A Mechanical Switch Couples T Cell Receptor Triggering to the Cytoplasmic Juxtamembrane Regions of CD3ζζ

Immunity

Volumn 43, Issue 2, 2015, Pages 227-239

  Lee, Mark S ^a   Glassman, Caleb R ^a   Deshpande, Neha R ^a   Badgandi, Hemant B ^a   Parrish, Heather L ^a   Uttamapinant, Chayasith ^b,c   Stawski, Philipp S ^b   Ting, Alice Y ^b   Kuhns, Michael S ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD33 ANTIGEN; T LYMPHOCYTE RECEPTOR; CD3 ANTIGEN; CD3 ANTIGEN, ZETA CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; MULTIPROTEIN COMPLEX;

ARTICLE; CELL FATE; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; PRIORITY JOURNAL; PROTEIN MOTIF; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CYTOPLASM; GENETICS; HUMAN; HYBRIDOMA; IMMUNOLOGY; MECHANOTRANSDUCTION; METABOLISM; MOUSE; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD3; CELL MEMBRANE; CYTOPLASM; HUMANS; HYBRIDOMAS; MECHANOTRANSDUCTION, CELLULAR; MICE; MULTIPROTEIN COMPLEXES; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR CROSS-TALK; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84941024008     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.06.018     Document Type: Article

References (48)

1. Aivazian D., Stern L.J. Phosphorylation of T cell receptor zeta is regulated by a lipid dependent folding transition. Nat. Struct. Biol. 2000, 7:1023-1026.
2. Brdicka T., Kadlecek T.A., Roose J.P., Pastuszak A.W., Weiss A. Intramolecular regulatory switch in ZAP-70: analogy with receptor tyrosine kinases. Mol. Cell. Biol. 2005, 25:4924-4933.
3. Call M.E., Pyrdol J., Wiedmann M., Wucherpfennig K.W. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 2002, 111:967-979.
4. Call M.E., Schnell J.R., Xu C., Lutz R.A., Chou J.J., Wucherpfennig K.W. The structure of the zetazeta transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell 2006, 127:355-368.
5. Constantinescu S.N., Huang L.J., Nam H., Lodish H.F. The erythropoietin receptor cytosolic juxtamembrane domain contains an essential, precisely oriented, hydrophobic motif. Mol. Cell 2001, 7:377-385.
6. Delgado P., Alarcón B. An orderly inactivation of intracellular retention signals controls surface expression of the T cell antigen receptor. J. Exp. Med. 2005, 201:555-566.
7. Endres N.F., Das R., Smith A.W., Arkhipov A., Kovacs E., Huang Y., Pelton J.G., Shan Y., Shaw D.E., Wemmer D.E., et al. Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 2013, 152:543-556.
8. Engelman D.M. Electrostatic fasteners hold the T cell receptor-CD3 complex together. Mol. Cell 2003, 11:5-6.
9. Fernandes R.A., Shore D.A., Vuong M.T., Yu C., Zhu X., Pereira-Lopes S., Brouwer H., Fennelly J.A., Jessup C.M., Evans E.J., et al. T cell receptors are structures capable of initiating signaling in the absence of large conformational rearrangements. J. Biol. Chem. 2012, 287:13324-13335.
10. Gagnon E., Schubert D.A., Gordo S., Chu H.H., Wucherpfennig K.W. Local changes in lipid environment of TCR microclusters regulate membrane binding by the CD3ε cytoplasmic domain. J. Exp. Med. 2012, 209:2423-2439.
11. Gil D., Schamel W.W., Montoya M., Sánchez-Madrid F., Alarcón B. Recruitment of Nck by CD3 epsilon reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 2002, 109:901-912.
12. Guy C.S., Vignali D.A. Organization of proximal signal initiation at the TCR:CD3 complex. Immunol. Rev. 2009, 232:7-21.
13. Huang B., Babcock H., Zhuang X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 2010, 143:1047-1058.
14. Irvine D.J., Purbhoo M.A., Krogsgaard M., Davis M.M. Direct observation of ligand recognition by T cells. Nature 2002, 419:845-849.
15. Kane L.P., Lin J., Weiss A. Signal transduction by the TCR for antigen. Curr. Opin. Immunol. 2000, 12:242-249.
16. Kersh G.J., Kersh E.N., Fremont D.H., Allen P.M. High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling. Immunity 1998, 9:817-826.
17. Kim S.T., Takeuchi K., Sun Z.Y., Touma M., Castro C.E., Fahmy A., Lang M.J., Wagner G., Reinherz E.L. The alphabeta T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 2009, 284:31028-31037.
18. Kuhns M.S., Davis M.M. Disruption of extracellular interactions impairs T cell receptor-CD3 complex stability and signaling. Immunity 2007, 26:357-369.
19. Kuhns M.S., Davis M.M. TCR signaling emerges from the sum of many parts. Front. Immunol. 2012, 3:159.
20. Kuhns M.S., Davis M.M., Garcia K.C. Deconstructing the form and function of the TCR/CD3 complex. Immunity 2006, 24:133-139.
21. Kuhns M.S., Girvin A.T., Klein L.O., Chen R., Jensen K.D., Newell E.W., Huppa J.B., Lillemeier B.F., Huse M., Chien Y.H., et al. Evidence for a functional sidedness to the alphabetaTCR. Proc. Natl. Acad. Sci. USA 2010, 107:5094-5099.
22. Kumar R., Ferez M., Swamy M., Arechaga I., Rejas M.T., Valpuesta J.M., Schamel W.W., Alarcon B., van Santen H.M. Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. Immunity 2011, 35:375-387.
23. Lauritsen J.P., Christensen M.D., Dietrich J., Kastrup J., Odum N., Geisler C. Two distinct pathways exist for down-regulation of the TCR. J. Immunol. 1998, 161:260-267.
24. Li Y.C., Chen B.M., Wu P.C., Cheng T.L., Kao L.S., Tao M.H., Lieber A., Roffler S.R. Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling. J. Immunol. 2010, 184:5959-5963.
25. Liu H., Rhodes M., Wiest D.L., Vignali D.A. On the dynamics of TCR:CD3 complex cell surface expression and downmodulation. Immunity 2000, 13:665-675.
26. Liu B., Chen W., Evavold B.D., Zhu C. Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 2014, 157:357-368.
27. Livnah O., Stura E.A., Middleton S.A., Johnson D.L., Jolliffe L.K., Wilson I.A. Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science 1999, 283:987-990.
28. Lu X., Gross A.W., Lodish H.F. Active conformation of the erythropoietin receptor: random and cysteine-scanning mutagenesis of the extracellular juxtamembrane and transmembrane domains. J. Biol. Chem. 2006, 281:7002-7011.
29. Ma Z., Sharp K.A., Janmey P.A., Finkel T.H. Surface-anchored monomeric agonist pMHCs alone trigger TCR with high sensitivity. PLoS Biol. 2008, 6:e43.
30. Manz B.N., Jackson B.L., Petit R.S., Dustin M.L., Groves J. T-cell triggering thresholds are modulated by the number of antigen within individual T-cell receptor clusters. Proc. Natl. Acad. Sci. USA 2011, 108:9089-9094.
31. Reth M. Antigen receptor tail clue. Nature 1989, 338:383-384.
32. Shi X., Bi Y., Yang W., Guo X., Jiang Y., Wan C., Li L., Bai Y., Guo J., Wang Y., et al. Ca2+ regulates T-cell receptor activation by modulating the charge property of lipids. Nature 2013, 493:111-115.
33. Slavoff S.A., Liu D.S., Cohen J.D., Ting A.Y. Imaging protein-protein interactions inside living cells via interaction-dependent fluorophore ligation. J. Am. Chem. Soc. 2011, 133:19769-19776.
34. Sun Z.J., Kim K.S., Wagner G., 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 2001, 105:913-923.
35. Sun Z.Y., Kim S.T., Kim I.C., Fahmy A., Reinherz E.L., 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 2004, 101:16867-16872.
36. Uttamapinant C., White K.A., Baruah H., Thompson S., Fernández-Suárez M., Puthenveetil S., Ting A.Y. A fluorophore ligase for site-specific protein labeling inside living cells. Proc. Natl. Acad. Sci. USA 2010, 107:10914-10919.
37. Uttamapinant C., Sanchez M.I., Liu D.S., Yao J.Z., Ting A.Y. Site-specific protein labeling using PRIME and chelation-assisted click chemistry. Nat. Protoc. 2013, 8:1620-1634.
38. van der Merwe P.A. The TCR triggering puzzle. Immunity 2001, 14:665-668.
39. Vanderklish P.W., Krushel L.A., Holst B.H., Gally J.A., Crossin K.L., Edelman G.M. Marking synaptic activity in dendritic spines with a calpain substrate exhibiting fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 2000, 97:2253-2258.
40. Xu C., Call M.E., Wucherpfennig K.W. A membrane-proximal tetracysteine motif contributes to assembly of CD3deltaepsilon and CD3gammaepsilon dimers with the T cell receptor. J. Biol. Chem. 2006, 281:36977-36984.
41. Xu C., Gagnon E., Call M.E., Schnell J.R., Schwieters C.D., Carman C.V., Chou J.J., Wucherpfennig K.W. Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif. Cell 2008, 135:702-713.
42. Yamasaki S., Ishikawa E., Sakuma M., Ogata K., Sakata-Sogawa K., Hiroshima M., Wiest D.L., Tokunaga M., Saito T. Mechanistic basis of pre-T cell receptor-mediated autonomous signaling critical for thymocyte development. Nat. Immunol. 2006, 7:67-75.
43. Yang J., Reth M. The dissociation activation model of B cell antigen receptor triggering. FEBS Lett. 2010, 584:4872-4877.
44. Yang J., Ma Y.Q., Page R.C., Misra S., Plow E.F., Qin J. Structure of an integrin alphaIIb beta3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc. Natl. Acad. Sci. USA 2009, 106:17729-17734.
45. Yokosuka T., Sakata-Sogawa K., Kobayashi W., Hiroshima M., Hashimoto-Tane A., Tokunaga M., Dustin M.L., Saito T. Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat. Immunol. 2005, 6:1253-1262.
46. Youvan D.C., Silva C.M., Bylina E.J., Coleman W.J., Dilworth M.R., Yang M.M. Calibration of Fluorescnece Resonance Energy Transfer in Microscopy Using Genetically Engineered GFP Derivatives on Nickle Chelating Beads. Biotechnol. Alia 1997, 3:1-18.
47. Zal T., Gascoigne N.R. Using live FRET imaging to reveal early protein-protein interactions during T cell activation. Curr. Opin. Immunol. 2004, 16:418-427.
48. Zhang H., Cordoba S.P., Dushek O., van der Merwe P.A. Basic residues in the T-cell receptor ζ cytoplasmic domain mediate membrane association and modulate signaling. Proc. Natl. Acad. Sci. USA 2011, 108:19323-19328.