T-cell Receptor (TCR)-peptide specificity overrides affinity-enhancing TCR-major histocompatibility complex interactions

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 628-638

  Cole, David K ^a   Miles, Kim M ^a   Madura, Florian ^a   Holland, Christopher J ^a   Schauenburg, Andrea J A ^a   Godkin, Andrew J ^a   Bulek, Anna M ^a   Fuller, Anna ^a   Akpovwa, Hephzibah J E ^a   Pymm, Phillip G ^a,b   Liddy, Nathaniel ^c   Sami, Malkit ^c   Li, Yi ^c   Rizkallah, Pierre J ^a   Jakobsen, Bent K ^c   Sewell, Andrew K ^a  

^a CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c Immunocore Limited   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; HISTOCOMPATIBILITY COMPLEXES; T-CELL RECEPTORS;

BINDING ENERGY; CELL MEMBRANES; PEPTIDES;

T-CELLS;

T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ARTICLE; BINDING AFFINITY; CELL SPECIFICITY; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION;

IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX (MHC); PROTEIN-PROTEIN INTERACTIONS; RECEPTOR STRUCTURE-FUNCTION; T-CELL BIOLOGY; T-CELL RECEPTOR;

AMINO ACID SEQUENCE; BINDING, COMPETITIVE; COMPLEMENTARITY DETERMINING REGIONS; CRYSTALLOGRAPHY, X-RAY; HLA ANTIGENS; HLA-A2 ANTIGEN; HUMANS; KINETICS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOPEPTIDES; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL; T-CELL ANTIGEN RECEPTOR SPECIFICITY;

EID: 84891939529     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.522110     Document Type: Article

References (64)

1. Davis, M. M., and Bjorkman, P. J. (1988) T-cell antigen receptor genes and T-cell recognition. Nature 334, 395-402
2. Garcia, K. C., Degano, M., Speir, J. A., and Wilson, I. A. (1999) Emerging principles for T cell receptor recognition of antigen in cellular immunity. Rev. Immunogenet. 1, 75-90
3. Mason, D. (1998) A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today 19, 395-404
4. Sewell, A. K. (2012) Why must T cells be cross-reactive? Nat. Rev. Immunol. 12, 669-677
5. Rudolph, M. G., Stanfield, R. L., and Wilson, I. A. (2006) How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24, 419-466
6. Gras, S., Burrows, S. R., Turner, S. J., Sewell, A. K., McCluskey, J., and Rossjohn, J. (2012) A structural voyage toward an understanding of the MHC-I-restricted immune response: lessons learned and much to be learned. Immunol. Rev. 250, 61-81
7. Dai, S., Huseby, E. S., Rubtsova, K., Scott-Browne, J., Crawford, F., Macdonald, W. A., Marrack, P., and Kappler, J. W. (2008) Crossreactive T cells spotlight the germ line rules for-Tcell-receptor interactions withMHC molecules. Immunity 28, 324-334
8. Feng, D., Bond, C. J., Ely, L. K., Maynard, J., and Garcia, K. C. (2007) Structural evidence for a germ line-encoded T cell receptor-major histocompatibility complex interaction "codon." Nat. Immunol. 8, 975-983
9. Garcia, K. C., Adams, J. J., Feng, D., and Ely, L. K. (2009) The molecular basis of TCR germ line bias forMHCis surprisingly simple. Nat. Immunol. 10, 143-147
10. Scott-Browne, J. P., White, J., Kappler, J. W., Gapin, L., and Marrack, P. (2009) Germ line-encoded amino acids in the-T-cell receptor control thymic selection. Nature 458, 1043-1046
11. Wu, L. C., Tuot, D. S., Lyons, D. S., Garcia, K. C., and Davis, M. M. (2002) Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 418, 552-556
12. Housset, D., and Malissen, B. (2003) What do TCR-pMHC crystal structures teach us aboutMHCrestriction and alloreactivity? Trends Immunol. 24, 429-437
13. Wooldridge, L., Ekeruche-Makinde, J., van den Berg, H. A., Skowera, A., Miles, J. J., Tan, M. P., Dolton, G., Clement, M., Llewellyn-Lacey, S., Price, D. A., Peakman, M., and Sewell, A. K. (2012) A single autoimmune T cell receptor recognizes more than a million different peptides. J. Biol. Chem. 287, 1168-1177
14. Colf, L. A., Bankovich, A. J., Hanick, N. A., Bowerman, N. A., Jones, L. L., Kranz, D. M., and Garcia, K. C. (2007) How a single T cell receptor recognizes both self and foreign MHC. Cell 129, 135-146
15. Borg, N. A., Ely, L. K., Beddoe, T., Macdonald, W. A., Reid, H. H., Clements, C. S., Purcell, A. W., Kjer-Nielsen, L., Miles, J. J., Burrows, S. R., McCluskey, J., and Rossjohn, J. (2005) The CDR3 regions of an immunodominant T cell receptor dictate the "energetic landscape" of peptide-MHC recognition. Nat. Immunol. 6, 171-180
16. Burrows, S. R., Chen, Z., Archbold, J. K., Tynan, F. E., Beddoe, T., Kjer-Nielsen, L., Miles, J. J., Khanna, R., Moss, D. J., Liu, Y. C., Gras, S., Kostenko, L., Brennan, R. M., Clements, C. S., Brooks, A. G., Purcell, A. W., McCluskey, J., and Rossjohn, J. (2010) Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Proc. Natl. Acad. Sci. U.S.A. 107, 10608-10613
17. Gras, S., Chen, Z., Miles, J. J., Liu, Y. C., Bell, M. J., Sullivan, L. C., Kjer-Nielsen, L., Brennan, R. M., Burrows, J. M., Neller, M. A., Khanna, R., Purcell, A. W., Brooks, A. G., McCluskey, J., Rossjohn, J., and Burrows, S. R. (2010) Allelic polymorphism in the T cell receptor and its impact on immune responses. J. Exp. Med. 207, 1555-1567
18. Sethi, D. K., Schubert, D. A., Anders, A. K., Heroux, A., Bonsor, D. A., Thomas, C. P., Sundberg, E. J., Pyrdol, J., and Wucherpfennig, K. W. (2011) A highly tilted binding mode by a self-reactive T cell receptor results in altered engagement of peptide and MHC. J. Exp. Med. 208, 91-102
19. Tynan, F. E., Burrows, S. R., Buckle, A. M., Clements, C. S., Borg, N. A., Miles, J. J., Beddoe, T., Whisstock, J. C., Wilce, M. C., Silins, S. L., Burrows, J. M., Kjer-Nielsen, L., Kostenko, L., Purcell, A. W., McCluskey, J., and Rossjohn, J. (2005) T cell receptor recognition of a "super- bulged" major histocompatibility complex class I-bound peptide. Nat. Immunol. 6, 1114-1122
20. Tynan, F. E., Reid, H. H., Kjer-Nielsen, L., Miles, J. J., Wilce, M. C., Kostenko, L., Borg, N. A., Williamson, N. A., Beddoe, T., Purcell, A. W., Burrows, S. R., McCluskey, J., and Rossjohn, J. (2007) A T cell receptor flattens a bulged antigenic peptide presented by a major histocompatibility complex class I molecule. Nat. Immunol. 8, 268-276
21. Yin, Y., Li, Y., Kerzic, M. C., Martin, R., and Mariuzza, R. A. (2011) Structure of a TCR with high affinity for self-antigen reveals basis for escape from negative selection. EMBO J. 30, 1137-1148
22. Bridgeman, J. S., Sewell, A. K., Miles, J. J., Price, D. A., and Cole, D. K. (2012) Structural and biophysical determinants of-T-cell antigen recognition. Immunology 135, 9-18
23. Cole, D. K., Pumphrey, N. J., Boulter, J. M., Sami, M., Bell, J. I., Gostick, E., Price, D. A., Gao, G. F., Sewell, A. K., and Jakobsen, B. K. (2007) Human TCR-binding affinity is governed by MHC class restriction. J. Immunol. 178, 5727-5734
24. Cole, D. K., Yuan, F., Rizkallah, P. J., Miles, J. J., Gostick, E., Price, D. A., Gao, G. F., Jakobsen, B. K., and Sewell, A. K. (2009) Germ line-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J. Biol. Chem. 284, 27281-27289
25. Purbhoo, M. A., Li, Y., Sutton, D. H., Brewer, J. E., Gostick, E., Bossi, G., Laugel, B., Moysey, R., Baston, E., Liddy, N., Cameron, B., Bennett, A. D., Ashfield, R., Milicic, A., Price, D. A., Classon, B. J., Sewell, A. K., and Jakobsen, B. K. (2007) TheHLAA*0201-restricted hTERT(540-548) peptide is not detected on tumor cells by a CTL clone or a high-affinity T-cell receptor. Mol. Cancer Ther. 6, 2081-2091
26. Li, Y., Moysey, R., Molloy, P. E., Vuidepot, A. L., Mahon, T., Baston, E., Dunn, S., Liddy, N., Jacob, J., Jakobsen, B. K., and Boulter, J. M. (2005) Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat. Biotechnol. 23, 349-354
27. Garboczi, D. N., Ghosh, P., Utz, U., Fan, Q. R., Biddison, W. E., and Wiley, D. C. (1996) Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141
28. Boulter, J. M., Glick, M., Todorov, P. T., Baston, E., Sami, M., Rizkallah, P., and Jakobsen, B. K. (2003) Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng. 16, 707-711
29. Cole, D. K., Dunn, S. M., Sami, M., Boulter, J. M., Jakobsen, B. K., and Sewell, A. K. (2008) T cell receptor engagement of peptide-major histocompatibility complex class I does not modify CD8 binding. Mol. Immunol. 45, 2700-2709
30. Cole, D. K., Rizkallah, P. J., Gao, F., Watson, N. I., Boulter, J. M., Bell, J. I., Sami, M., Gao, G. F., and Jakobsen, B. K. (2006) Crystal structure of HLAA* 2402 complexed with a telomerase peptide. Eur. J. Immunol. 36, 170-179
31. Wyer, J. R., Willcox, B. E., Gao, G. F., Gerth, U. C., Davis, S. J., Bell, J. I., van der Merwe, P. A., and Jakobsen, B. K. (1999)Tcell receptor and coreceptor CD8-bind peptide-MHC independently and with distinct kinetics. Immunity 10, 219-225
32. Holland, C. J., Rizkallah, P. J., Vollers, S., Calvo-Calle, J. M., Madura, F., Fuller, A., Sewell, A. K., Stern, L. J., Godkin, A., and Cole, D. K. (2012) Minimal conformational plasticity enables TCR cross-reactivity to different MHC class II heterodimers. Sci. Rep. 2, 629
33. Miles, J. J., Bulek, A. M., Cole, D. K., Gostick, E., Schauenburg, A. J., Dolton, G., Venturi, V., Davenport, M. P., Tan, M. P., Burrows, S. R., Wooldridge, L., Price, D. A., Rizkallah, P. J., and Sewell, A. K. (2010) Genetic and structural basis for selection of a ubiquitousTcell receptor deployed in Epstein-Barr virus infection. PLoS Pathog. 6, e1001198
34. Madura, F., Rizkallah, P. J., Miles, K. M., Holland, C. J., Bulek, A. M., Fuller, A., Schauenburg, A. J., Miles, J. J., Liddy, N., Sami, M., Li, Y., Hossain, M., Baker, B. M., Jakobsen, B. K., Sewell, A. K., and Cole, D. K. (2013) T-cell receptor specificity maintained by altered thermodynamics. J. Biol. Chem. 288, 18766-18775
35. Karlsson, R., Katsamba, P. S., Nordin, H., Pol, E., and Myszka, D. G. (2006) Analyzing a kinetic titration series using affinity biosensors. Anal. Biochem. 349, 136-147
36. Winter, G. (2010) xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186-190
37. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
38. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
39. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
40. Delano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific LLC, San Carlos, CA
41. Cole, D. K., Sami, M., Scott, D. R., Rizkallah, P. J., Borbulevych, O. Y., Todorov, P. T., Moysey, R. K., Jakobsen, B. K., Boulter, J. M., Baker, B. M., and Yi, L. (2013) Increased peptide contacts govern high affinity binding of a modified TCR whilst maintaining a native pMHC docking mode. Front. Immunol. 4, 168
42. Dunn, S. M., Rizkallah, P. J., Baston, E., Mahon, T., Cameron, B., Moysey, R., Gao, F., Sami, M., Boulter, J., Li, Y., and Jakobsen, B. K. (2006) Directed evolution of human T cell receptor CDR2 residues by phage display dramatically enhances affinity for cognate peptide-MHC without increasing apparent cross-reactivity. Protein Sci. 15, 710-721
43. Sami, M., Rizkallah, P. J., Dunn, S., Molloy, P., Moysey, R., Vuidepot, A., Baston, E., Todorov, P., Li, Y., Gao, F., Boulter, J. M., and Jakobsen, B. K. (2007) Crystal structures of high affinity human T-cell receptors bound to peptide major histocompatibility complex reveal native diagonal binding geometry. Protein Eng. Des. Sel. 20, 397-403
44. Varela-Rohena, A., Molloy, P. E., Dunn, S. M., Li, Y., Suhoski, M. M., Carroll, R. G., Milicic, A., Mahon, T., Sutton, D. H., Laugel, B., Moysey, R., Cameron, B. J., Vuidepot, A., Purbhoo, M. A., Cole, D. K., Phillips, R. E., June, C. H., Jakobsen, B. K., Sewell, A. K., and Riley, J. L. (2008) Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat. Med. 14, 1390-1395
45. Tickle, I. J., Laskowski, R. A., and Moss, D. S. (2000) Rfree and the Rfree ratio. II. Calculation of the expected values and variances of cross-validation statistics in macromolecular least-squares refinement. Acta Crystallogr. D Biol. Crystallogr. 56, 442-450
46. Donermeyer, D. L., Weber, K. S., Kranz, D. M., and Allen, P. M. (2006) The study of high-affinity TCRs reveals duality in T cell recognition of antigen: specificity and degeneracy. J. Immunol. 177, 6911-6919
47. Laugel, B., Boulter, J. M., Lissin, N., Vuidepot, A., Li, Y., Gostick, E., Crotty, L. E., Douek, D. C., Hemelaar, J., Price, D. A., Jakobsen, B. K., and Sewell, A. K. (2005) Design of soluble recombinant T cell receptors for antigen targeting and T cell inhibition. J. Biol. Chem. 280, 1882-1892
48. Persaud, S. P., Donermeyer, D. L., Weber, K. S., Kranz, D. M., and Allen, P. M. (2010) High-affinity T cell receptor differentiates cognate peptide-MHC and altered peptide ligands with distinct kinetics and thermodynamics. Mol. Immunol. 47, 1793-1801
49. Holland, S. J., Bartok, I., Attaf, M., Genolet, R., Luescher, I. F., Kotsiou, E., Richard, A., Wang, E., White, M., Coe, D. J., Chai, J. G., Ferreira, C., and Dyson, J. (2012) The T-cell receptor is not hardwired to engage MHC ligands. Proc. Natl. Acad. Sci. U.S.A. 109, E3111-3118
50. Piepenbrink, K. H., Blevins, S. J., Scott, D. R., and Baker, B. M. (2013) The basis for limited specificity and MHC restriction in a T cell receptor interface. Nat. Commun. 4, 1948
51. Ding, Y. H., Baker, B. M., Garboczi, D. N., Biddison, W. E., and Wiley, D. C. (1999) Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 11, 45-56
52. Ding, Y. H., Smith, K. J., Garboczi, D. N., Utz, U., Biddison, W. E., and Wiley, D. C. (1998) Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 8, 403-411
53. Alam, S. M., Travers, P. J., Wung, J. L., Nasholds, W., Redpath, S., Jameson, S. C., and Gascoigne, N. R. (1996) T-cell-receptor affinity and thymocyte positive selection. Nature 381, 616-620
54. Archbold, J. K., Macdonald, W. A., Miles, J. J., Brennan, R. M., Kjer-Nielsen, L., McCluskey, J., Burrows, S. R., and Rossjohn, J. (2006) Alloreactivity between disparate cognate and allogeneic pMHC-I complexes is the result of highly focused, peptide-dependent structural mimicry. J. Biol. Chem. 281, 34324-34332
55. Macdonald, W. A., Chen, Z., Gras, S., Archbold, J. K., Tynan, F. E., Clements, C. S., Bharadwaj, M., Kjer-Nielsen, L., Saunders, P. M., Wilce, M. C., Crawford, F., Stadinsky, B., Jackson, D., Brooks, A. G., Purcell, A. W., Kappler, J. W., Burrows, S. R., Rossjohn, J., and McCluskey, J. (2009) T cell allorecognition via molecular mimicry. Immunity 31, 897-908
56. Reiser, J. B., Darnault, C., Guimezanes, A., Grégoire, C., Mosser, T., Schmitt-Verhulst, A. M., Fontecilla-Camps, J. C., Malissen, B., Housset, D., and Mazza, G. (2000) Crystal structure of a T cell receptor bound to an allogeneic MHC molecule. Nat. Immunol. 1, 291-297
57. van der Merwe, P. A., and Davis, S. J. (2003) Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21, 659-684
58. Choudhuri, K., Wiseman, D., Brown, M. H., Gould, K., and van der Merwe, P. A. (2005) T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436, 578-582
59. Davis, S. J., and van der Merwe, P. A. (2006) The kinetic-segregation model: TCR triggering and beyond. Nat. Immunol. 7, 803-809
60. Dustin, M. L., Bromley, S. K., Kan, Z., Peterson, D. A., and Unanue, E. R. (1997) Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 94, 3909-3913
61. Mempel, T. R., Henrickson, S. E., and Von Andrian, U. H. (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427, 154-159
62. Negulescu, P. A., Krasieva, T. B., Khan, A., Kerschbaum, H. H., and Cahalan, M. D. (1996) Polarity of T cell shape, motility, and sensitivity to antigen. Immunity 4, 421-430
63. Schneider, H., Downey, J., Smith, A., Zinselmeyer, B. H., Rush, C., Brewer, J. M., Wei, B., Hogg, N., Garside, P., and Rudd, C. E. (2006) Reversal of the TCR stop signal by CTLA-4. Science 313, 1972-1975
64. Chen, J. L., Stewart-Jones, G., Bossi, G., Lissin, N. M., Wooldridge, L., Choi, E. M., Held, G., Dunbar, P. R., Esnouf, R. M., Sami, M., Boulter, J. M., Rizkallah, P., Renner, C., Sewell, A., van der Merwe, P. A., Jakobsen, B. K., Griffiths, G., Jones, E. Y., and Cerundolo, V. (2005) Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 201, 1243-1255