2oq1 Citations

Molecular basis for interaction of the protein tyrosine kinase ZAP-70 with the T-cell receptor.


The crystal structure of the tandem SH2 domains of human ZAP-70 in complex with a peptide derived from the zeta-subunit of the T-cell receptor reveals an unanticipated interaction between the two domains. A coiled coil of alpha-helices connects the two SH2 domains, producing an interface that constitutes one of the two critical phosphotyrosine binding sites. These and other unique features provide the molecular basis for highly selective association of ZAP-70 with the T-cell receptor.

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Reviews citing this publication (43)

  1. Molecular mechanisms of SH2- and PTB-domain-containing proteins in receptor tyrosine kinase signaling. Wagner MJ, Stacey MM, Liu BA, Pawson T. Cold Spring Harb Perspect Biol 5 a008987 (2013)
  2. Spleen tyrosine kinase: an Src family of non-receptor kinase has multiple functions and represents a valuable therapeutic target in the treatment of autoimmune and inflammatory diseases. Ghosh D, Tsokos GC. Autoimmunity 43 48-55 (2010)
  3. ZAP-70: an essential kinase in T-cell signaling. Wang H, Kadlecek TA, Au-Yeung BB, Goodfellow HE, Hsu LY, Freedman TS, Weiss A. Cold Spring Harb Perspect Biol 2 a002279 (2010)
  4. The Src, Syk, and Tec family kinases: distinct types of molecular switches. Bradshaw JM. Cell. Signal. 22 1175-1184 (2010)
  5. Syk-coupled C-type lectin receptors that mediate cellular activation via single tyrosine based activation motifs. Kerrigan AM, Brown GD. Immunol. Rev. 234 335-352 (2010)
  6. ZAP70: a master regulator of adaptive immunity. Fischer A, Picard C, Chemin K, Dogniaux S, le Deist F, Hivroz C. Semin Immunopathol 32 107-116 (2010)
  7. The structure, regulation, and function of ZAP-70. Au-Yeung BB, Deindl S, Hsu LY, Palacios EH, Levin SE, Kuriyan J, Weiss A. Immunol. Rev. 228 41-57 (2009)
  8. Organization of proximal signal initiation at the TCR:CD3 complex. Guy CS, Vignali DA. Immunol. Rev. 232 7-21 (2009)
  9. Kinome signaling through regulated protein-protein interactions in normal and cancer cells. Pawson T, Kofler M. Curr. Opin. Cell Biol. 21 147-153 (2009)
  10. Biochemical signaling pathways for memory T cell recall. Farber DL. Semin. Immunol. 21 84-91 (2009)
  11. Dynamic control of signaling by modular adaptor proteins. Pawson T. Curr. Opin. Cell Biol. 19 112-116 (2007)
  12. Tonic B-cell and viral ITAM signaling: context is everything. Grande SM, Bannish G, Fuentes-Panana EM, Katz E, Monroe JG. Immunol. Rev. 218 214-234 (2007)
  13. Spontaneous development of autoimmune arthritis due to genetic anomaly of T cell signal transduction: Part 1. Sakaguchi S, Sakaguchi N, Yoshitomi H, Hata H, Takahashi T, Nomura T. Semin. Immunol. 18 199-206 (2006)
  14. Reading protein modifications with interaction domains. Seet BT, Dikic I, Zhou MM, Pawson T. Nat. Rev. Mol. Cell Biol. 7 473-483 (2006)
  15. The target discovery process. Egner U, Krätzschmar J, Kreft B, Pohlenz HD, Schneider M. Chembiochem 6 468-479 (2005)
  16. WW or WoW: the WW domains in a union of bliss. Sudol M, Recinos CC, Abraczinskas J, Humbert J, Farooq A. IUBMB Life 57 773-778 (2005)
  17. Spleen tyrosine kinase (Syk) as a novel target for allergic asthma and rhinitis. Ulanova M, Duta F, Puttagunta L, Schreiber AD, Befus AD. Expert Opin. Ther. Targets 9 901-921 (2005)
  18. The formation and functions of the 21- and 23-kDa tyrosine-phosphorylated TCR zeta subunits. Pitcher LA, Young JA, Mathis MA, Wrage PC, Bartók B, van Oers NS. Immunol. Rev. 191 47-61 (2003)
  19. T-cell receptor signal transmission: who gives an ITAM? Pitcher LA, van Oers NS. Trends Immunol. 24 554-560 (2003)
  20. SH2 and PTB domains in tyrosine kinase signaling. Schlessinger J, Lemmon MA. Sci. STKE 2003 RE12 (2003)
  21. On the mechanism coupling phospholipase Cgamma1 to the B- and T-cell antigen receptors. Bonvini E, DeBell KE, Verí MC, Graham L, Stoica B, Laborda J, Aman MJ, DiBaldassarre A, Miscia S, Rellahan BL. Adv. Enzyme Regul. 43 245-269 (2003)
  22. Molecular mechanisms for protein kinase A-mediated modulation of immune function. Torgersen KM, Vang T, Abrahamsen H, Yaqub S, Taskén K. Cell. Signal. 14 1-9 (2002)
  23. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Samelson LE. Annu. Rev. Immunol. 20 371-394 (2002)
  24. Intracellular signaling by the killer immunoglobulin-like receptors and Ly49. McVicar DW, Burshtyn DN. Sci. STKE 2001 re1 (2001)
  25. Src inhibitors: genomics to therapeutics. Sawyer T, Boyce B, Dalgarno D, Iuliucci J. Expert Opin Investig Drugs 10 1327-1344 (2001)
  26. Lymphocyte antigen receptor signal integration and regulation by the SHC adaptor. Baldari CT, Telford JL. Biol. Chem. 380 129-134 (1999)
  27. The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Germain RN, Stefanová I. Annu. Rev. Immunol. 17 467-522 (1999)
  28. Genetic analysis of B cell antigen receptor signaling. Kurosaki T. Annu. Rev. Immunol. 17 555-592 (1999)
  29. SH2 domains: from structure to energetics, a dual approach to the study of structure-function relationships. Grucza RA, Bradshaw JM, Fütterer K, Waksman G. Med Res Rev 19 273-293 (1999)
  30. Src homology-2 domains: structure, mechanisms, and drug discovery. Sawyer TK. Biopolymers 47 243-261 (1998)
  31. The Syk family of protein tyrosine kinases in T-cell activation and development. Chu DH, Morita CT, Weiss A. Immunol. Rev. 165 167-180 (1998)
  32. Leukocyte protein tyrosine kinases: potential targets for drug discovery. Bolen JB, Brugge JS. Annu. Rev. Immunol. 15 371-404 (1997)
  33. SH2 and PTB domain interactions in tyrosine kinase signal transduction. Shoelson SE. Curr Opin Chem Biol 1 227-234 (1997)
  34. Protein tyrosine kinases in thymocyte development. Cheng AM, Chan AC. Curr. Opin. Immunol. 9 528-533 (1997)
  35. Modular peptide recognition domains in eukaryotic signaling. Kuriyan J, Cowburn D. Annu Rev Biophys Biomol Struct 26 259-288 (1997)
  36. Molecular mechanisms in B cell antigen receptor signaling. Kurosaki T. Curr. Opin. Immunol. 9 309-318 (1997)
  37. Initiation and processing of signals from the B cell antigen receptor. Reth M, Wienands J. Annu. Rev. Immunol. 15 453-479 (1997)
  38. Biophysical studies of T-cell receptors and their ligands. Fremont DH, Rees WA, Kozono H. Curr. Opin. Immunol. 8 93-100 (1996)
  39. Structure and function of the T-cell receptor: insights from X-ray crystallography. Fields BA, Mariuzza RA. Immunol. Today 17 330-336 (1996)
  40. Immunodeficiencies caused by genetic defects in protein kinases. Notarangelo LD. Curr. Opin. Immunol. 8 448-453 (1996)
  41. Complex complexes: signaling at the TCR. Wange RL, Samelson LE. Immunity 5 197-205 (1996)
  42. Cation-pi bonding and amino-aromatic interactions in the biomolecular recognition of substituted ammonium ligands. Scrutton NS, Raine AR. Biochem. J. 319 ( Pt 1) 1-8 (1996)
  43. The role of CTLA-4 in the regulation and initiation of T-cell responses. Chambers CA, Krummel MF, Boitel B, Hurwitz A, Sullivan TJ, Fournier S, Cassell D, Brunner M, Allison JP. Immunol. Rev. 153 27-46 (1996)

Articles citing this publication (81)

  1. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Jones RB, Gordus A, Krall JA, MacBeath G. Nature 439 168-174 (2006)
  2. Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif. Xu C, Gagnon E, Call ME, Schnell JR, Schwieters CD, Carman CV, Chou JJ, Wucherpfennig KW. Cell 135 702-713 (2008)
  3. Lck regulates the tyrosine phosphorylation of the T cell receptor subunits and ZAP-70 in murine thymocytes. van Oers NS, Killeen N, Weiss A. J. Exp. Med. 183 1053-1062 (1996)
  4. Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Deindl S, Kadlecek TA, Brdicka T, Cao X, Weiss A, Kuriyan J. Cell 129 735-746 (2007)
  5. Structure of the IRS-1 PTB domain bound to the juxtamembrane region of the insulin receptor. Eck MJ, Dhe-Paganon S, Trüb T, Nolte RT, Shoelson SE. Cell 85 695-705 (1996)
  6. Genetic evidence for differential coupling of Syk family kinases to the T-cell receptor: reconstitution studies in a ZAP-70-deficient Jurkat T-cell line. Williams BL, Schreiber KL, Zhang W, Wange RL, Samelson LE, Leibson PJ, Abraham RT. Mol. Cell. Biol. 18 1388-1399 (1998)
  7. CXCR4 physically associates with the T cell receptor to signal in T cells. Kumar A, Humphreys TD, Kremer KN, Bramati PS, Bradfield L, Edgar CE, Hedin KE. Immunity 25 213-224 (2006)
  8. The C-type lectin receptors CLEC-2 and Dectin-1, but not DC-SIGN, signal via a novel YXXL-dependent signaling cascade. Fuller GL, Williams JA, Tomlinson MG, Eble JA, Hanna SL, Pöhlmann S, Suzuki-Inoue K, Ozaki Y, Watson SP, Pearce AC. J. Biol. Chem. 282 12397-12409 (2007)
  9. Phosphotyrosines in the killer cell inhibitory receptor motif of NKB1 are required for negative signaling and for association with protein tyrosine phosphatase 1C. Fry AM, Lanier LL, Weiss A. J. Exp. Med. 184 295-300 (1996)
  10. Vinexin: a novel vinculin-binding protein with multiple SH3 domains enhances actin cytoskeletal organization. Kioka N, Sakata S, Kawauchi T, Amachi T, Akiyama SK, Okazaki K, Yaen C, Yamada KM, Aota S. J. Cell Biol. 144 59-69 (1999)
  11. Structural basis for Syk tyrosine kinase ubiquity in signal transduction pathways revealed by the crystal structure of its regulatory SH2 domains bound to a dually phosphorylated ITAM peptide. Fütterer K, Wong J, Grucza RA, Chan AC, Waksman G. J. Mol. Biol. 281 523-537 (1998)
  12. Letter Structural basis for specificity of Grb2-SH2 revealed by a novel ligand binding mode. Rahuel J, Gay B, Erdmann D, Strauss A, Garcia-Echeverría C, Furet P, Caravatti G, Fretz H, Schoepfer J, Grütter MG. Nat. Struct. Biol. 3 586-589 (1996)
  13. Supramodular structure and synergistic target binding of the N-terminal tandem PDZ domains of PSD-95. Long JF, Tochio H, Wang P, Fan JS, Sala C, Niethammer M, Sheng M, Zhang M. J. Mol. Biol. 327 203-214 (2003)
  14. RANTES induces tyrosine kinase activity of stably complexed p125FAK and ZAP-70 in human T cells. Bacon KB, Szabo MC, Yssel H, Bolen JB, Schall TJ. J. Exp. Med. 184 873-882 (1996)
  15. The structural basis for terminator recognition by the Rho transcription termination factor. Bogden CE, Fass D, Bergman N, Nichols MD, Berger JM. Mol. Cell 3 487-493 (1999)
  16. ErbB3 (HER3) interaction with the p85 regulatory subunit of phosphoinositide 3-kinase. Hellyer NJ, Cheng K, Koland JG. Biochem. J. 333 ( Pt 3) 757-763 (1998)
  17. Partially phosphorylated T cell receptor zeta molecules can inhibit T cell activation. Kersh EN, Kersh GJ, Allen PM. J. Exp. Med. 190 1627-1636 (1999)
  18. Crystal structure of the PI 3-kinase p85 amino-terminal SH2 domain and its phosphopeptide complexes. Nolte RT, Eck MJ, Schlessinger J, Shoelson SE, Harrison SC. Nat. Struct. Biol. 3 364-374 (1996)
  19. Differential association of protein tyrosine kinases with the T cell receptor is linked to the induction of anergy and its prevention by B7 family-mediated costimulation. Boussiotis VA, Barber DL, Lee BJ, Gribben JG, Freeman GJ, Nadler LM. J. Exp. Med. 184 365-376 (1996)
  20. C2 domain conformational changes in phospholipase C-delta 1. Grobler JA, Essen LO, Williams RL, Hurley JH. Nat. Struct. Biol. 3 788-795 (1996)
  21. Enhancement of lymphocyte responsiveness by a gain-of-function mutation of ZAP-70. Zhao Q, Weiss A. Mol. Cell. Biol. 16 6765-6774 (1996)
  22. The Tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding. Charier G, Couprie J, Alpha-Bazin B, Meyer V, Quéméneur E, Guérois R, Callebaut I, Gilquin B, Zinn-Justin S. Structure 12 1551-1562 (2004)
  23. A hypomorphic allele of ZAP-70 reveals a distinct thymic threshold for autoimmune disease versus autoimmune reactivity. Hsu LY, Tan YX, Xiao Z, Malissen M, Weiss A. J. Exp. Med. 206 2527-2541 (2009)
  24. ZAP-70 association with T cell receptor zeta (TCRzeta): fluorescence imaging of dynamic changes upon cellular stimulation. Sloan-Lancaster J, Presley J, Ellenberg J, Yamazaki T, Lippincott-Schwartz J, Samelson LE. J. Cell Biol. 143 613-624 (1998)
  25. The p56lck SH2 domain mediates recruitment of CD8/p56lck to the activated T cell receptor/CD3/zeta complex. Thome M, Germain V, DiSanto JP, Acuto O. Eur. J. Immunol. 26 2093-2100 (1996)
  26. A tandem SH2 domain in transcription elongation factor Spt6 binds the phosphorylated RNA polymerase II C-terminal repeat domain (CTD). Sun M, Larivière L, Dengl S, Mayer A, Cramer P. J. Biol. Chem. 285 41597-41603 (2010)
  27. Proximity and orientation underlie signaling by the non-receptor tyrosine kinase ZAP70. Graef IA, Holsinger LJ, Diver S, Schreiber SL, Crabtree GR. EMBO J. 16 5618-5628 (1997)
  28. Phosphorylation of Tyr342 in the linker region of Syk is critical for Fc epsilon RI signaling in mast cells. Zhang J, Berenstein E, Siraganian RP. Mol. Cell. Biol. 22 8144-8154 (2002)
  29. Solution structure of the C-terminal SH2 domain of the human tyrosine kinase Syk complexed with a phosphotyrosine pentapeptide. Narula SS, Yuan RW, Adams SE, Green OM, Green J, Philips TB, Zydowsky LD, Botfield MC, Hatada M, Laird ER. Structure 3 1061-1073 (1995)
  30. Structure of a specific peptide complex of the carboxy-terminal SH2 domain from the p85 alpha subunit of phosphatidylinositol 3-kinase. Breeze AL, Kara BV, Barratt DG, Anderson M, Smith JC, Luke RW, Best JR, Cartlidge SA. EMBO J. 15 3579-3589 (1996)
  31. Solution structure of the C-terminal SH2 domain of the p85 alpha regulatory subunit of phosphoinositide 3-kinase. Siegal G, Davis B, Kristensen SM, Sankar A, Linacre J, Stein RC, Panayotou G, Waterfield MD, Driscoll PC. J. Mol. Biol. 276 461-478 (1998)
  32. Tyr130 phosphorylation triggers Syk release from antigen receptor by long-distance conformational uncoupling. Zhang Y, Oh H, Burton RA, Burgner JW, Geahlen RL, Post CB. Proc. Natl. Acad. Sci. U.S.A. 105 11760-11765 (2008)
  33. ZAP-70 tyrosine kinase is required for LFA-1-dependent T cell migration. Soede RD, Wijnands YM, Van Kouteren-Cobzaru I, Roos E. J. Cell Biol. 142 1371-1379 (1998)
  34. Intramolecular interactions of the regulatory domains of the Bcr-Abl kinase reveal a novel control mechanism. Nam HJ, Haser WG, Roberts TM, Frederick CA. Structure 4 1105-1114 (1996)
  35. Noncanonical tandem SH2 enables interaction of elongation factor Spt6 with RNA polymerase II. Diebold ML, Loeliger E, Koch M, Winston F, Cavarelli J, Romier C. J. Biol. Chem. 285 38389-38398 (2010)
  36. Structural basis for the high affinity of amino-aromatic SH2 phosphopeptide ligands. Rahuel J, García-Echeverría C, Furet P, Strauss A, Caravatti G, Fretz H, Schoepfer J, Gay B. J. Mol. Biol. 279 1013-1022 (1998)
  37. The CD3 zeta subunit contains a phosphoinositide-binding motif that is required for the stable accumulation of TCR-CD3 complex at the immunological synapse. DeFord-Watts LM, Dougall DS, Belkaya S, Johnson BA, Eitson JL, Roybal KT, Barylko B, Albanesi JP, Wülfing C, van Oers NS. J. Immunol. 186 6839-6847 (2011)
  38. The kinase, SH3, and SH2 domains of Lck play critical roles in T-cell activation after ZAP-70 membrane localization. Yamasaki S, Takamatsu M, Iwashima M. Mol. Cell. Biol. 16 7151-7160 (1996)
  39. Requirement for tyrosine residues 315 and 319 within zeta chain-associated protein 70 for T cell development. Gong Q, Jin X, Akk AM, Foger N, White M, Gong G, Bubeck Wardenburg J, Chan AC. J. Exp. Med. 194 507-518 (2001)
  40. Specificity and autoregulation of Notch binding by tandem WW domains in suppressor of Deltex. Jennings MD, Blankley RT, Baron M, Golovanov AP, Avis JM. J. Biol. Chem. 282 29032-29042 (2007)
  41. Structural basis for activation of ZAP-70 by phosphorylation of the SH2-kinase linker. Yan Q, Barros T, Visperas PR, Deindl S, Kadlecek TA, Weiss A, Kuriyan J. Mol. Cell. Biol. 33 2188-2201 (2013)
  42. The SH2 domain from the tyrosine kinase Fyn in complex with a phosphotyrosyl peptide reveals insights into domain stability and binding specificity. Mulhern TD, Shaw GL, Morton CJ, Day AJ, Campbell ID. Structure 5 1313-1323 (1997)
  43. Functional analysis of immunoreceptor tyrosine-based activation motif (ITAM)-mediated signal transduction: the two YxxL segments within a single CD3zeta-ITAM are functionally distinct. Sunder-Plassmann R, Lialios F, Madsen M, Koyasu S, Reinherz EL. Eur. J. Immunol. 27 2001-2009 (1997)
  44. Interdomain B in ZAP-70 regulates but is not required for ZAP-70 signaling function in lymphocytes. Zhao Q, Williams BL, Abraham RT, Weiss A. Mol. Cell. Biol. 19 948-956 (1999)
  45. Crystal structure of the C-terminal SH2 domain of the p85alpha regulatory subunit of phosphoinositide 3-kinase: an SH2 domain mimicking its own substrate. Hoedemaeker FJ, Siegal G, Roe SM, Driscoll PC, Abrahams JP. J. Mol. Biol. 292 763-770 (1999)
  46. Structural and biophysical characterization of the Syk activation switch. Grädler U, Schwarz D, Dresing V, Musil D, Bomke J, Frech M, Greiner H, Jäkel S, Rysiok T, Müller-Pompalla D, Wegener A. J. Mol. Biol. 425 309-333 (2013)
  47. Stimulatory Effect of β-glucans on Immune Cells. Kim HS, Hong JT, Kim Y, Han SB. Immune Netw 11 191-195 (2011)
  48. Structural and functional evidence that Nck interaction with CD3epsilon regulates T-cell receptor activity. Takeuchi K, Yang H, Ng E, Park SY, Sun ZY, Reinherz EL, Wagner G. J. Mol. Biol. 380 704-716 (2008)
  49. Differential impact of the transcriptional repressor Gfi1 on mature CD4+ and CD8+ T lymphocyte function. Pargmann D, Yücel R, Kosan C, Saba I, Klein-Hitpass L, Schimmer S, Heyd F, Dittmer U, Möröy T. Eur. J. Immunol. 37 3551-3563 (2007)
  50. Structure induction of the T-cell receptor zeta-chain upon lipid binding investigated by NMR spectroscopy. Duchardt E, Sigalov AB, Aivazian D, Stern LJ, Schwalbe H. Chembiochem 8 820-827 (2007)
  51. Backbone dynamics of the C-terminal SH2 domain of the p85alpha subunit of phosphoinositide 3-kinase: effect of phosphotyrosine-peptide binding and characterization of slow conformational exchange processes. Kristensen SM, Siegal G, Sankar A, Driscoll PC. J. Mol. Biol. 299 771-788 (2000)
  52. Signaling efficiency of the T cell receptor controlled by a single amino acid in the beta chain constant region. Bäckström BT, Hausmann BT, Palmer E. J. Exp. Med. 186 1933-1938 (1997)
  53. Alternative modes of binding of proteins with tandem SH2 domains. O'Brien R, Rugman P, Renzoni D, Layton M, Handa R, Hilyard K, Waterfield MD, Driscoll PC, Ladbury JE. Protein Sci. 9 570-579 (2000)
  54. Mechanism of activation for Zap-70 catalytic activity. LoGrasso PV, Hawkins J, Frank LJ, Wisniewski D, Marcy A. Proc. Natl. Acad. Sci. U.S.A. 93 12165-12170 (1996)
  55. T-cell receptor-mediated anergy of a human immunodeficiency virus (HIV) gp120-specific CD4(+) cytotoxic T-cell clone, induced by a natural HIV type 1 variant peptide. Bouhdoud L, Villain P, Merzouki A, Arella M, Couture C. J. Virol. 74 2121-2130 (2000)
  56. Stability of an autoinhibitory interface in the structure of the tyrosine kinase ZAP-70 impacts T cell receptor response. Deindl S, Kadlecek TA, Cao X, Kuriyan J, Weiss A. Proc. Natl. Acad. Sci. U.S.A. 106 20699-20704 (2009)
  57. Protein flexibility and ligand rigidity: a thermodynamic and kinetic study of ITAM-based ligand binding to Syk tandem SH2. de Mol NJ, Catalina MI, Dekker FJ, Fischer MJ, Heck AJ, Liskamp RM. Chembiochem 6 2261-2270 (2005)
  58. Conformation-dependent intermolecular interaction energies of the triphosphate anion with divalent metal cations. Application to the ATP-binding site of a binuclear bacterial enzyme. A parallel quantum chemical and polarizable molecular mechanics investigation. Gresh N, Shi GB. J Comput Chem 25 160-168 (2004)
  59. Type II phosphatidylinositol 4-kinase beta associates with TCR-CD3 zeta chain in Jurkat cells. Srivastava R, Sinha RK, Subrahmanyam G. Mol. Immunol. 43 454-463 (2006)
  60. A comprehensive characterization of the T-cell antigen receptor complex composition by microcapillary liquid chromatography-tandem mass spectrometry. Heller M, Goodlett DR, Watts JD, Aebersold R. Electrophoresis 21 2180-2195 (2000)
  61. Phosphorylated T cell receptor zeta-chain and ZAP70 tandem SH2 domains form a 1:3 complex in vitro. Weissenhorn W, Eck MJ, Harrison SC, Wiley DC. Eur. J. Biochem. 238 440-445 (1996)
  62. T cell receptor dwell times control the kinase activity of Zap70. Klammt C, Novotná L, Li DT, Wolf M, Blount A, Zhang K, Fitchett JR, Lillemeier BF. Nat. Immunol. 16 961-969 (2015)
  63. Phosphorylation site dynamics of early T-cell receptor signaling. Chylek LA, Akimov V, Dengjel J, Rigbolt KT, Hu B, Hlavacek WS, Blagoev B. PLoS ONE 9 e104240 (2014)
  64. Application of azide-alkyne cycloaddition 'click chemistry' for the synthesis of Grb2 SH2 domain-binding macrocycles. Choi WJ, Shi ZD, Worthy KM, Bindu L, Karki RG, Nicklaus MC, Fisher RJ, Burke TR. Bioorg. Med. Chem. Lett. 16 5265-5269 (2006)
  65. A soluble LAT deletion mutant inhibits T-cell activation: reduced recruitment of signalling molecules to glycolipid-enriched microdomains. Torgersen KM, Vaage JT, Rolstad B, Taskén K. Cell. Signal. 13 213-220 (2001)
  66. The protein tyrosine phosphatase PTPN4/PTP-MEG1, an enzyme capable of dephosphorylating the TCR ITAMs and regulating NF-kappaB, is dispensable for T cell development and/or T cell effector functions. Young JA, Becker AM, Medeiros JJ, Shapiro VS, Wang A, Farrar JD, Quill TA, Hooft van Huijsduijnen R, van Oers NS. Mol. Immunol. 45 3756-3766 (2008)
  67. Binding of a diphosphorylated-ITAM peptide to spleen tyrosine kinase (Syk) induces distal conformational changes: a hydrogen exchange mass spectrometry study. Catalina MI, Fischer MJ, Dekker FJ, Liskamp RM, Heck AJ. J. Am. Soc. Mass Spectrom. 16 1039-1051 (2005)
  68. Nonpeptidic SH2 inhibitors of the tyrosine kinase ZAP-70. Vu CB, Corpuz EG, Pradeepan SG, Violette S, Bartlett C, Sawyer TK. Bioorg. Med. Chem. Lett. 9 3009-3014 (1999)
  69. Analysis of immunoreceptor tyrosine-based activation motif (ITAM) binding to ZAP-70 by surface plasmon resonance. Vély F, Nunès JA, Malissen B, Hedgecock CJ. Eur. J. Immunol. 27 3010-3014 (1997)
  70. The catalytic activity of the kinase ZAP-70 mediates basal signaling and negative feedback of the T cell receptor pathway. Goodfellow HS, Frushicheva MP, Ji Q, Cheng DA, Kadlecek TA, Cantor AJ, Kuriyan J, Chakraborty AK, Salomon A, Weiss A. Sci Signal 8 ra49 (2015)
  71. Fat-1 transgenic cattle as a model to study the function of ω-3 fatty acids. Guo T, Liu XF, Ding XB, Yang FF, Nie YW, An YJ, Guo H. Lipids Health Dis 10 244 (2011)
  72. Interdomain A is crucial for ITAM-dependent and -independent regulation of Syk. Adachi T, Wienands J, Tsubata T, Kurosaki T. Biochem. Biophys. Res. Commun. 364 111-117 (2007)
  73. FcgammaRII tyrosine phosphorylation differs between FcgammaRII cross-linking and platelet-activating anti-platelet monoclonal antibodies. Qi R, Ozaki Y, Asazuma N, Satoh K, Yatomi Y, Law CL, Hato T, Nomura S. Biochim. Biophys. Acta 1451 353-363 (1999)
  74. T cell activation deficiency associated with an aberrant pattern of protein tyrosine phosphorylation after CD3 perturbation in Down's syndrome. Scotese I, Gaetaniello L, Matarese G, Lecora M, Racioppi L, Pignata C. Pediatr. Res. 44 252-258 (1998)
  75. Functional role of T-cell receptor nanoclusters in signal initiation and antigen discrimination. Pageon SV, Tabarin T, Yamamoto Y, Ma Y, Bridgeman JS, Cohnen A, Benzing C, Gao Y, Crowther MD, Tungatt K, Dolton G, Sewell AK, Price DA, Acuto O, Parton RG, Gooding JJ, Rossy J, Rossjohn J, Gaus K. Proc. Natl. Acad. Sci. U.S.A. 113 E5454-63 (2016)
  76. Critical Role for an acidic amino acid region in platelet signaling by the HemITAM (hemi-immunoreceptor tyrosine-based activation motif) containing receptor CLEC-2 (C-type lectin receptor-2). Hughes CE, Sinha U, Pandey A, Eble JA, O'Callaghan CA, Watson SP. J. Biol. Chem. 288 5127-5135 (2013)
  77. Switching between low and high affinity for the Syk tandem SH2 domain by irradiation of azobenzene containing ITAM peptidomimetics. Kuil J, van Wandelen LT, de Mol NJ, Liskamp RM. J. Pept. Sci. 15 685-691 (2009)
  78. Molecular mechanism of selective recruitment of Syk kinases by the membrane antigen-receptor complex. Bond PJ, Faraldo-Gómez JD. J. Biol. Chem. 286 25872-25881 (2011)
  79. Aberrant T-lymphocyte development and function in mice overexpressing human soluble amyloid precursor protein-α: implications for autism. Bailey AR, Hou H, Obregon DF, Tian J, Zhu Y, Zou Q, Nikolic WV, Bengtson M, Mori T, Murphy T, Tan J. FASEB J. 26 1040-1051 (2012)
  80. Crystal structure of Src-like adaptor protein 2 reveals close association of SH3 and SH2 domains through β-sheet formation. Wybenga-Groot LE, McGlade CJ. Cell. Signal. 25 2702-2708 (2013)
  81. SH2 Domains Serve as Lipid-Binding Modules for pTyr-Signaling Proteins. Park MJ, Sheng R, Silkov A, Jung DJ, Wang ZG, Xin Y, Kim H, Thiagarajan-Rosenkranz P, Song S, Yoon Y, Nam W, Kim I, Kim E, Lee DG, Chen Y, Singaram I, Wang L, Jang MH, Hwang CS, Honig B, Ryu S, Lorieau J, Kim YM, Cho W. Mol. Cell 62 7-20 (2016)