web of Science ®Google Scholar
• Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation. Annu Rev Immunol. 2009;27:591–619.
   PubMed Web of Science ®Google Scholar
• Baker RG, Koretzky GA. Regulation of T cell integrin function by adapter proteins. Immunol Res. 2008;42(1–3):132–144.
   PubMed Web of Science ®Google Scholar
• Mor A, Dustin ML, Philips MR. Small GTPases and LFA-1 reciprocally modulate adhesion and signaling. Immunol Rev. 2007;218:114–125.
   PubMed Web of Science ®Google Scholar
• Garcia-Bernal D, Parmo-Cabanas M, Dios-Esponera A, et al. Chemokine-induced Zap70 kinase-mediated dissociation of the Vav1-talin complex activates alpha4beta1 integrin for T cell adhesion. Immunity. 2009;31(6):953–964.
   PubMed Web of Science ®Google Scholar
• Smith X, Schneider H, Kohler K, et al. The chemokine CXCL12 generates costimulatory signals in T cells to enhance phosphorylation and clustering of the adaptor protein SLP-76. Sci Signal. 2013;6(286):ra65.
   PubMed Web of Science ®Google Scholar
• Kumar A, Humphreys TD, Kremer KN, et al. CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity. 2006;25(2):213–224.
   PubMed Web of Science ®Google Scholar
• da Silva AJ, Janssen O, Rudd CE. T cell receptor zeta/CD3-p59fyn(T)-associated p120/130 binds to the SH2 domain of p59fyn(T). J Exp Med. 1993;178(6):2107–2113.
   PubMed Web of Science ®Google Scholar
• Boerth NJ, Judd BA, Koretzky GA. Functional association between SLAP-130 and SLP-76 in Jurkat T cells. J Biol Chem. 2000;275(7):5143–5152.
   PubMed Web of Science ®Google Scholar
• DaSilva AJ, Li ZW, DeVera C, et al. 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. 1997;94(14):7493–7498.
   PubMed Web of Science ®Google Scholar
• Jackman JK, Motto DG, Sun Q, et al. Molecular cloning of SLP-76, a 76-kDa tyrosine phosphoprotein associated with Grb2 in T cells. J Biol Chem. 1995;270(13):7029–7032.
   PubMed Web of Science ®Google Scholar
• Musci MA, Hendricks-Taylor LR, Motto DG, et al. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J Biol Chem. 1997;272(18):11674–11677.
   PubMed Web of Science ®Google Scholar
• Griffiths EK, Krawczyk C, Kong YY, et al. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science. 2001;293(5538):2260–2263.
   PubMed Web of Science ®Google Scholar
• Peterson EJ, Woods ML, Dmowski SA, et al. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science. 2001;293(5538):2263–2265.
   PubMed Web of Science ®Google Scholar
• Lange S, Sylvester M, Schumann M, et al. Identification of phosphorylation-dependent interaction partners of the adapter protein ADAP using quantitative mass spectrometry: SILAC vs O-18-labeling. J Proteome Res. 2010;9(8):4113–4122.
   PubMed Web of Science ®Google Scholar
• Krause M, Sechi AS, Konradt M, et al. Fyn-binding protein (Fyb)/SLP-76-associated protein (SLAP), Ena/vasodilator-stimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. J Cell Biol. 2000;149(1):181–194.
   PubMed Web of Science ®Google Scholar
• Stephanowitz H, Lange S, Lang D, et al. Improved two-dimensional reversed phase-reversed phase LC-MS/MS approach for identification of peptide-protein interactions. J Proteome Res. 2012;11(2):1175–1183.
   PubMed Web of Science ®Google Scholar
• Sylvester M, Kliche S, Lange S, et al. Adhesion and degranulation promoting adapter protein (ADAP) is a central hub for phosphotyrosine-mediated interactions in T cells. PLoS One. 2010;5(7):e11708.
   PubMed Web of Science ®Google Scholar
• Chan AC, Irving BA, Weiss A. New insights into T-cell antigen receptor structure and signal transduction. Curr Opin Immunol. 1992;4(3):246–251.
   PubMed Web of Science ®Google Scholar
• Samelson LE, Klausner RD. Tyrosine kinases and tyrosine-based activation motifs. Current research on activation via the T cell antigen receptor. J Biol Chem. 1992;267(35):24913–24916.
   PubMed Web of Science ®Google Scholar
• Horejsi V, Zhang W, Schraven B. Transmembrane adaptor proteins: organizers of immunoreceptor signalling. Nat Rev Immunol. 2004;4(8):603–616.
   PubMed Web of Science ®Google Scholar
• Samelson LE. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu Rev Immunol. 2002;20:371–394.
   PubMed Web of Science ®Google Scholar
• Wilkinson B, Wang H, Rudd CE. Positive and negative adaptors in T-cell signalling. Immunology. 2004;111(4):368–374.
   PubMed Web of Science ®Google Scholar
• Carrizosa E, Gomez TS, Labno CM, et al. Hematopoietic lineage cell-specific protein 1 is recruited to the immunological synapse by IL-2-inducible T cell kinase and regulates phospholipase Cgamma1 microcluster dynamics during T cell spreading. J Immunology. 2009;183(11):7352–7361.
   PubMed Web of Science ®Google Scholar
• Hauck CR, Klingbeil CK, Schlaepfer DD. Focal adhesion kinase functions as a receptor-proximal signaling component required for directed cell migration. Immunol Res. 2000;21(2–3):293–303.
   PubMed Web of Science ®Google Scholar
• Hauser MA, Schaeuble K, Kindinger I, et al. Inflammation-induced CCR7 oligomers form scaffolds to integrate distinct signaling pathways for efficient cell migration. Immunity. 2016;44(1):59–72.
   PubMed Web of Science ®Google Scholar
• Kliche S, Worbs T, Wang X, et al. CCR7-mediated LFA-1 functions in T cells are regulated by 2 independent ADAP/SKAP55 modules. Blood. 2012;119(3):777–785.
   PubMed Web of Science ®Google Scholar
• Kliche S, Breitling D, Togni M, et al. The ADAP/SKAP55 signaling module regulates T-cell receptor-mediated integrin activation through plasma membrane targeting of Rap1. Mol Cell Biol. 2006;26(19):7130–7144.
   PubMed Web of Science ®Google Scholar
• Heuer K, Kofler M, Langdon G, et al. Structure of a helically extended SH3 domain of the T cell adapter protein ADAP. Structure. 2004;12(4):603–610.
   PubMed Web of Science ®Google Scholar
• Heuer K, Arbuzova A, Strauss H, et al. The helically extended SH3 domain of the T cell adaptor protein ADAP is a novel lipid interaction domain. J Mol Biol. 2005;348(4):1025–1035.
   PubMed Web of Science ®Google Scholar
• Heuer K, Sylvester M, Kliche S, et al. Lipid-binding hSH3 domains in immune cell adapter proteins. J Mol Biol. 2006;361(1):94–104.
   PubMed Web of Science ®Google Scholar
• Swanson KD, Tang Y, Ceccarelli DF, et al. The Skap-hom dimerization and PH domains comprise a 3ʹ-phosphoinositide-gated molecular switch. Mol Cell. 2008;32(4):564–575.
   PubMed Web of Science ®Google Scholar
• Raab M, Smith X, Matthess Y, et al. 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. 2011;286(34):29663–29670.
   PubMed Web of Science ®Google Scholar
• Witte A, Degen J, Baumgart K, et al. Emerging roles of ADAP, SKAP55, and SKAP-HOM for integrin and NF-κB signaling in T cells. J Clin Cell Immunol. 2012. doi:10.4172/2155-9899.S12-002.
   Google Scholar
• Engelmann S, Togni M, Kliche S, et al. The adhesion- and degranulation-promoting adaptor protein and its role in the modulation of experimental autoimmune encephalomyelitis. Crit Rev Immunol. 2015;35(1):1–14.
   PubMed Web of Science ®Google Scholar
• Wang H, Liu H, Lu Y, et al. Functional defects of SKAP-55-deficient T cells identify a regulatory role for the adaptor in LFA-1 adhesion. Mol Cell Biol. 2007;27(19):6863–6875.
   PubMed Web of Science ®Google Scholar
• Lehmann R, Meyer J, Schuemann M, et al. A novel S3S-TAP-tag for the isolation of T-cell interaction partners of adhesion and degranulation promoting adaptor protein. Proteomics. 2009;9(23):5288–5295.
   PubMed Web of Science ®Google Scholar
• Marie-Cardine A, Hendricks-Taylor LR, Boerth NJ, et al. Molecular interaction between the Fyn-associated protein SKAP55 and the SLP-76-associated phosphoprotein SLAP-130. J Biol Chem. 1998;273(40):25789–25795.
   PubMed Web of Science ®Google Scholar
• Lettau M, Pieper J, Gerneth A, et al. The adapter protein Nck: role of individual SH3 and SH2 binding modules for protein interactions in T lymphocytes. Protein Sci. 2010;19(4):658–669.
   PubMed Web of Science ®Google Scholar
• Raab M, Kang H, da Silva A, et al. FYN-T-FYB-SLP-76 interactions define a T-cell receptor zeta/CD3-mediated tyrosine phosphorylation pathway that up-regulates interleukin 2 transcription in T-cells. J Biol Chem. 1999;274(30):21170–21179.
   PubMed Web of Science ®Google Scholar
• Veale M, Raab M, Li Z, et al. Novel isoform of lymphoid adaptor FYN-T-binding protein (FYB-130) interacts with SLP-76 and up-regulates interleukin 2 production. J Biol Chem. 1999;274(40):28427–28435.
   PubMed Web of Science ®Google Scholar
• Coussens NP, Hayashi R, Brown PH, et al. Multipoint binding of the SLP-76 SH2 domain to ADAP is critical for oligomerization of SLP-76 signaling complexes in stimulated T cells. Mol Cell Biol. 2013;33(21):4140–4151.
   PubMed Web of Science ®Google Scholar
• Lettau M, Kliche S, Kabelitz D, et al. The adapter proteins ADAP and Nck cooperate in T cell adhesion. Mol Immunol. 2014;60(1):72–79.
   PubMed Web of Science ®Google Scholar
• Bunnell SC, Singer AL, Hong DI, et al. Persistence of cooperatively stabilized signaling clusters drives T-cell activation. Mol Cell Biol. 2006;26(19):7155–7166.
   PubMed Web of Science ®Google Scholar
• Burns JC, Corbo E, Degen J, et al. The SLP-76 Src homology 2 domain is required for T cell development and activation. J Immunol. 2011;187(9):4459–4466.
   PubMed Web of Science ®Google Scholar
• Pauker MH, Reicher B, Fried S, et al. Functional cooperation between the proteins Nck and ADAP is fundamental for actin reorganization. Mol Cell Biol. 2011;31(13):2653–2666.
   PubMed Web of Science ®Google Scholar
• Pauker MH, Reicher B, Joseph N, et al. WASp family verprolin-homologous protein-2 (WAVE2) and Wiskott-Aldrich syndrome protein (WASp) engage in distinct downstream signaling interactions at the T cell antigen receptor site. J Biol Chem. 2014;289(50):34503–34519.
   PubMed Web of Science ®Google Scholar
• Pils S, Kopp K, Peterson L, et al. The adaptor molecule Nck localizes the WAVE complex to promote actin polymerization during CEACAM3-mediated phagocytosis of bacteria. Plos One. 2012;7(3):e32808.
   PubMed Web of Science ®Google Scholar
• Lettau M, Kabelitz D, Janssen O. SDF1alpha-induced interaction of the adapter proteins Nck and HS1 facilitates actin polymerization and migration in T cells. Eur J Immunol. 2015;45(2):551–561.
   PubMed Web of Science ®Google Scholar
• Boehm ME, Seidler J, Hahn B, et al. Site-specific degree of phosphorylation in proteins measured by liquid chromatography-electrospray mass spectrometry. Proteomics. 2012;12(13):2167–2178.
   PubMed Web of Science ®Google Scholar
• Kuropka B, Witte A, Sticht J, et al. Analysis of phosphorylation-dependent protein interactions of adhesion and degranulation promoting adaptor protein (ADAP) reveals novel interaction partners required for chemokine-directed T cell migration. Mol Cell Proteomics. 2015;14(11):2961–2972.
   PubMed Web of Science ®Google Scholar
• Seidler J, Adal M, Kubler D, et al. Analysis of autophosphorylation sites in the recombinant catalytic subunit alpha of cAMP-dependent kinase by nano-UPLC-ESI-MS/MS. Anal Bioanal Chem. 2009;395(6):1713–1720.
   PubMed Web of Science ®Google Scholar
• Roncagalli R, Hauri S, Fiore F, et al. Quantitative proteomics analysis of signalosome dynamics in primary T cells identifies the surface receptor CD6 as a Lat adaptor-independent TCR signaling hub. Nat Immunol. 2014;15(4):384–392.
   PubMed Web of Science ®Google Scholar
• Dunham WH, Mullin M, Gingras AC. Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics. 2012;12(10):1576–1590.
   PubMed Web of Science ®Google Scholar
• Vermeulen M, Hubner NC, Mann M. High confidence determination of specific protein-protein interactions using quantitative mass spectrometry. Curr Opin Biotechnol. 2008;19(4):331–337.
   PubMed Web of Science ®Google Scholar
• Kuropka B, Royla N, Freund C, et al. Sortase A mediated site-specific immobilization for identification of protein interactions in affinity purification-mass spectrometry experiments. Proteomics. 2015;15(7):1230–1234.
   PubMed Web of Science ®Google Scholar
• Ong SE, Blagoev B, Kratchmarova I, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002;1(5):376–386.
   PubMed Web of Science ®Google Scholar
• Ong SE, Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc. 2006;1(6):2650–2660.
   PubMed Web of Science ®Google Scholar
• Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367–1372.
   PubMed Web of Science ®Google Scholar
• Cox J, Neuhauser N, Michalski A, et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794–1805.
   PubMed Web of Science ®Google Scholar
• Lang D, Anker S, Kuropka B, et al. Combining enzymatic O-18-labeling and 2-DLC-MS/MS for a study of protein interactions in primary T cells. Anal Methods. 2013;5(4):1058–1061.
   Web of Science ®Google Scholar
• Majkut P, Claussnitzer I, Merk H, et al. Completion of proteomic data sets by Kd measurement using cell-free synthesis of site-specifically labeled proteins. Plos One. 2013;8(12):e82352.
   PubMed Web of Science ®Google Scholar
• Geng L, Raab M, Rudd CE. 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 Immunology. 1999;163(11):5753–5757.
   PubMed Web of Science ®Google Scholar
• Wang H, McCann FE, Gordan JD, et al. ADAP-SLP-76 binding differentially regulates supramolecular activation cluster (SMAC) formation relative to T cell-APC conjugation. J Exp Med. 2004;200(8):1063–1074.
   PubMed Web of Science ®Google Scholar
• Piotukh K, Kosslick D, Zimmermann J, et al. Reversible disulfide bond formation of intracellular proteins probed by NMR spectroscopy. Free Radic Biol Med. 2007;43(9):1263–1270.
   PubMed Web of Science ®Google Scholar
• Zimmermann J, Kuhne R, Sylvester M, et al. Redox-regulated conformational changes in an SH3 domain. Biochemistry. 2007;46(23):6971–6977.
   PubMed Web of Science ®Google Scholar
• Levin C, Koren A, Pretorius E, et al. Deleterious mutation in the FYB gene is associated with congenital autosomal recessive small-platelet thrombocytopenia. J Thromb Haemost. 2015;13(7):1285–1292.
   PubMed Web of Science ®Google Scholar
• Jarvis GE, Best D, Watson SP. Glycoprotein VI/Fc receptor gamma chain-independent tyrosine phosphorylation and activation of murine platelets by collagen. Biochem J. 2004;383(Pt. 3):581–588.
   PubMed Web of Science ®Google Scholar
• Jarvis GE, Bihan D, Hamaia S, et al. A role for adhesion and degranulation-promoting adapter protein in collagen-induced platelet activation mediated via integrin alpha 2 beta 1. J Thromb Haemostasis. 2012;10(2):268–277.
   PubMed Web of Science ®Google Scholar
• Engelmann S, Togni M, Thielitz A, et al. T cell-independent modulation of experimental autoimmune encephalomyelitis in ADAP-deficient mice. J Immunology. 2013;191(10):4950–4959.
   PubMed Web of Science ®Google Scholar
• Addobbati CJ, De Azevedo Silva J, Tavares NA, et al. Short communication FYB polymorphisms in Brazilian patients with type I diabetes mellitus and autoimmune polyglandular syndrome type III. Genet Mol Res. 2015;14(1):29–33.
   PubMed Web of Science ®Google Scholar
• Addobbati C, Brandao LA, Guimaraes RL, et al. FYB gene polymorphisms are associated with susceptibility for systemic lupus erythemathosus (SLE). Hum Immunol. 2013;74(8):1009–1014.
   PubMed Web of Science ®Google Scholar
• Deleuil F, Mogemark L, Francis MS, et al. Interaction between the Yersinia protein tyrosine phosphatase YopH and eukaryotic Cas/Fyb is an important virulence mechanism. Cell Microbiol. 2003;5(1):53–64.
   PubMed Web of Science ®Google Scholar
• Wei B, Han L, Abbink TE, et al. Immune adaptor ADAP in T cells regulates HIV-1 transcription and cell-cell viral spread via different co-receptors. Retrovirology. 2013;10:101.
   PubMed Web of Science ®Google Scholar
• Singleton KL, Roybal KT, Sun Y, et al. Spatiotemporal patterning during T cell activation is highly diverse. Sci Signal. 2009;2(65):ra15.
   PubMed Web of Science ®Google Scholar