2D TCR-pMHC-CD8 kinetics determines T-cell responses in a self-antigen-specific TCR system

European Journal of Immunology

Volumn 44, Issue 1, 2014, Pages 239-250

  Liu, Baoyu ^a   Zhong, Shi ^c   Malecek, Karolina ^c   Johnson, Laura A ^d,e   Rosenberg, Steven A ^d   Zhu, Cheng ^a,b   Krogsgaard, Michelle ^c  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

2D kinetics; Micropipette adhesion frequency assay; T cell activation; Thermal fluctuation assay

Indexed keywords

CD8 ANTIGEN; INTERLEUKIN 2; MELANOMA ANTIGEN; PEPTIDE; T LYMPHOCYTE RECEPTOR; HLA A2 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MELANOCYTE PROTEIN PMEL 17; PMEL PROTEIN, HUMAN; PROTEIN BINDING;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; PEPTIDE MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; CELL CULTURE; CELL JUNCTION; CHEMISTRY; IMMUNOLOGY; KINETICS; LYMPHOCYTE ACTIVATION; METABOLISM; NEOPLASMS;

ANTIGENS, CD8; CELLS, CULTURED; GP100 MELANOMA ANTIGEN; HLA-A2 ANTIGEN; HUMANS; INTERCELLULAR JUNCTIONS; KINETICS; LYMPHOCYTE ACTIVATION; NEOPLASMS; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84892469907     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343774     Document Type: Article

References (54)

1. Smith-Garvin, J. E., Koretzky, G. A. and Jordan, M. S., T cell activation. Annu. Rev. Immunol. 2009. 27: 591-619.
2. Krogsgaard, M. and Davis, M. M., How T cells 'see' antigen. Nat. Immunol. 2005. 6: 239-245.
3. Holler, P. D. and Kranz, D. M., Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 2003. 18: 255-264.
4. Stone, J. D., Chervin, A. S. and Kranz, D. M., T-cell receptor binding affinities and kinetics: impact on T-cell activity and specificity. Immunology 2009. 126: 165-176.
5. 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.
6. Alam, S. M., Travers, P. J., Wung, J. L., Nasholds, W., Redpath, S., Jameson, S. C. and Gascoigne, N. R., T-cell-receptor affinity and thymocyte positive selection. Nature 1996. 381: 616-620.
7. Lyons, D. S., Lieberman, S. A., Hampl, J., Boniface, J. J., Chien, Y., Berg, L. J. and Davis, M. M., A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity 1996. 5: 53-61.
8. Laugel, B., van den Berg, H. A., Gostick, E., Cole, D. K., Wooldridge, L., Boulter, J., Milicic, A. et al., Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J. Biol. Chem. 2007. 282: 23799-23810.
9. Minguet, S., Swamy, M., Alarcon, B., Luescher, I. F. and Schamel, W. W., Full activation of the T cell receptor requires both clustering and conformational changes at CD3. Immunity 2007. 26: 43-54.
10. Boniface, J. J., Rabinowitz, J. D., Wulfing, C., Hampl, J., Reich, Z., Altman, J. D., Kantor, R. M. et al., Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands [corrected]. Immunity 1998. 9: 459-466.
11. Krogsgaard, M., Li, Q. J., Sumen, C., Huppa, J. B., Huse, M. and Davis, M. M., Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 2005. 434: 238-243.
12. 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.
13. Rabinowitz, J. D., Beeson, C., Lyons, D. S., Davis, M. M. and McConnell, H. M., Kinetic discrimination in T-cell activation. Proc. Natl. Acad. Sci. USA 1996. 93: 1401-1405.
14. van der Merwe, P. A., The TCR triggering puzzle. Immunity 2001. 14: 665-668.
15. Rudolph, M. G. and Wilson, I. A., The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 2002. 14: 52-65.
16. Rosette, C., Werlen, G., Daniels, M. A., Holman, P. O., Alam, S. M., Travers, P. J., Gascoigne, N. R. 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.
17. Tian, S., Maile, R., Collins, E. J. and Frelinger, J. A., CD8+ T cell activation is governed by TCR-peptide/MHC affinity, not dissociation rate. J. Immunol. 2007. 179: 2952-2960.
18. Zehn, D., Lee, S. Y. and Bevan, M. J., Complete but curtailed T-cell response to very low-affinity antigen. Nature 2009. 458: 211-214.
19. Schmid, D. A., Irving, M. B., Posevitz, V., Hebeisen, M., Posevitz-Fejfar, A., Sarria, J. C., Gomez-Eerland, R. et al., Evidence for a TCR affinity threshold delimiting maximal CD8 T cell function. J. Immunol. 2010. 184: 4936-4946.
20. McMahan, R. H., McWilliams, J. A., Jordan, K. R., Dow, S. W., Wilson, D. B. and Slansky, J. E., Relating TCR-peptide-MHC affinity to immunogenicity for the design of tumor vaccines. J. Clin. Invest. 2006. 116: 2543-2551.
21. Irving, M., Zoete, V., Hebeisen, M., Schmid, D., Baumgartner, P., Guillaume, P., Romero, P. et al., Interplay between T cell receptor binding kinetics and the level of cognate peptide presented by major histocompatibility complexes governs CD8+ T cell responsiveness. J. Biol. Chem. 2012. 287: 23068-23078.
22. Corse, E., Gottschalk, R. A., Krogsgaard, M. and Allison, J. P., Attenuated T cell responses to a high-potency ligand in vivo. PLoS Biol. 2010. 9: e1000481.
23. Dushek, O., Aleksic, M., Wheeler, R. J., Zhang, H., Cordoba, S. P., Peng, Y. C., Chen, J. L. et al., Antigen potency and maximal efficacy reveal a mechanism of efficient T cell activation. Sci. Signal. 2011. 4: ra39.
24. Savage, P. A., Boniface, J. J. and Davis, M. M., A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 1999. 10: 485-492.
25. Wang, X. L. and Altman, J. D., Caveats in the design of MHC class I tetramer/antigen-specific T lymphocytes dissociation assays. J. Immunol. Methods 2003. 280: 25-35.
26. Sabatino, J. J., Jr., Huang, J., Zhu, C. and Evavold, B. D., High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses. J. Exp. Med. 2011. 208: 81-90.
27. 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.
28. 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.
29. Edwards, L. J., Zarnitsyna, V. I., Hood, J. D., Evavold, B. D. and Zhu, C., Insights into T cell recognition of antigen: significance of two-dimensional kinetic parameters. Front. Immunol. 2012. 3: 86.
30. 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.
31. Huang, J., Meyer, C. and Zhu, C., T cell antigen recognition at the cell membrane. Mol. Immunol. 2012. 52: 155-164.
32. Zarnitsyna, V. and Zhu, C., T cell triggering: insights from 2D kinetics analysis of molecular interactions. Phys. Biol. 2012. 9: 045005.
33. 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.
34. 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.
35. Parkhurst, M. R., Salgaller, M. L., Southwood, S., Robbins, P. F., Sette, A., Rosenberg, S. A. and Kawakami, Y., Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J. Immunol. 1996. 157: 2539-2548.
36. Zhong, S., Malecek, K., Johnson, L. A., Yu, Z., Vega-Saenz de Miera, E., 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. USA 2013. 110: 6973-6978.
37. Chesla, S. E., Selvaraj, P. and Zhu, C., Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 1998. 75: 1553-1572.
38. 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.
39. 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.
40. Huang, J., Edwards, L. J., Evavold, B. D. and Zhu, C., Kinetics of MHC-CD8 interaction at the T cell membrane. J. Immunol. 2007. 179: 7653-7662.
41. Govern, C. C., Paczosa, M. K., Chakraborty, A. K. and Huseby, E. S., Fast on-rates allow short dwell time ligands to activate T cells. Proc. Natl. Acad. Sci. USA 2010. 107: 8724-8729.
42. 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.
43. 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.
44. 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.
45. Wu, L., Xiao, B., Jia, X., Zhang, Y., Lu, 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. Artyomov, M. N., Lis, M., Devadas, S., Davis, M. M. and Chakraborty, A. K., CD4 and CD8 binding to MHC molecules primarily acts to enhance Lck delivery. Proc. Natl. Acad. Sci. USA 2010. 107: 16916-16921.
48. Li, Q. J., Dinner, A. R., Qi, S., Irvine, D. J., Huppa, J. B., Davis, M. M. and Chakraborty, A. K., CD4 enhances T cell sensitivity to antigen by coordinating Lck accumulation at the immunological synapse. Nat. Immunol. 2004. 5: 791-799.
49. Garcia, K. C., Scott, C. A., Brunmark, A., Carbone, F. R., Peterson, P. A., Wilson, I. A. and Teyton, L., CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 1996. 384: 577-581.
50. Wyer, J. R., Willcox, B. E., Gao, G. F., Gerth, U. C., Davis, S. J., Bell, J. I., van der Merwe, P. A. et al., T cell receptor and coreceptor CD8±± bind peptide-MHC independently and with distinct kinetics. Immunity 1999. 10: 219-225.
51. Wooldridge, L., van den Berg, H. A., Glick, M., Gostick, E., Laugel, B., Hutchinson, S. L., Milicic, A. et al., Interaction between the CD8 coreceptor and major histocompatibility complex class I stabilizes T cell receptor-antigen complexes at the cell surface. J. Biol. Chem. 2005. 280: 27491-27501.
52. Engels, B., Chervin, A. S., Sant, A. J., Kranz, D. M. and Schreiber, H., Long-term persistence of CD4+ but rapid disappearance of CD8+ T cells expressing an MHC class I-restricted TCR of nanomolar affinity. Mol. Ther. 2012. 20: 652-660.
53. Merhavi-Shoham, E., Haga-Friedman, A. and Cohen, C. J., Genetically modulating T-cell function to target cancer. Sem. Cancer Biol. 2012. 22: 14-22.
54. Malecek, K., Zhong, S., McGary, K., Yu, C., Huang, K., Johnson, L. A., Rosenberg, S. A. et al., Engineering improved T cell receptors using an alanine-scan guided T cell display selection system. J. Immunol. Methods 2013. 392: 1-11.