Modification of MHC anchor residues generates heteroclitic peptides that alter TCR binding and T cell recognition

Journal of Immunology

Volumn 185, Issue 4, 2010, Pages 2600-2610

  Cole, David K ^a   Edwards, Emily S J ^a   Wynn, Katherine K ^a   Clement, Mathew ^a   Miles, John J ^a,d   Ladell, Kristin ^a   Ekeruche, Julia ^a   Gostick, Emma ^a   Adams, Katherine J ^b   Skowera, Ania ^c   Peakman, Mark ^c   Wooldridge, Linda ^a   Price, David A ^a   Sewell, Andrew K ^a  

^a CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^b Immunocore Limited   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; TETRAMER; CYTOKINE; EPITOPE; HLA A ANTIGEN; HLA A*0201 ANTIGEN; HLA-A*0201 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MHC BINDING PEPTIDE; OLIGOPEPTIDE; PEPTIDE LIBRARY;

AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CELL SURFACE; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BINDING; SURFACE PLASMON RESONANCE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VACCINATION; CD8+ T LYMPHOCYTE; CELL CULTURE; CYTOTOXIC T LYMPHOCYTE; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MUTATION; PROTEIN BINDING;

AMINO ACID SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; EPITOPES, T-LYMPHOCYTE; FLOW CYTOMETRY; HLA-A ANTIGENS; HUMANS; MUTATION; OLIGOPEPTIDES; PEPTIDE LIBRARY; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; SURFACE PLASMON RESONANCE; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 77956914881     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000629     Document Type: Article

References (59)

1. Davis, M. M., and P. J. Bjorkman. 1988. T-cell antigen receptor genes and T-cell recognition. Nature 334: 395-402.
2. Garcia, K. C., M. Degano, J. A. Speir, and I. A. Wilson. 1999. Emerging principles for T cell receptor recognition of antigen in cellular immunity. Rev. Immunogenet. 1: 75-90.
3. Chen, J. L., G. Stewart-Jones, G. Bossi, N. M. Lissin, L. Wooldridge, E. M. Choi, G. Held, P. R. Dunbar, R. M. Esnouf, M. Sami, et al. 2005. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 201: 1243-1255.
4. Keogh, E., J. Fikes, S. Southwood, E. Celis, R. Chesnut, and A. Sette. 2001. Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA-Ap0201-binding affinity. J. Immunol. 167: 787-796.
5. Laugel, B., H. A. van den Berg, E. Gostick, D. K. Cole, L. Wooldridge, J. Boulter, A. Milicic, D. A. Price, and A. K. Sewell. 2007. Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J. Biol. Chem. 282: 23799-23810.
6. Parkhurst, M. R., M. L. Salgaller, S. Southwood, P. F. Robbins, A. Sette, S. A. Rosenberg, and Y. Kawakami. 1996. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-Ap0201-binding residues. J. Immunol. 157: 2539-2548.
7. Shang, X., L.Wang, W. Niu, G. Meng, X. Fu, B. Ni, Z. Lin, Z. Yang, X. Chen, and Y. Wu. 2009. Rational optimization of tumor epitopes using in silico analysis-assisted substitution of TCR contact residues. Eur. J. Immunol. 39: 2248-2258.
8. Terasawa, H., K. Y. Tsang, J. Gulley, P. Arlen, and J. Schlom. 2002. Identification and characterization of a human agonist cytotoxic T-lymphocyte epitope of human prostate-specific antigen. Clin. Cancer Res. 8: 41-53.
9. Valmori, D., J. F. Fonteneau, C. M. Lizana, N. Gervois, D. Liénard, D. Rimoldi, V. Jongeneel, F. Jotereau, J. C. Cerottini, and P. Romero. 1998. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J. Immunol. 160: 1750-1758.
10. La Rosa, C., R. Krishnan, S. Markel, J. P. Schneck, R. Houghten, C. Pinilla, and D. J. Diamond. 2001. Enhanced immune activity of cytotoxic T-lymphocyte epitope analogs derived from positional scanning synthetic combinatorial libraries. Blood 97: 1776-1786.
11. Udaka, K., K. H. Wiesmüller, S. Kienle, G. Jung, and P. Walden. 1995. Decrypting the structure of major histocompatibility complex class I-restricted cytotoxic T lymphocyte epitopes with complex peptide libraries. J. Exp. Med. 181: 2097-2108.
12. Rammensee, H. G., T. Friede, and S. Stevanoviíc. 1995. MHC ligands and peptide motifs: first listing. Immunogenetics 41: 178-228.
13. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanović. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
14. Parker, K. C., M. A. Bednarek, L. K. Hull, U. Utz, B. Cunningham, H. J. Zweerink, W. E. Biddison, and J. E. Coligan. 1992. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J. Immunol. 149: 3580-3587.
15. Hunt, D. F., R. A. Henderson, J. Shabanowitz, K. Sakaguchi, H. Michel, N. Sevilir, A. L. Cox, E. Appella, and V. H. Engelhard. 1992. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science 255: 1261-1263.
16. Peakman, M., and C. M. Dayan. 2001. Antigen-specific immunotherapy for autoimmune disease: fighting fire with fire? Immunology 104: 361-366.
17. Voskens, C. J., S. E. Strome, and D. A. Sewell. 2009. Synthetic peptide-based cancer vaccines: lessons learned and hurdles to overcome. Curr. Mol. Med. 9: 683-693.
18. Cole, D. K., N. J. Pumphrey, J. M. Boulter, M. Sami, J. I. Bell, E. Gostick, D. A. Price, G. F. Gao, A. K. Sewell, and B. K. Jakobsen. 2007. Human TCRbinding affinity is governed by MHC class restriction. J. Immunol. 178: 5727-5734.
19. Rosenberg, S. A., J. C. Yang, D. J. Schwartzentruber, P. Hwu, F. M. Marincola, S. L. Topalian, N. P. Restifo, M. E. Dudley, S. L. Schwarz, P. J. Spiess, et al. 1998. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 4: 321-327.
20. Houghton, C. S., M. E. Engelhorn, C. Liu, D. Song, P. Gregor, P. O. Livingston, F. Orlandi, J. D. Wolchok, J. McCracken, A. N. Houghton, and J. A. Guevara-Patiño. 2007. Immunological validation of the EpitOptimizer program for streamlined design of heteroclitic epitopes. Vaccine 25: 5330-5342.
21. Speiser, D. E., P. Baumgaertner, V. Voelter, E. Devevre, C. Barbey, N. Rufer, and P. Romero. 2008. Unmodified self antigen triggers human CD8 T cells with stronger tumor reactivity than altered antigen. Proc. Natl. Acad. Sci. USA 105: 3849-3854.
22. Skowera, A., R. J. Ellis, R. Varela-Calviño, S. Arif, G. C. Huang, C. Van-Krinks, A. Zaremba, C. Rackham, J. S. Allen, T. I. Tree, et al. 2008. CTLs are targeted to kill beta cells in patients with type 1 diabetes through recognition of a glucoseregulated preproinsulin epitope. J. Clin. Invest. 118: 3390-3402.
23. Lissina, A., K. Ladell, A. Skowera, M. Clement, E. Edwards, R. Seggewiss, H. A. van den Berg, E. Gostick, K. Gallagher, E. Jones, et al. 2009. Protein kinase inhibitors substantially improve the physical detection of T-cells with peptide-MHC tetramers. J. Immunol. Methods 340: 11-24.
24. Cole, D. K., F. Yuan, P. J. Rizkallah, J. J. Miles, E. Gostick, D. A. Price, G. F. Gao, B. K. Jakobsen, and A. K. Sewell. 2009. Germ line-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J. Biol. Chem. 284: 27281-27289.
25. Wooldridge, L., A. Lissina, J. Vernazza, E. Gostick, B. Laugel, S. L. Hutchinson, F. Mirza, P. R. Dunbar, J. M. Boulter, M. Glick, et al. 2007. Enhanced immunogenicity of CTL antigens through mutation of the CD8 binding MHC class I invariant region. Eur. J. Immunol. 37: 1323-1333.
26. Garboczi, D. N., P. Ghosh, U. Utz, Q. R. Fan, W. E. Biddison, and D. C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384: 134-141.
27. Boulter, J. M., M. Glick, P. T. Todorov, E. Baston, M. Sami, P. Rizkallah, and B. K. Jakobsen. 2003. Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng. 16: 707-711.
28. Wyer, J. R., B. E. Willcox, G. F. Gao, U. C. Gerth, S. J. Davis, J. I. Bell, P. A. van der Merwe, and B. K. Jakobsen. 1999. T cell receptor and coreceptor CD8 alphaalpha bind peptide-MHC independently and with distinct kinetics. Immunity 10: 219-225.
29. Salter, R. D., and P. Cresswell. 1986. Impaired assembly and transport of HLA-A and -B antigens in a mutant TxB cell hybrid. EMBO J. 5: 943-949.
30. Betts, M. R., J. M. Brenchley, D. A. Price, S. C. De Rosa, D. C. Douek, M. Roederer, and R. A. Koup. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78.
31. Wooldridge, L., A. Lissina, D. K. Cole, H. A. van den Berg, D. A. Price, and A. K. Sewell. 2009. Tricks with tetramers: how to get the most from multimeric peptide-MHC. Immunology 126: 147-164.
32. Wooldridge, L., H. A. van den Berg, M. Glick, E. Gostick, B. Laugel, S. L. Hutchinson, A. Milicic, J. M. Brenchley, D. C. Douek, D. A. Price, and A. K. Sewell. 2005. Interaction between the CD8 coreceptor and major histocompatibility complex class I stabilizes T cell receptor-antigen complexes at the cell surface. J. Biol. Chem. 280: 27491-27501.
33. Price, D. A., J. M. Brenchley, L. E. Ruff, M. R. Betts, B. J. Hill, M. Roederer, R. A. Koup, S. A. Migueles, E. Gostick, L. Wooldridge, et al. 2005. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
34. Lefranc, M. P., C. Pommié, M. Ruiz, V. Giudicelli, E. Foulquier, L. Truong, V. Thouvenin-Contet, and G. Lefranc. 2003. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev. Comp. Immunol. 27: 55-77.
35. Rosenberg, S. A., J. C. Yang, and N. P. Restifo. 2004. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10: 909-915.
36. Morgan, R. A., M. E. Dudley, J. R. Wunderlich, M. S. Hughes, J. C. Yang, R. M. Sherry, R. E. Royal, S. L. Topalian, U. S. Kammula, N. P. Restifo, et al. 2006. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129.
37. Bins, A., H. Mallo, J. Sein, C. van den Bogaard, W. Nooijen, F. Vyth-Dreese, B. Nuijen, G. C. de Gast, and J. B. Haanen. 2007. Phase I clinical study with multiple peptide vaccines in combination with tetanus toxoid and GM-CSF in advanced-stage HLA-Ap0201-positive melanoma patients. J. Immunother. 30: 234-239.
38. Meidenbauer, N., J. Marienhagen, M. Laumer, S. Vogl, J. Heymann, R. Andreesen, and A. Mackensen. 2003. Survival and tumor localization of adoptively transferred Melan-A-specific T cells in melanoma patients. J. Immunol. 170: 2161-2169.
39. Chen, Q., H. Jackson, M. Shackleton, P. Parente, W. Hopkins, S. Sturrock, D. MacGregor, E. Maraskovsky, T. Y. Tai, N. Dimopoulos, et al. 2005. Characterization of antigen-specific CD8+ T lymphocyte responses in skin and peripheral blood following intradermal peptide vaccination. Cancer Immun. 5: 5.
40. Clay, T. M., M. C. Custer, M. D. McKee, M. Parkhurst, P. F. Robbins, K. Kerstann, J. Wunderlich, S. A. Rosenberg, and M. I. Nishimura. 1999. Changes in the fine specificity of gp100(209-217)-reactive T cells in patients following vaccination with a peptide modified at an HLA-A2.1 anchor residue. J. Immunol. 162: 1749-1755.
41. Pass, H. A., S. L. Schwarz, J. R. Wunderlich, and S. A. Rosenberg. 1998. Immunization of patients with melanoma peptide vaccines: immunologic assessment using the ELISPOT assay. Cancer J. Sci. Am. 4: 316-323.
42. Rubio, V., T. B. Stuge, N. Singh, M. R. Betts, J. S. Weber, M. Roederer, and P. P. Lee. 2003. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat. Med. 9: 1377-1382.
43. Madden, D. R., D. N. Garboczi, and D. C. Wiley. 1993. The antigenic identity of peptide-MHC complexes: a comparison of the conformations of five viral peptides presented by HLA-A2. Cell 75: 693-708.
44. Guo, H. C., D. R. Madden, M. L. Silver, T. S. Jardetzky, J. C. Gorga, J. L. Strominger, and D. C. Wiley. 1993. Comparison of the P2 specificity pocket in three human histocompatibility antigens: HLA-Ap6801, HLA-Ap0201, and HLA-Bp2705. Proc. Natl. Acad. Sci. USA 90: 8053-8057.
45. Speiser, D. E., D. Liénard, M. J. Pittet, P. Batard, D. Rimoldi, P. Guillaume, J. C. Cerottini, and P. Romero. 2002. In vivo activation of melanoma-specific CD8(+) T cells by endogenous tumor antigen and peptide vaccines. A comparison to virus-specific T cells. Eur. J. Immunol. 32: 731-741.
46. Varela-Rohena, A., P. E. Molloy, S. M. Dunn, Y. Li, M. M. Suhoski, R. G. Carroll, A. Milicic, T. Mahon, D. H. Sutton, B. Laugel, et al. 2008. Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat. Med. 14: 1390-1395.
47. Borbulevych, O. Y., F. K. Insaidoo, T. K. Baxter, D. J. Powell, Jr., L. A. Johnson, N. P. Restifo, and B. M. Baker. 2007. 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. 372: 1123-1136.
48. Sliz, P., O. Michielin, J. C. Cerottini, I. Luescher, P. Romero, M. Karplus, and D. C. Wiley. 2001. Crystal structures of two closely related but antigenically distinct HLA-A2/melanocyte-melanoma tumor-antigen peptide complexes. J. Immunol. 167: 3276-3284.
49. Tynan, F. E., S. R. Burrows, A. M. Buckle, C. S. Clements, N. A. Borg, J. J. Miles, T. Beddoe, J. C. Whisstock, M. C. Wilce, S. L. Silins, et al. 2005. T cell receptor recognition of a 'super-bulged' major histocompatibility complex class I-bound peptide. Nat. Immunol. 6: 1114-1122.
50. Tynan, F. E., H. H. Reid, L. Kjer-Nielsen, J. J. Miles, M. C. Wilce, L. Kostenko, N. A. Borg, N. A. Williamson, T. Beddoe, A. W. Purcell, et al. 2007. A T cell receptor flattens a bulged antigenic peptide presented by a major histocompatibility complex class I molecule. Nat. Immunol. 8: 268-276.
51. Macdonald, W. A., Z. Chen, S. Gras, J. K. Archbold, F. E. Tynan, C. S. Clements, M. Bharadwaj, L. Kjer-Nielsen, P. M. Saunders, M. C. Wilce, et al. 2009. T cell allorecognition via molecular mimicry. Immunity 31: 897-908.
52. Wieckowski, S., P. Baumgaertner, P. Corthesy, V. Voelter, P. Romero, D. E. Speiser, and N. Rufer. 2009. Fine structural variations of alphabetaTCRs selected by vaccination with natural versus altered self-antigen in melanoma patients. J. Immunol. 183: 5397-5406.
53. Vignard, V., B. Lemercier, A. Lim, M. C. Pandolfino, Y. Guilloux, A. Khammari, C. Rabu, K. Echasserieau, F. Lang, M. L. Gougeon, et al. 2005. Adoptive transfer of tumor-reactive Melan-A-specific CTL clones in melanoma patients is followed by increased frequencies of additional Melan-A-specific T cells. J. Immunol. 175: 4797-4805.
54. Serana, F., A. Sottini, L. Caimi, B. Palermo, P. G. Natali, P. Nisticò, and L. Imberti. 2009. Identification of a public CDR3 motif and a biased utilization of T-cell receptor V beta and J beta chains in HLA-A2/Melan-A-specific T-cell clonotypes of melanoma patients. J. Transl. Med. 7: 21.
55. Rudolph, M. G., R. L. Stanfield, and I. A. Wilson. 2006. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24: 419-466.
56. Borbulevych, O. Y., T. K. Baxter, Z. Yu, N. P. Restifo, and B. M. Baker. 2005. Increased immunogenicity of an anchor-modified tumor-associated antigen is due to the enhanced stability of the peptide/MHC complex: implications for vaccine design. J. Immunol. 174: 4812-4820.
57. Bowerman, N. A., T. S. Crofts, L. Chlewicki, P. Do, B. M. Baker, K. Christopher Garcia, and D. M. Kranz. 2009. Engineering the binding properties of the T cell receptor:peptide:MHC ternary complex that governs T cell activity. Mol. Immunol. 46: 3000-3008.
58. Finke, L. H., K. Wentworth, B. Blumenstein, N. S. Rudolph, H. Levitsky, and A. Hoos. 2007. Lessons from randomized phase III studies with active cancer immunotherapies - outcomes from the 2006 meeting of the Cancer Vaccine Consortium (CVC). Vaccine 25(Suppl 2): B97-B109.
59. Jones, V. E., and M. S. Mitchell. 1996. Therapeutic vaccines for melanoma: progress and problems. Trends Biotechnol. 14: 349-355.