Structural basis for ineffective T-cell responses to MHC anchor residue-improved "heteroclitic" peptides

European Journal of Immunology

Volumn 45, Issue 2, 2015, Pages 584-591

  Madura, Florian ^a   Rizkallah, Pierre J ^a   Holland, Christopher J ^a   Fuller, Anna ^a   Bulek, Anna ^a   Godkin, Andrew J ^a   Schauenburg, Andrea J ^a   Cole, David K ^a   Sewell, Andrew K ^a  

^a CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Cross reactivity; Crystal structure; MART 1; Melan A; Melanoma; Peptide major histocompatibility complex; Surface plasmon resonance; T cell; TCR

Indexed keywords

HLA A ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; MELAN A; ALANINE; EPITOPE; HLA A2 ANTIGEN; HLA-A*02:01 ANTIGEN; LEUCINE; LYMPHOCYTE ANTIGEN RECEPTOR; PEPTIDE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE; T LYMPHOCYTE; THERMODYNAMICS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY;

ALANINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CRYSTALLOGRAPHY, X-RAY; EPITOPES, T-LYMPHOCYTE; ESCHERICHIA COLI; GENE EXPRESSION; HLA-A2 ANTIGEN; HUMANS; LEUCINE; MART-1 ANTIGEN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINANT PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84923104148     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445114     Document Type: Article

References (49)

1. Rosenberg, S. A., Yang, J. C. and Restifo, N. P., Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 2004. 10: 909-915.
2. Bridgeman, J. S., Sewell, A. K., Miles, J. J., Price, D. A. and Cole, D. K., Structural and biophysical determinants of αβ T-cell antigen recognition. Immunology 2012. 135: 9-18.
3. 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.
4. Cole, D. K., Pumphrey, N. J., Boulter, J. M., Sami, M., Bell, J. I., Gostick, E., Price, D. A. et al., Human TCR-binding affinity is governed by MHC class restriction. J. Immunol. 2007. 178: 5727-5734.
5. Aleksic, M., Liddy, N., Molloy, P. E., Pumphrey, N., Vuidepot, A., Chang, K.-M. and Jakobsen, B. K., Different affinity windows for virus and cancer-specific T-cell receptors: implications for therapeutic strategies. Eur. J. Immunol. 2012. 42: 3174-3179.
6. Miles, K. M., Miles, J. J., Madura, F., Sewell, A. K. and Cole, D. K., Real time detection of peptide-MHC dissociation reveals that improvement of primary MHC-binding residues can have a minimal, or no, effect on stability. Mol. Immunol. 2011. 48: 728-732.
7. Saper, M. A., Bjorkman, P. J. and Wiley, D. C., Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J. Mol. Biol. 1991. 219: 277-319.
8. Falk, K., Rotzschke, O., Takiguchi, M., Grahovac, B., Gnau, V., Stevanovic, S., Jung, G. et al., Peptide motifs of HLA-A1, -A11, -A31, and -A33 molecules. Immunogenetics 1994. 40: 238-241.
9. Rammensee, H. G., Friede, T. and Stevanoviic, S., MHC ligands and peptide motifs: first listing. Immunogenetics 1995. 41: 178-228.
10. Tynan, F. E., Burrows, S. R., Buckle, A. M., Clements, C. S., Borg, N. A., Miles, J. J., Beddoe, T. et al., T cell receptor recognition of a "super-bulged" major histocompatibility complex class I-bound peptide. Nat. Immunol. 2005. 6: 1114-1122.
11. Ekeruche-Makinde, J., Miles, J. J., van den Berg, H. A., Skowera, A., Cole, D. K., Dolton, G., Schauenburg, A. J. A. et al., Peptide length determines the outcome of TCR/peptide-MHCI engagement. Blood 2013. 121: 1112-1123.
12. Robinson, J., Halliwell, J. A., McWilliam, H., Lopez, R., Parham, P. and Marsh, S. G. E., The IMGT/HLA database. Nucleic Acids Res. 2013. 41: D1222-D1227.
13. Liénard, D., Rimoldi, D., Marchand, M., Dietrich, P.-Y., van Baren, N., Geldhof, C., Batard, P. et al., Ex vivo detectable activation of Melan-A-specific T cells correlating with inflammatory skin reactions in melanoma patients vaccinated with peptides in IFA. Cancer Immun. 2004. 4: 4.
14. Rosenberg, S. A., Yang, J. C., Schwartzentruber, D. J., Hwu, P., Marincola, F. M., Topalian, S. L., Restifo, N. P. et al., Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 1998. 4: 321-327.
15. Houghton, C. S. B., Engelhorn, M. E., Liu, C., Song, D., Gregor, P., Livingston, P. O., Orlandi, F. et al., Immunological validation of the EpitOptimizer program for streamlined design of heteroclitic epitopes. Vaccine 2007. 25: 5330-5342.
16. Chen, J.-L., Stewart-Jones, G., Bossi, G., Lissin, N. M., Wooldridge, L., Choi, E. M. L., Held, G. et al., Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 2005. 201: 1243-1255.
17. Garboczi, D. N., Ghosh, P., Utz, U., Fan, Q. R., Biddison, W. E. and Wiley, D. C., Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996. 384: 134-141.
18. Rudolph, M. G., Stanfield, R. L. and Wilson, I. A., How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 2006. 24: 419-466.
19. Cole, D. K., Edwards, E. S. J., Wynn, K. K., Clement, M., Miles, J. J., Ladell, K., Ekeruche, J. et al., Modification of MHC anchor residues generates heteroclitic peptides that alter TCR binding and T cell recognition. J. Immunol. 2010. 185: 2600-2610.
20. Valmori, D., Fonteneau, J. F., Lizana, C. M., Gervois, N., Liénard, D., Rimoldi, D., Jongeneel, V. et al., Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J. Immunol. 1998. 160: 1750-1758.
21. Ayyoub, M., Zippelius, A., Pittet, M. J., Rimoldi, D., Valmori, D., Cerottini, J.-C., Romero, P. et al., Activation of human melanoma reactive CD8+ T cells by vaccination with an immunogenic peptide analog derived from Melan-A/melanoma antigen recognized by T cells-1. Clin. Cancer Res. 2003. 9: 669-677.
22. Romero, P., Valmori, D., Pittet, M. J., Zippelius, A., Rimoldi, D., Lévy, F., Dutoit, V. et al., Antigenicity and immunogenicity of Melan-A/MART-1 derived peptides as targets for tumor reactive CTL in human melanoma. Immunol. Rev. 2002. 188: 81-96.
23. Speiser, D. E., Baumgaertner, P., Voelter, V., Devevre, E., Barbey, C., Rufer, N. and Romero, P., Unmodified self antigen triggers human CD8 T cells with stronger tumor reactivity than altered antigen. Proc. Natl. Acad. Sci. USA 2008. 105: 3849-3854.
24. Wieckowski, S., Baumgaertner, P., Corthesy, P., Voelter, V., Romero, P., Speiser, D. E. and Rufer, N., Fine structural variations of alphabetaTCRs selected by vaccination with natural versus altered self-antigen in melanoma patients. J. Immunol. 2009. 183: 5397-5406.
25. Cole, D. K., Yuan, F., Rizkallah, P. J., Miles, J. J., Gostick, E., Price, D. A., Gao, G. F. et al., Germ line-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J. Biol. Chem. 2009. 284: 27281-27289.
26. Borbulevych, O. Y., Insaidoo, F. K., Baxter, T. K., Powell, D. J., Johnson, L. A., Restifo, N. P. and Baker, B. M., Structures of MART-126/27-35 Peptide/HLA-A2 complexes reveal a remarkable disconnect between antigen structural homology and T cell recognition. J. Mol. Biol. 2007. 372: 1123-1136.
27. Borbulevych, O. Y., Santhanagopolan, S. M., Hossain, M. and Baker, B. M., TCRs used in cancer gene therapy cross-react with MART-1/Melan-A tumor antigens via distinct mechanisms. J. Immunol. 2011. 187: 2453-2463.
28. Armstrong, K. M., Insaidoo, F. K. and Baker, B. M., Thermodynamics of T-cell receptor-peptide/MHC interactions: progress and opportunities. J. Mol. Recognit. 2008. 21: 275-287.
29. Miles, J. J., Bulek, A. M., Cole, D. K., Gostick, E., Schauenburg, A. J. A., Dolton, G., Venturi, V. et al., Genetic and structural basis for selection of a ubiquitous T cell receptor deployed in Epstein-Barr virus infection. PLoS Pathog. 2010. 6: e1001198.
30. Rudolph, M. G. and Wilson, I. A., The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 2002. 14: 52-65.
31. Li, Y., Huang, Y., Lue, J., Quandt, J. A., Martin, R. and Mariuzza, R. A., Structure of a human autoimmune TCR bound to a myelin basic protein self-peptide and a multiple sclerosis-associated MHC class II molecule. EMBO J. 2005. 24: 2968-2979.
32. Bulek, A. M., Cole, D. K., Skowera, A., Dolton, G., Gras, S., Madura, F., Fuller, A. et al., Structural basis for the killing of human beta cells by CD8(+) T cells in type 1 diabetes. Nat. Immunol. 2012. 13: 283-289.
33. Van Stipdonk, M. J. B., Badia-Martinez, D., Sluijter, M., Offringa, R., van Hall, T. and Achour, A., Design of agonistic altered peptides for the robust induction of CTL directed towards H-2Db in complex with the melanoma-associated epitope gp100. Cancer Res. 2009. 69: 7784-7792.
34. Madura, F., Rizkallah, P. J., Miles, K. M., Holland, C. J., Bulek, A. M., Fuller, A., Schauenburg, A. J. A. et al., T-cell receptor specificity maintained by altered thermodynamics. J. Biol. Chem. 2013. 288: 18766-18775.
35. Cole, D. K., Miles, K. M., Madura, F., Holland, C. J., Schauenburg, A. J. A., Godkin, A. J., Bulek, A. M. et al., T-cell receptor (TCR)-peptide specificity overrides affinity-enhancing TCR-major histocompatibility complex interactions. J. Biol. Chem. 2014. 289: 628-638.
36. Allerbring, E. B., Duru, A. D., Uchtenhagen, H., Madhurantakam, C., Tomek, M. B., Grimm, S., Mazumdar, P. A. et al., Unexpected T-cell recognition of an altered peptide ligand is driven by reversed thermodynamics. Eur. J. Immunol. 2012. 42: 2990-3000.
37. Buhrman, J. D., Jordan, K. R., Munson, D. J., Moore, B. L., Kappler, J. W. and Slansky, J. E., Improving antigenic peptide vaccines for cancer immunotherapy using a dominant tumor-specific T cell receptor. J. Biol. Chem. 2013. 288: 33213-33225.
38. Buhrman, J. D. and Slansky, J. E., Improving T cell responses to modified peptides in tumor vaccines. Immunol. Res. 2013. 55: 34-47.
39. Ekeruche-Makinde, J., Clement, M., Cole, D. K., Edwards, E. S. J., Ladell, K., Miles, J. J., Matthews, K. K. et al., T-cell receptor-optimized peptide skewing of the T-cell repertoire can enhance antigen targeting. J. Biol. Chem. 2012. 287: 37269-37281.
40. Sewell, A. K., Why must T cells be cross-reactive? Nat. Rev. Immunol. 2012. 12: 669-677.
41. Holland, C. J., Rizkallah, P. J., Vollers, S., Calvo-Calle, J. M., Madura, F., Fuller, A., Sewell, A. K. et al., Minimal conformational plasticity enables TCR cross-reactivity to different MHC class II heterodimers. Sci. Rep. 2012. 2: 629.
42. Cole, D. K., Dunn, S. M., Sami, M., Boulter, J. M., Jakobsen, B. K. and Sewell, A. K., T cell receptor engagement of peptide-major histocompatibility complex class I does not modify CD8 binding. Mol. Immunol. 2008. 45: 2700-2709.
43. Cole, D. K., Rizkallah, P. J., Gao, F., Watson, N. I., Boulter, J. M., Bell, J. I., Sami, M. et al., Crystal structure of HLA-A*2402 complexed with a telomerase peptide. Eur. J. Immunol. 2006. 36: 170-179.
44. Bulek, A. M., Madura, F., Fuller, A., Holland, C. J., Schauenburg, A. J. A., Sewell, A. K., Rizkallah, P. J. et al., TCR/pMHC optimized protein crystallization screen. J. Immunol. Methods 2012. 382: 203-210.
45. Winter, G., Lobley, C. M. C. and Prince, S. M., Decision making in xia2. Acta Crystallogr. D Biol. Crystallogr. 2013. 69: 1260-1273.
46. Collaborative Computational Project N 4. The CCP4 suite: programs for protein crystallography. Acta. Crystallogr. D. Biol. Crystallogr. 1994. 50: 760-763.
47. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J., Phaser crystallographic software. J. Appl. Crystallogr. 2007. 40: 658-674.
48. Emsley, P. and Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004. 60: 2126-2132.
49. Murshudov, G. N., Vagin, A. A. and Dodson, E. J., Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D Biol. Crystallogr. 1997. 53: 240-255.