The cellular environment regulates in situ kinetics of T-cell receptor interaction with peptide major histocompatibility complex

European Journal of Immunology

Volumn 45, Issue 7, 2015, Pages 2099-2110

  Liu, Baoyu ^a   Chen, Wei ^a,d   Natarajan, Kannan ^c   Li, Zhenhai ^a   Margulies, David H ^c   Zhu, Cheng ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

Adhesion; Cellular immunology; Molecular immunology; T cells; TCRs

Indexed keywords

MONOCLONAL ANTIBODY; PEPTIDE; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ARTICLE; BINDING AFFINITY; CELL KINETICS; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PRIORITY JOURNAL; ANTIGEN PRESENTING CELL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; FLOW CYTOMETRY; IMMUNOLOGY; KINETICS; LYMPHOCYTE ACTIVATION; PROCEDURES; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANTIGEN-PRESENTING CELLS; FLOW CYTOMETRY; HUMANS; KINETICS; LYMPHOCYTE ACTIVATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MODELS, IMMUNOLOGICAL; MODELS, MOLECULAR; PEPTIDES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84935713589     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445358     Document Type: Article

References (63)

1. Gascoigne, N. R., Zal, T. and Alam, S. M., T-cell receptor binding kinetics in T-cell development and activation. Expert Rev. Mol. Med. 2001. 2001: 1-17.
2. vander Merwe, P. A. and Dushek, O., Mechanisms for T cell receptor triggering. Nat. Rev. Immunol. 2011. 11: 47-55.
3. Aleksic, M., Dushek, O., Zhang, H., Shenderov, E., Chen, J.-L., Cerundolo, V., Coombs, D. et al., Dependence of T cell antigen recognition on T cell receptor-peptide MHC confinement time. Immunity 2010. 32: 163-174.
4. Huang, J., Zarnitsyna, V. I., Liu, B., Edwards, L. J., Jiang, N., Evavold, B. D. and Zhu, C., The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 2010. 464: 932-936.
5. Huppa, J. B., Axmann, M., Mortelmaier, M. A., Lillemeier, B. F., Newell, E. W., Brameshuber, M., Klein, L. O. et al., TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 2010. 463: 963-967.
6. Liu, B. Y., Zhong, S., Malecek, K., Johnson, L. A., Rosenberg, S. A., Zhu, C. and Krogsgaard, M., 2D TCR-pMHC-CD8 kinetics determines T-cell responses in a self-antigen-specific TCR system. Eur. J. Immunol. 2014. 44: 239-250.
7. Zhong, S., Malecek, K., Johnson, L. A., Yu, Z. Y., deMiera, E. V. S., Darvishian, F., McGary, K. et al., T-cell receptor affinity and avidity defines antitumor response and autoimmunity in T-cell immunotherapy. Proc. Natl. Acad. Sci. U S A 2013. 110: 6973-6978.
8. Krogsgaard, M., Prado, N., Adams, E. J., He, X.-L., Chow, D.-C., Wilson, D. B., Garcia, K. C. et al., Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol. Cell 2003. 12: 1367-1378.
9. Dushek, O., Das, R. and Coombs, D., A role for rebinding in rapid and reliable T cell responses to antigen. PloS Comput. Biol. 2009. 5: e1000578. DOI: 10.1371/journal.pcbi.1000578.
10. McKeithan, T. W., Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. U S A 1995. 92: 5042-5046.
11. Axmann, M., Huppa, J. B., Davis, M. M. and Schutz, G. J., Determination of interaction kinetics between the T cell receptor and peptide-loaded MHC Class II via single-molecule diffusion measurements. Biophys. J. 2012. 103: L17-L19.
12. O'Donoghue, G. P., Pielak, R. M., Smoligovets, A. A., Lin, J. J. and Groves, J. T., Direct single molecule measurement of TCR triggering by agonist pMHC in living primary T cells. Elife 2013. 2: e00778.
13. Adams, J. J., Narayanan, S., Liu, B., Birnbaum, M. E., Kruse, A. C., Bowerman, N. A., Chen, W. et al., T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 2011. 35: 681-693.
14. Sabatino, J., Huang, J., Zhu, C. and Evavold, B., High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses. J. Exp. Med. 2011. 208: 81-90.
15. Jiang, N., Huang, J., Edwards, L. J., Liu, B., Zhang, Y., Beal, C. D., Evavold, B. D. et al., Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination. Immunity 2011. 34: 13-23.
16. Dustin, M. L., Bromley, S. K., Davis, M. M. and Zhu, C., Identification of self through two-dimensional chemistry and synapses. Annu. Rev. Cell Dev. Biol. 2001. 17: 133-157.
17. Wu, Y. H., Vendome, J., Shapiro, L., Ben-Shaul, A. and Honig, B., Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 2011. 475: 510-513.
18. Bell, G. I., Models for the specific adhesion of cells to cells. Science 1978. 200: 618-627.
19. Zarnitsyna, V. and Zhu, C., T cell triggering: insights from 2D kinetics analysis of molecular interactions. Phys. Biol. 2012. 9: 045005. DOI: 10.1088/1478-3975/9/4/045005.
20. Zhu, C., Jiang, N., Huang, J., Zarnitsyna, V. I. and Evavold, B. D., Insights from in situ analysis of TCR-pMHC recognition: response of an interaction network. Immunol. Rev. 2013. 251: 49-64.
21. Chesla, S. E., Selvaraj, P. and Zhu, C., Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 1998. 75: 1553-1572.
22. Chen, W., Evans, E. A., McEver, R. P. and Zhu, C., Monitoring receptor-ligand interactions between surfaces by thermal fluctuations. Biophys. J. 2008. 94: 694-701.
23. Alam, S. M., Davies, G. M., Lin, C. M., Zal, T., Nasholds, W., Jameson, S. C., Hogquist, K. A. et al., Qualitative and quantitative differences in T cell receptor binding of agonist and antagonist ligands. Immunity 1999. 10: 227-237.
24. Allard, J. F., Dushek, O., Coombs, D. and vander Merwe, P. A., Mechanical modulation of receptor-ligand interactions at cell-cell interfaces. Biophys. J. 2012. 102: 1265-1273.
25. Klotzsch, E. and Schutz, G. J., Improved ligand discrimination by force-induced unbinding of the T cell receptor from peptide-MHC. Biophys. J. 2013. 104: 1670-1675.
26. Liu, B., Chen, W., Evavold, B. D. and Zhu, C., Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 2014. 157: 357-368.
27. Robert, P., Aleksic, M., Dushek, O., Cerundolo, V., Bongrand, P. and vander Merwe, P. A., Kinetics and mechanics of two-dimensional interactions between T cell receptors and different activating ligands. Biophys. J. 2012. 102: 248-257.
28. Das, D. K., Feng, Y., Mallis, R. J., Li, X., Keskin, D. B., Hussey, R. E., Brady, S. K. et al., Force-dependent transition in the T-cell receptor beta-subunit allosterically regulates peptide discrimination and pMHC bond lifetime. Proc. Natl. Acad. Sci. U S A 2015. 112: 1517-1522.
29. Alam, S. M., Travers, P. J., Wung, J. L., Nasholds, W., Redpath, S., Jameson, S. C. and Gascoigne, N. R. J., T-cell-receptor affinity and thymocyte positive selection. Nature 1996. 381: 616-620.
30. Rosette, C., Werlen, G., Daniels, M. A., Holman, P. O., Alam, S. M., Travers, P. J., Gascoigne, N. R. J. et al., The impact of duration versus extent of TCR occupancy on T cell activation: a revision of the kinetic proofreading model. Immunity 2001. 15: 59-70.
31. Li, P., Jiang, N., Nagarajan, S., Wohlhueter, R., Selvaraj, P. and Zhu, C., Affinity and kinetic analysis of Fcγ receptor IIIa (CD16a) binding to IgG ligands. J. Biol. Chem. 2007. 282: 6210-6221.
32. Molnar, E., Deswal, S. and Schamel, W. W., Pre-clustered TCR complexes. FEBS Lett. 2010. 584: 4832-4837.
33. Bosch, B., Heipertz, E. L., Drake, J. R. and Roche, P. A., Major histocompatibility complex (MHC) class II-peptide complexes arrive at the plasma membrane in cholesterol-rich microclusters. J. Biol. Chem. 2013. 288: 13236-13242.
34. Fooksman, D. R., Gronvall, G. K., Tang, Q. and Edidin, M., Clustering class I MHC modulates sensitivity of T cell recognition. J. Immunol. 2006. 176: 6673-6680.
35. Howarth, M., Chinnapen, D. J., Gerrow, K., Dorrestein, P. C., Grandy, M. R., Kelleher, N. L., El-Husseini, A. et al., A monovalent streptavidin with a single femtomolar biotin binding site. Nat. Methods 2006. 3: 267-273.
36. Marshall, B. T., Long, M., Piper, J. W., Yago, T., McEver, R. P. and Zhu, C., Direct observation of catch bonds involving cell-adhesion molecules. Nature 2003. 423: 190-193.
37. Ramachandran, V., Yago, T., Epperson, T. K., Kobzdej, M. M., Nollert, M. U., Cummings, R. D., Zhu, C. et al., Dimerization of a selectin and its ligand stabilizes cell rolling and enhances tether strength in shear flow. Proc. Natl. Acad. Sci. U S A 2001. 98: 10166-10171.
38. Williams, T. E., Nagarajan, S., Selvaraj, P. and Zhu, C., Quantifying the impact of membrane microtopology on effective two-dimensional affinity. J. Biol. Chem. 2001. 276: 13283-13288.
39. Wu, L., Xiao, B. T., Jia, X. L., Zhang, Y., Lu, S. Q., Chen, J. and Long, M., Impact of carrier stiffness and microtopology on two-dimensional kinetics of P-selectin and P-selectin glycoprotein ligand-1 (PSGL-1) interactions. J. Biol. Chem. 2007. 282: 9846-9854.
40. Chen, W., Zarnitsyna, V. I., Sarangapani, K. K., Huang, J. and Zhu, C., Measuring receptor-ligand binding kinetics on cell surfaces: from adhesion frequency to thermal fluctuation methods. Cell Mol. Bioeng. 2008. 1: 276-288.
41. Pierres, A., Touchard, D., Benoliel, A. M. and Bongrand, P., Dissecting streptavidin-biotin interaction with a laminar flow chamber. Biophys. J. 2002. 82: 3214-3223.
42. Stepanek, O., Prabhakar, A. S., Osswald, C., King, C. G., Bulek, A., Naeher, D., Beaufils-Hugot, M. et al., Coreceptor scanning by the T cell receptor provides a mechanism for T cell tolerance. Cell 2014. 159: 333-345.
43. Chervin, A. S., Stone, J. D., Holler, P. D., Bai, A., Chen, J., Eisen, H. N. and Kranz, D. M., The impact of TCR-binding properties and antigen presentation format on T cell responsiveness. J. Immunol. 2009. 183: 1166-1178.
44. Degano, M., Garcia, K. C., Apostolopoulos, V., Rudolph, M. G., Teyton, L. and Wilson, I. A., A functional hot spot for antigen recognition in a superagonist TCR/MHC complex. Immunity 2000. 12: 251-261.
45. Wu, L., Xiao, B., Jia, X., Zhang, Y., Lü, S., Chen, J. and Long, M., Impact of carrier stiffness and microtopology on two-dimensional kinetics of P-selectin and P-selectin glycoprotein ligand-1 (PSGL-1) interactions. J. Biol. Chem. 2007. 282: 9846-9854.
46. Huang, J., Chen, J., Chesla, S. E., Yago, T., Mehta, P., McEver, R. P., Zhu, C. et al., Quantifying the effects of molecular orientation and length on two-dimensional receptor-ligand binding kinetics. J. Biol. Chem. 2004. 279: 44915-44923.
47. Kumar, R., Ferez, M., Swamy, M., Arechaga, I., Rejas, M. T., Valpuesta, J. M., Schamel, W. W. A. et al., Increased sensitivity of antigen-experienced T cells through the enrichment of oligomeric T cell receptor complexes. Immunity 2011. 35: 375-387.
48. Crites, T. J., Padhan, K., Muller, J., Krogsgaard, M., Gudla, P. R., Lockett, S. J. and Varma, R., TCR microclusters pre-exist and contain molecules necessary for TCR signal transduction. J. Immunol. 2014. 193: 56-67.
49. Lillemeier, B. F., Mortelmaier, M. A., Forstner, M. B., Huppa, J. B., Groves, J. T. and Davis, M. M., TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat. Immunol. 2010. 11: 90-96.
50. Rozdzial, M. M., Malissen, B. and Finkel, T. H., Tyrosine-phosphorylated T cell receptor zeta chain associates with the actin cytoskeleton upon activation of mature T lymphocytes. Immunity 1995. 3: 623-633.
51. Rozdzial, M. M., Pleiman, C. M., Cambier, J. C. and Finkel, T. H., pp56Lck mediates TCR zeta-chain binding to the microfilament cytoskeleton. J. Immunol. 1998. 161: 5491-5499.
52. Kabouridis, P. S., Lipid rafts in T cell receptor signalling. Mol. Membr. Biol. 2006. 23: 49-57.
53. Kim, S. T., Takeuchi, K., Sun, Z.-Y. J., Touma, M., Castro, C. E., Fahmy, A., Lang, M. J. et al., The alphabeta T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 2009. 284: 31028-31037.
54. Daniels, M. A., Levine, L., Miller, J. D., Moser, J. M., Lukacher, A. E., Altman, J. D., Kavathas, P. et al., CD8 binding to MHC class I molecules is influenced by maturation and T cell glycosylation. Immunity 2001. 15: 1051-1061.
55. Kuball, J., Hauptrock, B., Malina, V., Antunes, E., Voss, R. H., Wolfl, M., Strong, R. et al., Increasing functional avidity of TCR-redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J. Exp. Med. 2009. 206: 463-475.
56. Moody, A. M., Chui, D., Reche, P. A., Priatel, J. J., Marth, J. D. and Reinherz, E. L., Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell 2001. 107: 501-512.
57. Chen, W., Lou, J. and Zhu, C., Forcing switch from short- to intermediate- and long-lived states of the alphaA domain generates LFA-1/ICAM-1 catch bonds. J. Biol. Chem. 2010. 285: 35967-35978.
58. Kuhns, M. S. and Davis, M. M., Disruption of extracellular interactions impairs T cell receptor-CD3 complex stability and signaling. Immunity 2007. 26: 357-369.
59. Ortiz-Navarrete, V. and Hammerling, G. J., Surface appearance and instability of empty H-2 class I molecules under physiological conditions. Proc. Natl. Acad. Sci. U S A 1991. 88: 3594-3597.
60. Hansen, T. and Myers, N., Peptide induction of surface expression of class I MHC. Curr. Protoc. Immunol. 2003. Chapter 18: Unit 18. 11.
61. Boulter, J. M., Glick, M., Todorov, P. T., Baston, E., Sami, M., Rizkallah, P. and Jakobsen, B. K., Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng. 2003. 16: 707-711.
62. Li, H. M., Natarajan, K., Malchiodi, E. L., Margulies, D. H. and Mariuzza, R. A., Three-dimensional structure of H-2D(d) complexed with an immunodominant peptide from human immunodeficiency virus envelope glycoprotein 120. J. Mol. Biol. 1998. 283: 179-191.
63. Klopocki, A. G., Yago, T., Mehta, P., Yang, J., Wu, T., Leppanen, A., Bovin, N. V. et al., Replacing a lectin domain residue in L-selectin enhances binding to P-selectin glycoprotein ligand-1 but not to 6-sulfo-sialyl Lewis x. J. Biol. Chem. 2008. 283: 11493-11500.