Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling

Cell

Volumn 157, Issue 2, 2014, Pages 357-368

  Liu, Baoyu ^a   Chen, Wei ^a   Evavold, Brian D ^c   Zhu, Cheng ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; PEPTIDE; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ARTICLE; CATCH BOND; CELL KINETICS; CHEMICAL BOND; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; NONHUMAN; PEPTIDE MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE SIGNALING; THROMBOCYTE LIFESPAN;

ANIMALS; ANTIGEN-PRESENTING CELLS; CALCIUM; ERYTHROCYTES; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84898644308     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.02.053     Document Type: Article

References (55)

1. J.J. Adams, S. Narayanan, B. Liu, M.E. Birnbaum, A.C. Kruse, N.A. Bowerman, W. Chen, A.M. Levin, J.M. Connolly, and C. Zhu et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex Immunity 35 2011 681 693
2. S.M. Alam, P.J. Travers, J.L. Wung, W. Nasholds, S. Redpath, S.C. Jameson, and N.R.J. Gascoigne T-cell-receptor affinity and thymocyte positive selection Nature 381 1996 616 620
3. M. Aleksic, O. Dushek, H. Zhang, E. Shenderov, J.-L. Chen, V. Cerundolo, D. Coombs, and P.A. van der Merwe Dependence of T cell antigen recognition on T cell receptor-peptide MHC confinement time Immunity 32 2010 163 174
4. G. Altan-Bonnet, and R.N. Germain Modeling T cell antigen discrimination based on feedback control of digital ERK responses PLoS Biol. 3 2005 e356
5. W. Chen, and C. Zhu Mechanical regulation of T-cell functions Immunol. Rev. 256 2013 160 176
6. W. Chen, E.A. Evans, R.P. McEver, and C. Zhu Monitoring receptor-ligand interactions between surfaces by thermal fluctuations Biophys. J. 94 2008 694 701
7. W. Chen, V.I. Zarnitsyna, K.K. Sarangapani, J. Huang, and C. Zhu Measuring Receptor-Ligand Binding Kinetics on Cell Surfaces: From Adhesion Frequency to Thermal Fluctuation Methods Cell. Mol. Bioeng. 1 2008 276 288
8. S.E. Chesla, P. Selvaraj, and C. Zhu Measuring two-dimensional receptor-ligand binding kinetics by micropipette Biophys. J. 75 1998 1553 1572
9. S.J. Davis, and P.A. van der Merwe The kinetic-segregation model: TCR triggering and beyond Nat. Immunol. 7 2006 803 809
10. O. Dushek, R. Das, and D. Coombs A role for rebinding in rapid and reliable T cell responses to antigen PLoS Comput. Biol. 5 2009 e1000578
11. E. Evans, K. Ritchie, and R. Merkel Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces Biophys. J. 68 1995 2580 2587
12. N.R. Gascoigne, T. Zal, and S.M. Alam T-cell receptor binding kinetics in T-cell development and activation Expert Rev. Mol. Med. 2001 2001 1 17
13. M. Howarth, D.J. Chinnapen, K. Gerrow, P.C. Dorrestein, M.R. Grandy, N.L. Kelleher, A. El-Husseini, and A.Y. Ting A monovalent streptavidin with a single femtomolar biotin binding site Nat. Methods 3 2006 267 273
14. J.F. Huang, Y. Yang, H. Sepulveda, W. Shi, I. Hwang, P.A. Peterson, M.R. Jackson, J. Sprent, and Z. Cai TCR-Mediated internalization of peptide-MHC complexes acquired by T cells Science 286 1999 952 954
15. J. Huang, V.I. Zarnitsyna, B. Liu, L.J. Edwards, N. Jiang, B.D. Evavold, and C. Zhu The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness Nature 464 2010 932 936
16. J.B. Huppa, M. Axmann, M.A. Mörtelmaier, B.F. Lillemeier, E.W. Newell, M. Brameshuber, L.O. Klein, G.J. Schütz, and M.M. Davis TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity Nature 463 2010 963 967
17. M. Huse, L.O. Klein, A.T. Girvin, J.M. Faraj, Q.-J. Li, M.S. Kuhns, and M.M. Davis Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist Immunity 27 2007 76 88
18. T. Ilani, G. Vasiliver-Shamis, S. Vardhana, A. Bretscher, and M.L. Dustin T cell antigen receptor signaling and immunological synapse stability require myosin IIA Nat. Immunol. 10 2009 531 539
19. J.R. James, and R.D. Vale Biophysical mechanism of T-cell receptor triggering in a reconstituted system Nature 487 2012 64 69
20. A. Jansson Kinetic proofreading and the search for nonself-peptides Self Nonself 2 2011 1 3
21. N. Jiang, J. Huang, L.J. Edwards, B. Liu, Y. Zhang, C.D. Beal, B.D. Evavold, and C. Zhu Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination Immunity 34 2011 13 23
22. G.J. Kersh, E.N. Kersh, D.H. Fremont, and P.M. Allen High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling Immunity 9 1998 817 826
23. N.E. Kilgore, J.D. Carter, U. Lorenz, and B.D. Evavold Cutting edge: dependence of TCR antagonism on Src homology 2 domain-containing protein tyrosine phosphatase activity J. Immunol. 170 2003 4891 4895
24. S.T. Kim, K. Takeuchi, Z.-Y.J. Sun, M. Touma, C.E. Castro, A. Fahmy, M.J. Lang, G. Wagner, and E.L. Reinherz The alphabeta T cell receptor is an anisotropic mechanosensor J. Biol. Chem. 284 2009 31028 31037
25. M. Krogsgaard, N. Prado, E.J. Adams, X.L. He, D.-C. Chow, D.B. Wilson, K.C. Garcia, and M.M. Davis Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation Mol. Cell 12 2003 1367 1378
26. Y.-C. Li, B.-M. Chen, P.-C. Wu, T.-L. Cheng, L.-S. Kao, M.-H. Tao, A. Lieber, and S.R. Roffler Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling J. Immunol. 184 2010 5959 5963
27. B. Liu, S. Zhong, K. Malecek, L.A. Johnson, S.A. Rosenberg, C. Zhu, and M. Krogsgaard 2D TCR-pMHC-CD8 kinetics determines T-cell responses in a self-antigen-specific TCR system Eur. J. Immunol. 44 2014 239 250
28. Z. Ma, P.A. Janmey, and T.H. Finkel The receptor deformation model of TCR triggering FASEB J. 22 2008 1002 1008
29. S. Majstoravich, J. Zhang, S. Nicholson-Dykstra, S. Linder, W. Friedrich, K.A. Siminovitch, and H.N. Higgs Lymphocyte microvilli are dynamic, actin-dependent structures that do not require Wiskott-Aldrich syndrome protein (WASp) for their morphology Blood 104 2004 1396 1403
30. B.T. Marshall, M. Long, J.W. Piper, T. Yago, R.P. McEver, and C. Zhu Direct observation of catch bonds involving cell-adhesion molecules Nature 423 2003 190 193
31. T.W. McKeithan Kinetic proofreading in T-cell receptor signal transduction Proc. Natl. Acad. Sci. USA 92 1995 5042 5046
32. R.H. McMahan, J.A. McWilliams, K.R. Jordan, S.W. Dow, D.B. Wilson, and J.E. Slansky Relating TCR-peptide-MHC affinity to immunogenicity for the design of tumor vaccines J. Clin. Invest. 116 2006 2543 2551
33. T.R. Mempel, S.E. Henrickson, and U.H. Von Andrian T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases Nature 427 2004 154 159
34. K.D. Mossman, G. Campi, J.T. Groves, and M.L. Dustin Altered TCR signaling from geometrically repatterned immunological synapses Science 310 2005 1191 1193
35. H. Mukhopadhyay, S.P. Cordoba, P.K. Maini, P.A. van der Merwe, and O. Dushek Systems model of T cell receptor proximal signaling reveals emergent ultrasensitivity PLoS Comput. Biol. 9 2013 e1003004
36. P.-H. Puech, D. Nevoltris, P. Robert, L. Limozin, C. Boyer, and P. Bongrand Force measurements of TCR/pMHC recognition at T cell surface PLoS ONE 6 2011 e22344
37. M.A. Purbhoo, D.J. Irvine, J.B. Huppa, and M.M. Davis T cell killing does not require the formation of a stable mature immunological synapse Nat. Immunol. 5 2004 524 530
38. M.G. Rudolph, R.L. Stanfield, and I.A. Wilson How TCRs bind MHCs, peptides, and coreceptors Annu. Rev. Immunol. 24 2006 419 466
39. J.J. Sabatino Jr., J. Huang, C. Zhu, and B.D. Evavold High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses J. Exp. Med. 208 2011 81 90
40. T.N. Sims, T.J. Soos, H.S. Xenias, B. Dubin-Thaler, J.M. Hofman, J.C. Waite, T.O. Cameron, V.K. Thomas, R. Varma, and C.H. Wiggins et al. Opposing effects of PKCtheta and WASp on symmetry breaking and relocation of the immunological synapse Cell 129 2007 773 785
41. J. Sloan-Lancaster, A.S. Shaw, J.B. Rothbard, and P.M. Allen Partial T cell signaling: altered phospho-zeta and lack of zap70 recruitment in APL-induced T cell anergy Cell 79 1994 913 922
42. J.E. Smith-Garvin, G.A. Koretzky, and M.S. Jordan T cell activation Annu. Rev. Immunol. 27 2009 591 619
43. Z.J. Sun, K.S. Kim, G. Wagner, and E.L. Reinherz 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
44. P.A. van der Merwe, and O. Dushek Mechanisms for T cell receptor triggering Nat. Rev. Immunol. 11 2011 47 55
45. J.H. Wang, and E.L. Reinherz The structural basis of αβ T-lineage immune recognition: TCR docking topologies, mechanotransduction, and co-receptor function Immunol. Rev. 250 2012 102 119
46. C. Xu, E. Gagnon, M.E. Call, J.R. Schnell, C.D. Schwieters, C.V. Carman, J.J. Chou, and K.W. Wucherpfennig Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif Cell 135 2008 702 713
47. D.K. Yao, and J.Y. Shao Flexibility of single microvilli on live neutrophils and lymphocytes Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76 2007 021907
48. V.I. Zarnitsyna, J. Huang, F. Zhang, Y.-H. Chien, D. Leckband, and C. Zhu Memory in receptor-ligand-mediated cell adhesion Proc. Natl. Acad. Sci. USA 104 2007 18037 18042
49. H. Zhang, S.P. Cordoba, O. Dushek, and P.A. van der Merwe Basic residues in the T-cell receptor ζ cytoplasmic domain mediate membrane association and modulate signaling Proc. Natl. Acad. Sci. USA 108 2011 19323 19328
50. C. Zhu, N. Jiang, J. Huang, V.I. Zarnitsyna, and B.D. Evavold Insights from in situ analysis of TCR-pMHC recognition: response of an interaction network Immunol. Rev. 251 2013 49 64
51. W. Chen, J. Lou, and C. Zhu Forcing switch from short- to intermediate- and long-lived states of the alphaA domain generates LFA-1/ICAM-1 catch bonds J. Biol. Chem. 285 2010 35967 35978
52. M. Degano, K.C. Garcia, V. Apostolopoulos, M.G. Rudolph, L. Teyton, and I.A. Wilson A functional hot spot for antigen recognition in a superagonist TCR/MHC complex Immunity 12 2000 251 261
53. J. Gelles, B.J. Schnapp, and M.P. Sheetz Tracking kinesin-driven movements with nanometre-scale precision Nature 331 1988 450 453
54. N. Otsu A threshold selection method from gray-level histograms IEEE Trans. Syst. Man Cybernetics 9 1979 62 66
55. C. Zhu, M. Long, S.E. Chesla, and P. Bongrand Measuring receptor/ligand interaction at the single-bond level: experimental and interpretative issues Ann. Biomed. Eng. 30 2002 305 314