Unexpected T-cell recognition of an altered peptide ligand is driven by reversed thermodynamics

European Journal of Immunology

Volumn 42, Issue 11, 2012, Pages 2990-3000

  Allerbring, Eva B ^a   Duru, Adil D ^a   Uchtenhagen, Hannes ^a   Madhurantakam, Chaithanya ^a   Tomek, Markus B ^a   Grimm, Sebastian ^b   Mazumdar, Pooja A ^a   Friemann, Rosmarie ^c   Uhlin, Michael ^d   Sandalova, Tatyana ^a   Nygren, Per Åke ^b   Achour, Adnane ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

MHC; Molecular immunology; Protein protein interactions; Structural biology; TCR

Indexed keywords

ALANINE; GP33 PEPTIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PHENYLALANINE; PROTEIN P14; SERINE; T LYMPHOCYTE RECEPTOR; TYROSINE; UNCLASSIFIED DRUG; Y4A PEPTIDE; Y4F PEPTIDE; Y4S PEPTIDE;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENTHALPY; ENTROPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THERMODYNAMICS;

ANIMALS; ANTIGENS, VIRAL; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; GLYCOPROTEINS; H-2 ANTIGENS; KINETICS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; PEPTIDES; PROTEINS; RECEPTORS, ANTIGEN, T-CELL; SPECIFIC PATHOGEN-FREE ORGANISMS; SURFACE PLASMON RESONANCE; THERMODYNAMICS; VIRAL PROTEINS;

EID: 84868097098     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242588     Document Type: Article

References (70)

1. Godfrey, D. I., Rossjohn, J. and McCluskey, J., The fidelity, occasional promiscuity, and versatility of T cell receptor recognition. Immunity 2008. 28: 304-314.
2. Martinez-Hackert, E., Anikeeva, N., Kalams, S. A., Walker, B. D., Hendrickson, W. A. and Sykulev, Y., Structural basis for degenerate recognition of natural HIV peptide variants by cytotoxic lymphocytes. J. Biol. Chem. 2006. 281: 20205-20212.
3. 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.
4. Colf, L. A., Bankovich, A. J., Hanick, N. A., Bowerman, N. A., Jones, L. L., Kranz, D. M. and Garcia, K. C., How a single T cell receptor recognizes both self and foreign MHC. Cell 2007. 129: 135-146.
5. Mazza, C., Auphan-Anezin, N., Gregoire, C., Guimezanes, A., Kellenberger, C., Roussel, A., Kearney, A. et al., How much can a T-cell antigen receptor adapt to structurally distinct antigenic peptides? EMBO. J. 2007. 26: 1972-1983.
6. Macdonald, W. A., Chen, Z., Gras, S., Archbold, J. K., Tynan, F. E., Clements, C. S., Bharadwaj, M. et al., T cell allorecognition via molecular mimicry. Immunity 2009. 31: 897-908.
7. Baker, B. M., Gagnon, S. J., Biddison, W. E. and Wiley, D. C., Conversion of a T cell antagonist into an agonist by repairing a defect in the TCR/peptide/MHC interface: implications for TCR signaling. Immunity 2000. 13: 475-484.
8. Sloan-Lancaster, J. and Allen, P. M., Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu. Rev. Immunol. 1996. 14: 1-27.
9. Jones, L. L., Colf, L. A., Bankovich, A. J., Stone, J. D., Gao, Y. G., Chan, C. M., Huang, R. H. et al., Different thermodynamic binding mechanisms and peptide fine specificities associated with a panel of structurally similar high-affinity T cell receptors. Biochemistry 2008. 47: 12398-12408.
10. Baker, B. M., Turner, R. V., Gagnon, S. J., Wiley, D. C. and Biddison, W. E., Identification of a crucial energetic footprint on the alpha1 helix of human histocompatibility leukocyte antigen (HLA)-A2 that provides functional interactions for recognition by tax peptide/HLA-A2-specific T cell receptors. J. Exp. Med. 2001. 193: 551-562.
11. Baxter, T. K., Gagnon, S. J., Davis-Harrison, R. L., Beck, J. C., Binz, A. K., Turner, R. V., Biddison, W. E. et al., Strategic mutations in the class I major histocompatibility complex HLA-A2 independently affect both peptide binding and T cell receptor recognition. J. Biol. Chem. 2004. 279: 29175-29184.
12. Gagnon, S. J., Borbulevych, O. Y., Davis-Harrison, R. L., Baxter, T. K., Clemens, J. R., Armstrong, K. M., Turner, R. V. et al., Unraveling a hotspot for TCR recognition on HLA-A2: evidence against the existence of peptide-independent TCR binding determinants. J. Mol. Biol. 2005. 353: 556-573.
13. Miller, P. J., Pazy, Y., Conti, B., Riddle, D., Appella, E. and Collins, E. J., Single MHC mutation eliminates enthalpy associated with T cell receptor binding. J. Mol. Biol. 2007. 373: 315-327.
14. Rudolph, M. G., Stanfield, R. L. and Wilson, I. A., How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 2006. 24: 419-466.
15. 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.
16. Burrows, S. R., Chen, Z., Archbold, J. K., Tynan, F. E., Beddoe, T., Kjer-Nielsen, L., Miles, J. J. et al., Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Proc. Natl. Acad. Sci. USA 2010. 107: 10608-10613.
17. 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.
18. Gras, S., Chen, Z., Miles, J. J., Liu, Y. C., Bell, M. J., Sullivan, L. C., Kjer-Nielsen, L. et al., Allelic polymorphism in the T cell receptor and its impact on immune responses. J. Exp. Med. 2010. 207: 1555-1567.
19. 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.
20. 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 464: 932-936.
21. 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 463: 963-967.
22. 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.
23. Boulter, J. M., Schmitz, N., Sewell, A. K., Godkin, A. J., Bachmann, M. F. and Gallimore, A. M., Potent T cell agonism mediated by a very rapid TCR/pMHC interaction. Eur. J. Immunol. 2007. 37: 798-806.
24. 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.
25. 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.
26. Armstrong, K. M., Piepenbrink, K. H. and Baker, B. M., Conformational changes and flexibility in T-cell receptor recognition of peptide-MHC complexes. Biochem. J. 2008. 415: 183-196.
27. Boniface, J. J., Reich, Z., Lyons, D. S. and Davis, M. M., Thermodynamics of T cell receptor binding to peptide-MHC: evidence for a general mechanism of molecular scanning. Proc. Natl. Acad. Sci. USA 1999. 96: 11446-11451.
28. Davis-Harrison, R. L., Armstrong, K. M. and Baker, B. M., Two different T cell receptors use different thermodynamic strategies to recognize the same peptide/MHC ligand. J. Mol. Biol. 2005. 346: 533-550.
29. Ely, L. K., Beddoe, T., Clements, C. S., Matthews, J. M., Purcell, A. W., Kjer-Nielsen, L., McCluskey, J. et al., Disparate thermodynamics governing T cell receptor-MHC-I interactions implicate extrinsic factors in guiding MHC restriction. Proc. Natl. Acad. Sci. USA 2006. 103: 6641-6646.
30. 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.
31. Lee, J. K., Stewart-Jones, G., Dong, T., Harlos, K., Di Gleria, K., Dorrell, L., Douek, D. C. et al., T cell cross-reactivity and conformational changes during TCR engagement. J. Exp. Med. 2004. 200: 1455-1466.
32. Willcox, B. E., Gao, G. F., Wyer, J. R., Ladbury, J. E., Bell, J. I., Jakobsen, B. K. and van der Merwe, P. A., TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 1999. 10: 357-365.
33. Persaud, S. P., Donermeyer, D. L., Weber, K. S., Kranz, D. M. and Allen, P. M., High-affinity T cell receptor differentiates cognate peptide-MHC and altered peptide ligands with distinct kinetics and thermodynamics. Mol. Immunol. 47: 1793-1801.
34. Ding, Y. H., Smith, K. J., Garboczi, D. N., Utz, U., Biddison, W. E. and Wiley, D. C., Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 1998. 8: 403-411.
35. Dressel, A., Chin, J. L., Sette, A., Gausling, R., Hollsberg, P. and Hafler, D. A., Autoantigen recognition by human CD8 T cell clones: enhanced agonist response induced by altered peptide ligands. J. Immunol. 1997. 159: 4943-4951.
36. Goldrath, A. W. and Bevan, M. J., Low-affinity ligands for the TCR drive proliferation of mature CD8+ T cells in lymphopenic hosts. Immunity 1999. 11: 183-190.
37. Borbulevych, O. Y., Piepenbrink, K. H., Gloor, B. E., Scott, D. R., Sommese, R. F., Cole, D. K., Sewell, A. K. et al., T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility. Immunity 2009. 31: 885-896.
38. Iversen, A. K., Stewart-Jones, G., Learn, G. H., Christie, N., Sylvester-Hviid, C., Armitage, A. E., Kaul, R. et al., Conflicting selective forces affect T cell receptor contacts in an immunodominant human immunodeficiency virus epitope. Nat. Immunol. 2006. 7: 179-189.
39. Bachmann, M. F., Ohteki, T., Faienza, K. M., Zakarian, A., Kagi, D., Speiser, D. E. and Ohashi, P. S., Altered peptide ligands trigger perforin- rather than Fas-dependent cell lysis. J. Immunol. 1997. 159: 4165-4170.
40. Bachmann, M. F., Oxenius, A., Speiser, D. E., Mariathasan, S., Hengartner, H., Zinkernagel, R. M. and Ohashi, P. S., Peptide-induced T cell receptor down-regulation on naive T cells predicts agonist/partial agonist properties and strictly correlates with T cell activation. Eur. J. Immunol. 1997. 27: 2195-2203.
41. Bachmann, M. F., Speiser, D. E., Zakarian, A. and Ohashi, P. S., Inhibition of TCR triggering by a spectrum of altered peptide ligands suggests the mechanism for TCR antagonism. Eur. J. Immunol. 1998. 28: 3110-3119.
42. Martin, S., Kohler, H., Weltzien, H. U. and Leipner, C., Selective activation of CD8 T cell effector functions by epitope variants of lymphocytic choriomeningitis virus glycoprotein. J. Immunol. 1996. 157: 2358-2365.
43. Achour, A., Michaelsson, J., Harris, R. A., Ljunggren, H. G., Karre, K., Schneider, G. and Sandalova, T., Structural basis of the differential stability and receptor specificity of H-2Db in complex with murine versus human beta2-microglobulin. J. Mol. Biol. 2006. 356: 382-396.
44. Achour, A., Michaelsson, J., Harris, R. A., Odeberg, J., Grufman, P., Sandberg, J. K., Levitsky, V. et al., A structural basis for LCMV immune evasion: subversion of H-2D(b) and H-2K(b) presentation of gp33 revealed by comparative crystal structure. Analyses. Immunity 2002. 17: 757-768.
45. Tissot, A. C., Ciatto, C., Mittl, P. R., Grutter, M. G. and Pluckthun, A., Viral escape at the molecular level explained by quantitative T-cell receptor/peptide/MHC interactions and the crystal structure of a peptide/MHC complex. J. Mol. Biol. 2000. 302: 873-885.
46. Wang, B., Sharma, A., Maile, R., Saad, M., Collins, E. J. and Frelinger, J. A., Peptidic termini play a significant role in TCR recognition. J. Immunol. 2002. 169: 3137-3145.
47. Pircher, H., Moskophidis, D., Rohrer, U., Burki, K., Hengartner, H. and Zinkernagel, R. M., Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 1990. 346: 629-633.
48. Velloso, L. M., Michaelsson, J., Ljunggren, H. G., Schneider, G. and Achour, A., Determination of structural principles underlying three different modes of lymphocytic choriomeningitis virus escape from CTL recognition. J. Immunol. 2004. 172: 5504-5511.
49. Tissot, A. C., Pecorari, F. and Pluckthun, A., Characterizing the functionality of recombinant T-cell receptors in vitro: a pMHC tetramer based approach. J. Immunol. Methods 2000. 236: 147-165.
50. Holmberg, K., Mariathasan, S., Ohteki, T., Ohashi, P. S. and Gascoigne, N. R., TCR binding kinetics measured with MHC class I tetramers reveal a positive selecting peptide with relatively high affinity for TCR. J. Immunol. 2003. 171: 2427-2434.
51. van Stipdonk, M. J., 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.
52. Chen, J. L., Stewart-Jones, G., Bossi, G., Lissin, N. M., Wooldridge, L., Choi, E. M., Held, G. et al., Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J. Exp. Med. 2005. 201: 1243-1255.
53. Al-Ramadi, B. K., Jelonek, M. T., Boyd, L. F., Margulies, D. H. and Bothwell, A. L., Lack of strict correlation of functional sensitization with the apparent affinity of MHC/peptide complexes for the TCR. J. Immunol. 1995. 155: 662-673.
54. Kersh, G. J., Kersh, E. N., Fremont, D. H. and Allen, P. M., High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling. Immunity 1998. 9: 817-826.
55. Pinilla-Ibarz, J., May, R. J., Korontsvit, T., Gomez, M., Kappel, B., Zakhaleva, V., Zhang, R. H. et al., Improved human T-cell responses against synthetic HLA-0201 analog peptides derived from the WT1 oncoprotein. Leukemia 2006. 20: 2025-2033.
56. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J. and Carbone, F. R., T cell receptor antagonist peptides induce positive selection. Cell 1994. 76: 17-27.
57. Colbert, R. A., Rowland-Jones, S. L., McMichael, A. J. and Frelinger, J. A., Differences in peptide presentation between B27 subtypes: the importance of the P1 side chain in maintaining high affinity peptide binding to B 2703. Immunity 1994. 1: 121-130.
58. Scott, D. R., Borbulevych, O. Y., Piepenbrink, K. H., Corcelli, S. A. and Baker, B. M., Disparate degrees of hypervariable loop flexibility control T-cell receptor cross-reactivity, specificity, and binding mechanism. J. Mol. Biol. 2011. 414: 385-400.
59. Jones, L. L., Colf, L. A., Stone, J. D., Garcia, K. C. and Kranz, D. M., Distinct CDR3 conformations in TCRs determine the level of cross-reactivity for diverse antigens, but not the docking orientation. J. Immunol. 2008. 181: 6255-6264.
60. Reiser, J. B., Darnault, C., Guimezanes, A., Gregoire, C., Mosser, T., Schmitt-Verhulst, A. M., Fontecilla-Camps, J. C. et al., Crystal structure of a T cell receptor bound to an allogeneic MHC molecule. Nat. Immunol. 2000. 1: 291-297.
61. Anikeeva, N., Lebedeva, T., Krogsgaard, M., Tetin, S. Y., Martinez-Hackert, E., Kalams, S. A., Davis, M. M. et al., Distinct molecular mechanisms account for the specificity of two different T-cell receptors. Biochemistry 2003. 42: 4709-4716.
62. Huseby, E. S., Crawford, F., White, J., Marrack, P. and Kappler, J. W., Interface-disrupting amino acids establish specificity between T cell receptors and complexes of major histocompatibility complex and peptide. Nat. Immunol. 2006. 7: 1191-1199.
63. Achour, A., Harris, R. A., Persson, K., Sundback, J., Sentman, C. L., Schneider, G., Lindqvist, Y. et al., Murine class I major histocompatibility complex H-2Dd: expression, refolding and crystallization. Acta Crystallogr. D Biol. Crystallogr. 1999. 55: 260-262.
64. Sandalova, T., Michaelsson, J., Harris, R. A., Ljunggren, H. G., Karre, K., Schneider, G. and Achour, A., Expression, refolding and crystallization of murine MHC class I H-2Db in complex with human beta2-microglobulin. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2005. 61: 1090-1093.
65. Sandalova, T., Michaelsson, J., Harris, R. A., Odeberg, J., Schneider, G., Karre, K. and Achour, A., A structural basis for CD8+ T cell-dependent recognition of non-homologous peptide ligands: implications for molecular mimicry in autoreactivity. J. Biol. Chem. 2005. 280: 27069-27075.
66. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R. and Leslie, A. G., iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta. Crystallogr. D. Biol. Crystallogr. 2011. 67: 271-281.
67. Evans, P., Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 2006. 62: 72-82.
68. 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.
69. 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.
70. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 2010. 66: 486-501.