Structural and Functional Evidence that Nck Interaction with CD3ε Regulates T-Cell Receptor Activity

Journal of Molecular Biology

Volumn 380, Issue 4, 2008, Pages 704-716

  Takeuchi, Koh ^a   Yang, Hailin ^b   Ng, Elise ^a   Park, Sungh youk ^a,c   Sun, Zhen Yu J ^a   Reinherz, Ellis L ^b   Wagner, Gerhard ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c Inha University School of Medicine   (South Korea)

Author keywords

CD3 ; Nck; nuclear magnetic resonance; phosphorylation; receptor internalization

Indexed keywords

CD3 ANTIGEN; CD3 EPSILON ANTIGEN; NCK PROTEIN; PROTEIN KINASE FYN; PROTEIN KINASE LCK; T LYMPHOCYTE RECEPTOR; TYROSINE;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; LYMPH NODE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; T LYMPHOCYTE;

EID: 45649085424     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.05.037     Document Type: Article

References (51)

1. Wang J.-H., and Reinherz E.L. Structural basis of T cell recognition of peptides bound to MHC molecules. Mol. Immunol. 38 (2002) 1039-1049
2. Qian D., and Weiss A. T cell antigen receptor signal transduction. Curr. Opin. Cell. Biol. 9 (1997) 205-212
3. Werlen G., and Palmer E. The T-cell receptor signalosome: a dynamic structure with expanding complexity. Curr. Opin. Immunol. 14 (2002) 299-305
4. Alarcon B., Gil D., Delgado P., and Schamel W.W. Initiation of TCR signaling: regulation within CD3 dimers. Immunol. Rev. 191 (2003) 38-46
5. Kuhns M.S., Davis M.M., and Garcia K.C. Deconstructing the form and function of the TCR/CD3 complex. Immunity 24 (2006) 133-139
6. Hayes S.M., Shores E.W., and Love P.E. An architectural perspective on signaling by the pre-, alphabeta and gammadelta T cell receptors. Immunol. Rev. 191 (2003) 28-37
7. Sun Z.J., Kim K.S., Wagner G., and Reinherz E.L. Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 epsilon gamma heterodimer. Cell 105 (2001) 913-923
8. Sun Z.Y., Kim S.T., Kim I.C., Fahmy A., Reinherz E.L., and Wagner G. Solution structure of the CD3epsilondelta ectodomain and comparison with CD3epsilongamma as a basis for modeling T cell receptor topology and signaling. Proc. Natl Acad. Sci. USA 101 (2004) 16867-16872
9. Arnett K.L., Harrison S.C., and Wiley D.C. Crystal structure of a human CD3-epsilon/delta dimer in complex with a UCHT1 single-chain antibody fragment. Proc. Natl Acad. Sci. USA 101 (2004) 16268-16273
10. Rudolph M.G., Luz J.G., and Wilson I.A. Structural and thermodynamic correlates of T cell signaling. Annu. Rev. Biophys. Biomol. Struct. 31 (2002) 121-149
11. Garcia K.C., Teyton L., and Wilson I.A. Structural basis of T cell recognition. Annu. Rev. Immunol. 17 (1999) 369-397
12. Pitcher L.A., and van Oers N.S. T-cell receptor signal transmission: who gives an ITAM?. Trends Immunol. 24 (2003) 554-560
13. Underhill D.M., and Goodridge H.S. The many faces of ITAMs. Trends Immunol. 28 (2007) 66-73
14. Cantrell D. T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol. 14 (1996) 259-274
15. Alberola-Ila J., Takaki S., Kerner J.D., and Perlmutter R.M. Differential signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 15 (1997) 125-154
16. Lin J., and Weiss A. T cell receptor signalling. J. Cell Sci. 114 (2001) 243-244
17. Boggon T.J., and Eck M.J. Structure and regulation of Src family kinases. Oncogene 23 (2004) 7918-7927
18. Hatada M.H., Lu X., Laird E.R., Green J., Morgenstern J.P., Lou M., et al. Molecular basis for interaction of the protein tyrosine kinase ZAP-70 with the T-cell receptor. Nature 377 (1995) 32-38
19. Deindl S., Kadlecek T.A., Brdicka T., Cao X., Weiss A., and Kuriyan J. Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 129 (2007) 735-746
20. Gil D., Schamel W.W., Montoya M., Sanchez-Madrid F., and Alarcon B. Recruitment of Nck by CD3 epsilon reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 109 (2002) 901-912
21. Gil D., Schrum A.G., Alarcon B., and Palmer E. T cell receptor engagement by peptide-MHC ligands induces a conformational change in the CD3 complex of thymocytes. J. Exp. Med. 201 (2005) 517-522
22. Borroto A., Lama J., Niedergang F., Dautry-Varsat A., Alarcon B., and Alcover A. The CD3{epsilon} subunit of the TCR contains endocytosis signals. J. Immunol. 163 (1999) 25-31
23. Szymczak A.L., Workman C.J., Gil D., Dilioglou S., Vignali K.M., Palmer E., and Vignali D.A. The CD3epsilon proline-rich sequence, and its interaction with Nck, is not required for T cell development and function. J. Immunol. 175 (2005) 270-275
24. Kesti T., Ruppelt A., Wang J.H., Liss M., Wagner R., Tasken K., and Saksela K. Reciprocal regulation of SH3 and SH2 domain binding via tyrosine phosphorylation of a common site in CD3epsilon. J. Immunol. 179 (2007) 878-885
25. Mongiovi A.M., Romano P.R., Panni S., Mendoza M., Wong W.T., Musacchio A., et al. A novel peptide-SH3 interaction. EMBO J. 18 (1999) 5300-5309
26. Freund C., Kuhne R., Park S., Thiemke K., Reinherz E.L., and Wagner G. Structural investigations of a GYF domain covalently linked to a proline-rich peptide. J. Biomolecular NMR 27 (2003) 143-149
27. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
28. Park S., Takeuchi K., and Wagner G. Solution structure of the first SRC homology 3 domain of human Nck2. J. Biomol. NMR 34 (2006) 203-208
29. Mayer B.J. SH3 domains: complexity in moderation. J. Cell. Sci. 114 (2001) 1253-1263
30. Feng S., Chen J.K., Yu H., Simon J.A., and Schreiber S.L. Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266 (1994) 1241-1247
31. Burley S.K., and Petsko G.A. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229 (1985) 23-28
32. Castagnoli L., Costantini A., Dall'Armi C., Gonfloni S., Montecchi-Palazzi L., Panni S., et al. Selectivity and promiscuity in the interaction network mediated by protein recognition modules. FEBS Lett. 567 (2004) 74-79
33. Gauen L.K., Zhu Y., Letourneur F., Hu Q., Bolen J.B., Matis L.A., et al. Interactions of p59fyn and ZAP-70 with T-cell receptor activation motifs: defining the nature of a signalling motif. Mol. Cell. Biol. 14 (1994) 3729-3741
34. Mingueneau M., Sansoni A., Gregoire C., Roncagalli R., Aguado E., Weiss A., et al. The proline-rich sequence of CD3epsilon controls T cell antigen receptor expression on and signaling potency in preselection CD4+CD8+ thymocytes. Nat. Immunol. 9 (2008) 522-532
35. Vaynberg J., Fukuda T., Chen K., Vinogradova O., Velyvis A., Tu Y., et al. Structure of an ultraweak protein-protein complex and its crucial role in regulation of cell morphology and motility. Mol. Cell. 17 (2005) 513-523
36. Qualmann B., and Kessels M.M. Endocytosis and the cytoskeleton. Int. Rev. Cytol. 220 (2002) 93-144
37. Yang H., and Reinherz E.L. CD2BP1 modulates CD2-dependent T cell activation via linkage to protein tyrosine phosphatase (PTP)-PEST. J. Immunol. 176 (2006) 5898-5907
38. Geisler C. TCR trafficking in resting and stimulated T cells. Crit. Rev. Immunol. 24 (2004) 67-86
39. Szymczak A.L., Workman C.J., Wang Y., Vignali K.M., Dilioglou S., Vanin E.F., and Vignali D.A. Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat. Biotechnol. 22 (2004) 589-594
40. McCarty J.H. The Nck SH2/SH3 adaptor protein: a regulator of multiple intracellular signal transduction events. Bioessays 20 (1998) 913-921
41. Zhang J., Shehabeldin A., da Cruz L.A., Butler J., Somani A.K., McGavin M., et al. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J. Exp. Med. 190 (1999) 1329-1342
42. Sebzda E., Mariathasan S., Ohteki T., Jones R., Bachmann M.F., and Ohashi P.S. Selection of the T cell repertoire. Annu. Rev. Immunol. 17 (1999) 829-874
43. Ghendler Y., Hussey R.E., Witte T., Mizoguchi E., Clayton L.K., Bhan A.K., et al. Double-positive T cell receptor(high) thymocytes are resistant to peptide/major histocompatibility complex ligand-induced negative selection. Eur J. Immunol. 27 (1997) 2279-2289
44. 15N background for NMR studies of large proteins. J. Biomol. NMR 38 (2007) 89-98
45. Goddard T.D., and Kneller D.G. SPARKY 3-NMR Assignment and Integration Software (2006), University of California, San Francisco, CA
46. Keller R. The Computer Aided Resonance Assignment Tutorial. 1st edit. (2004), CANTINA Verlag, Goldau, CH. 3-85600-112-3
47. 15N-HSQC peaks using high-resolution 3D HNcocaNH experiments with non-uniform sampling. J. Biomol. NMR 33 (2005) 43-50
48. Sun Z.Y., Hyberts S.G., Rovnyak D., Park S., Stern A.S., Hoch J.C., and Wagner G. High-resolution aliphatic side-chain assignments in 3D HCcoNH experiments with joint H-C evolution and non-uniform sampling. J. Biomol. NMR 32 (2005) 55-60
49. Ferentz A.E., and Wagner G. NMR spectroscopy: a multifaceted approach to macromolecular structure. Q. Rev. Biophys. 33 (2000) 29-65
50. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
51. Guntert P., Mumenthaler C., and Wuthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273 (1997) 283-298