Adhesion and degranulation promoting adapter protein (ADAP) is a central hub for phosphotyrosine-mediated interactions in T cells

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Sylvester, Marc ^a,b,f   Kliche, Stefanie ^c   Lange, Sabine ^a   Geithner, Sabine ^a,b   Klemm, Clementine ^a   Schlosser, Andreas ^d,g   Großmann, Arndt ^e   Stelzl, Ulrich ^e   Schraven, Burkhart ^c   Krause, Eberhard ^a   Freund, Christian ^a,b  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^f UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^g UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADHESION AND DEGRANULATION PROMOTING ADAPTER PROTEIN; CELL PROTEIN; CRK LIKE PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; INTEGRIN; NCK PROTEIN; PEPTIDE; PHENYLALANINE; PHOSPHOLIPASE C GAMMA; PHOSPHOTYROSINE; PROTEIN GADS; PROTEIN SH3; PROTEIN YDDV; UNCLASSIFIED DRUG; FYB PROTEIN, HUMAN; ONCOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TYROSINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; ISOTOPE LABELING; LEUKEMIA CELL LINE; LEUKOCYTE ADHERENCE; LYMPHOCYTE MIGRATION; MASS SPECTROMETRY; MOLECULAR WEIGHT; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION; CELL ADHESION; CELL MOTION; CHEMISTRY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; T LYMPHOCYTE; TWO HYBRID SYSTEM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; CELL ADHESION; CELL MOVEMENT; HUMANS; JURKAT CELLS; ONCOGENE PROTEINS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN BINDING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; T-LYMPHOCYTES; TWO-HYBRID SYSTEM TECHNIQUES; TYROSINE;

EID: 77955343608     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011708     Document Type: Article

References (54)

1. Dustin ML, Bivona TG, Philips MR (2004) Membranes as messengers in T cell adhesion signaling. Nat Immunol 5: 363-372.
2. Griffiths EK, Krawczyk C, Kong YY, Raab M, Hyduk SJ, et al. (2001) Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293: 2260-2263.
3. Boerth NJ, Judd BA, Koretzky GA (2000) Functional association between SLAP- 130 and SLP-76 in Jurkat T cells. JBiolChem 275: 5143-5152.
4. Peterson EJ, Woods ML, Dmowski SA, Derimanov G, Jordan MS, et al. (2001) Coupling of the TCR to integrin activation by Slap-130/Fyb. Science 293: 2263-2265.
5. da Silva AJ, Janssen O, Rudd CE (1993) T cell receptor zeta/CD3-p59fyn(T)-associated p120/130 binds to the SH2 domain of p59fyn(T). JExpMed 178: 2107-2113.
6. Heuer K, Arbuzova A, Strauss H, Kofler M, Freund C (2005) The helically extended SH3 domain of the T cell adaptor protein ADAP is a novel lipid interaction domain. J Mol Biol 348: 1025-1035.
7. Heuer K, Kofler M, Langdon G, Thiemke K, Freund C (2004) Structure of a helically extended SH3 domain of the T cell adapter protein ADAP. Structure 12: 603-610.
8. Piotukh K, Kosslick D, Zimmermann J, Krause E, Freund C (2007) Reversible disulfide bond formation of intracellular proteins probed by NMR spectroscopy. Free Radical Biology and Medicine 43: 1263-1270.
9. Zimmermann J, Kuhne R, Sylvester M, Freund C (2007) Redox-regulated conformational changes in an SH3 domain. Biochemistry 46: 6971-6977.
10. Raab M, Kang H, da Silva A, Zhu X, Rudd CE (1999) 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 Thema. JBiolChem 274: 21170-21179.
11. Geng L, Raab M, Rudd CE (1999) 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. JImmunol 163: 5753-5757.
12. Bezman N, Koretzky GA (2007) Compartmentalization of ITAM and integrin signaling by adapter molecules. Immunol Rev 218: 9-28.
13. Wang H, McCann FE, Gordan JD, Wu X, Raab M, et al. (2004) ADAP-SLP-76 binding differentially regulates supramolecular activation cluster (SMAC) formation relative to T cell-APC conjugation. JExpMed 200: 1063-1074.
14. 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.
15. Musci MA, Hendricks-Taylor LR, Motto DG, Paskind M, Kamens J, et al. (1997) Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. JBiolChem 272: 11674-11677.
16. Machida K, Thompson CM, Dierck K, Jablonowski K, Karkkainen S, et al. (2007) High-throughput phosphotyrosine profiling using SH2 domains. Mol Cell 26: 899-915.
17. DeLano WL. (2002) The PyMOL Molecular Graphics System. http://www.pymol.org.
18. 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.
19. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, et al. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1: 376-386.
20. Kliche S, Breitling D, Togni M, Pusch R, Heuer K, et al. (2006) The ADAP/SKAP55 Signaling Module Regulates T-Cell Receptor-Mediated Integrin Activation through Plasma Membrane Targeting of Rap1. Mol Cell Biol 26: 7130-7144.
21. Heuer K, Sylvester M, Kliche S, Pusch R, Thiemke K, et al. (2006) Lipid-binding hSH3 domains in immune cell adapter proteins. J Mol Biol 361: 94-104.
22. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, et al. (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122: 957-968.
23. Goehler H, Lalowski M, Stelzl U, Waelter S, Stroedicke M, et al. (2004) A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol Cell 15: 853-865.
24. Klemm C, Otto S, Wolf C, Haseloff RF, Beyermann M, et al. (2006) Evaluation of the titanium dioxide approach for MS analysis of phosphopeptides. J Mass Spectrom 41: 1623-1632.
25. Trojan P, Rausch S, Giebl A, Klemm C, Krause E, et al. (2008) Light-dependent CK2-mediated phosphorylation of centrins regulates complex formation with visual G-protein. Biochim Biophys Acta 1783: 1248-1260.
26. Schlosser A, Vanselow JT, Kramer A (2005) Mapping of phosphorylation sites by a multi-protease approach with specific phosphopeptide enrichment and NanoLC-MS/MS analysis. Anal Chem 77: 5243-5250.
27. Hunter AJ, Ottoson N, Boerth N, Koretzky GA, Shimizu Y (2000) Cutting edge: a novel function for the SLAP-130/FYB adapter protein in beta 1 integrin signaling and T lymphocyte migration. JImmunol 164: 1143-1147.
28. Bubeck Wardenburg J, Pappu R, Bu JY, Mayer B, Chernoff J, et al. (1998) Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity 9: 607-616.
29. Wunderlich L, Farago A, Downward J, Buday L (1999) Association of Nck with tyrosine-phosphorylated SLP-76 in activated T lymphocytes. Eur J Immunol 29: 1068-1075.
30. Li L, Wu C, Huang H, Zhang K, Gan J, et al. (2008) Prediction of phosphotyrosine signaling networks using a scoring matrix-assisted ligand identification approach. Nucleic Acids Res 36: 3263-3273.
31. Huang H, Li L, Wu C, Schibli D, Colwill K, et al. (2008) Defining the specificity space of the human SRC homology 2 domain. Mol Cell Proteomics 7: 768-784.
32. Krause M, Sechi AS, Konradt M, Monner D, Gertler FB, et al. (2000) Fynbinding protein (Fyb)/SLP-76-associated protein (SLAP), Ena/vasodilatorstimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. JCell Biol 149: 181-194.
33. Brill LM, Salomon AR, Ficarro SB, Mukherji M, Stettler-Gill M, et al. (2004) Robust phosphoproteomic profiling of tyrosine phosphorylation sites from human T cells using immobilized metal affinity chromatography and tandem mass spectrometry. AnalChem 76: 2763-2772.
34. Ficarro SB, Salomon AR, Brill LM, Mason DE, Stettler-Gill M, et al. (2005) Automated immobilized metal affinity chromatography/nano-liquid chromatography/electrospray ionization mass spectrometry platform for profiling protein phosphorylation sites. Rapid Commun Mass Spectrom 19: 57-71.
35. Zahedi RP, Lewandrowski U, Wiesner J, Wortelkamp S, Moebius J, et al. (2008) Phosphoproteome of resting human platelets. J Proteome Res 7: 526-534.
36. Goss VL, Lee KA, Moritz A, Nardone J, Spek EJ, et al. (2006) A common phosphotyrosine signature for the Bcr-Abl kinase. Blood 107: 4888-4897.
37. Autiero M, Waltenberger J, Communi D, Kranz A, Moons L, et al. (2003) Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med 9: 936-943.
38. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, et al. (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131: 1190-1203.
39. Mulhern TD, Shaw GL, Morton CJ, Day AJ, Campbell ID (1997) The SH2 domain from the tyrosine kinase Fyn in complex with a phosphotyrosyl peptide reveals insights into domain stability and binding specificity. Structure 5: 1313-1323.
40. da Silva AJ, Li Z, de Vera C, Canto E, Findell P, et al. (1997) Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production Thema. ProcNatlAcadSciUSA 94: 7493-7498.
41. Miller ML, Hanke S, Hinsby AM, Friis C, Brunak S, et al. (2008) Motif decomposition of the phosphotyrosine proteome reveals a new N-terminal binding motif for SHIP2. Mol Cell Proteomics 7: 181-192.
42. Kosco KA, Cerignoli F, Williams S, Abraham RT, Mustelin T (2008) SKAP55 modulates T cell antigen receptor-induced activation of the Ras-Erk-AP1 pathway by binding RasGRP1. Molecular Immunology 45: 510-522.
43. Schneider H, Wang H, Raab M, Valk E, Smith X, et al. (2008) Adaptor SKAP- 55 Binds p21 Activating Exchange Factor RasGRP1 and Negatively Regulates the p21-ERK Pathway in T-Cells. PLoS ONE 3: e1718.
44. Torti M, Lapetina EG (1992) Role of rap1B and p21ras GTPase-activating protein in the regulation of phospholipase C-gamma 1 in human platelets. Proc Natl Acad Sci U S A 89: 7796-7800.
45. Lettau M, Pieper J, Gerneth A, Lengl-Janssen B, Voss M, et al. (2010) The adapter protein Nck: Role of individual SH3 and SH2 binding modules for protein interactions in T lymphocytes. Protein Sci 19: 658-669.
46. Okabe S, Tauchi T, Ohyashiki K, Broxmeyer HE (2006) Stromal-cell-derived factor-1/CXCL12-induced chemotaxis of a T cell line involves intracellular signaling through Cbl and Cbl-b and their regulation by Src kinases and CD45. Blood Cells Mol Dis 36: 308-314.
47. Wu C, Ma MH, Brown KR, Geisler M, Li L, et al. (2007) Systematic identification of SH3 domain-mediated human protein-protein interactions by peptide array target screening. Proteomics 7: 1775-1785.
48. Coppolino MG, Krause M, Hagendorff P, Monner DA, Trimble W, et al. (2001) Evidence for a molecular complex consisting of Fyb/SLAP, SLP-76, Nck, VASP and WASP that links the actin cytoskeleton to Fcgamma receptor signaling during phagocytosis. JCell Sci 114: 4307-4318.
49. Breitsprecher D, Kiesewetter AK, Linkner J, Urbanke C, Resch GP, et al. (2008) Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. Embo J 27: 2943-2954.
50. Xue Y, Ren J, Gao X, Jin C, Wen L, et al. (2008) GPS 2.0: Prediction of kinasespecific phosphorylation sites in hierarchy. Mol Cell Proteomics 7: 1598-1608.
51. Marie-Cardine A, Kirchgessner H, Schraven B (1999) Molecular alterations of the Fyn-complex occur as late events of human T cell activation. EurJImmunol 29: 1175-1187.
52. Mamchak AA, Sullivan BM, Hou B, Lee LM, Gilden JK, et al. (2008) Normal development and activation but altered cytokine production of Fyn-deficient CD4+ T cells. J Immunol 181: 5374-5385.
53. Cao L, Yu K, Banh C, Nguyen V, Ritz A, et al. (2007) Quantitative timeresolved phosphoproteomic analysis of mast cell signaling. J Immunol 179: 5864-5876.
54. Koga S, Yogo K, Yoshikawa K, Samori H, Goto M, et al. (2005) Physical and functional association of c-Src and adhesion and degranulation-promoting adaptor protein (ADAP) inosteoclastogenesis in vitro. J Biol Chem 280: 31564-31571.