A structural basis for varied αβ TCR usage against an immunodominant EBV antigen restricted to a HLA-B8 molecule

Journal of Immunology

Volumn 188, Issue 1, 2012, Pages 311-321

  Gras, Stephanie ^a   Wilmann, Pascal G ^a   Chen, Zhenjun ^b   Halim, Hanim ^a   Liu, Yu Chih ^a   Kjer Nielsen, Lars ^b   Purcell, Anthony W ^c   Burrows, Scott R ^d   McCluskey, James ^b   Rossjohn, Jamie ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN; HLA B8 ANTIGEN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; IMMUNOLOGICAL TOLERANCE; MOLECULAR DOCKING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ADAPTIVE IMMUNITY; ANTIGENS, VIRAL; CELL LINE; CRYSTALLOGRAPHY, X-RAY; HERPESVIRUS 4, HUMAN; HLA-B8 ANTIGEN; HUMANS; PEPTIDES; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS;

EID: 84855367088     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102686     Document Type: Article

References (54)

1. Rickinson, A. B., and D. J. Moss. 1997. Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu. Rev. Immunol. 15: 405-431. (Pubitemid 27169287)
2. Long, H. M., G. S. Taylor, and A. B. Rickinson. 2011. Immune defence against EBV and EBV-associated disease. Curr. Opin. Immunol. 23: 258-264.
3. Theodossis, A., C. Guillonneau, A. Welland, L. K. Ely, C. S. Clements, N. A. Williamson, A. I. Webb, J. A. Wilce, R. J. Mulder, M. A. Dunstone, et al. 2010. Constraints within major histocompatibility complex class I restricted peptides: presentation and consequences for T-cell recognition. Proc. Natl. Acad. Sci. USA 107: 5534-5539.
4. Miles, J. J., N. A. Borg, R. M. Brennan, F. E. Tynan, L. Kjer-Nielsen, S. L. Silins, M. J. Bell, J. M. Burrows, J. McCluskey, J. Rossjohn, and S. R. Burrows. 2006. TCR alpha genes direct MHC restriction in the potent human T cell response to a class I-bound viral epitope. J. Immunol. 177: 6804-6814. (Pubitemid 44715045)
5. Archbold, J. K., W. A. Macdonald, S. Gras, L. K. Ely, J. J. Miles, M. J. Bell, R. M. Brennan, T. Beddoe, M. C. Wilce, C. S. Clements, et al. 2009. Natural micropolymorphism in human leukocyte antigens provides a basis for genetic control of antigen recognition. J. Exp. Med. 206: 209-219.
6. Tynan, F. E., N. A. Borg, J. J. Miles, T. Beddoe, D. El-Hassen, S. L. Silins, W. J. van Zuylen, A.W. Purcell, L. Kjer-Nielsen, J. McCluskey, et al. 2005. High resolution structures of highly bulged viral epitopes bound to major histocompatibility complex class I. Implications for T-cell receptor engagement and T-cell immunodominance. J. Biol. Chem. 280: 23900-23909. (Pubitemid 40884878)
7. 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.
8. Luz, J. G., M. Huang, K. C. Garcia, M. G. Rudolph, V. Apostolopoulos, L. Teyton, and I. A. Wilson. 2002. Structural comparison of allogeneic and syngeneic T cell receptor-peptide-major histocompatibility complex complexes: a buried alloreactive mutation subtly alters peptide presentation substantially increasing V(beta) Interactions. J. Exp. Med. 195: 1175-1186. (Pubitemid 34517143)
9. Turner, S. J., P. C. Doherty, J. McCluskey, and J. Rossjohn. 2006. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6: 883-894. (Pubitemid 44851731)
10. Borg, N. A., L. K. Ely, T. Beddoe, W. A. Macdonald, H. H. Reid, C. S. Clements, A. W. Purcell, L. Kjer-Nielsen, J. J. Miles, S. R. Burrows, et al. 2005. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape'of peptide-MHC recognition. Nat. Immunol. 6: 171-180. (Pubitemid 40268198)
11. Kjer-Nielsen, L., C. S. Clements, A. G. Brooks, A. W. Purcell, M. R. Fontes, J. McCluskey, and J. Rossjohn. 2002. The structure of HLA-B8 complexed to an immunodominant viral determinant: peptide-induced conformational changes and a mode of MHC class I dimerization. J. Immunol. 169: 5153-5160. (Pubitemid 35217185)
12. Kjer-Nielsen, L., C. S. Clements, A. W. Purcell, A. G. Brooks, J. C. Whisstock, S. R. Burrows, J. McCluskey, and J. Rossjohn. 2003. A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 18: 53-64. (Pubitemid 36120687)
13. Burrows, S. R., S. L. Silins, D. J. Moss, R. Khanna, I. S. Misko, and V. P. Argaet. 1995. T cell receptor repertoire for a viral epitope in humans is diversified by tolerance to a background major histocompatibility complex antigen. J. Exp. Med. 182: 1703-1715.
14. Burrows, S. R., S. L. Silins, S. M. Cross, C. A. Peh, M. Rischmueller, J. M. Burrows, S. L. Elliott, and J. McCluskey. 1997. Human leukocyte antigen phenotype imposes complex constraints on the antigen-specific cytotoxic T lymphocyte repertoire. Eur. J. Immunol. 27: 178-182. (Pubitemid 27046075)
15. Burrows, S. R., R. Khanna, J. M. Burrows, and D. J. Moss. 1994. An alloresponse in humans is dominated by cytotoxic T lymphocytes (CTL) cross-reactive with a single Epstein-Barr virus CTL epitope: implications for graft-versus-host disease. J. Exp. Med. 179: 1155-1161. (Pubitemid 24091774)
16. Gras, S., S. R. Burrows, L. Kjer-Nielsen, C. S. Clements, Y. C. Liu, L. C. Sullivan, M. J. Bell, A. G. Brooks, A. W. Purcell, J. McCluskey, and J. Rossjohn. 2009. The shaping of T cell receptor recognition by self-tolerance. Immunity 30: 193-203.
17. Clements, C. S., L. Kjer-Nielsen, A. G. Brooks, A.W. Purcell, J. McCluskey, and J. Rossjohn. 2002. The production, purification and crystallization of a soluble, heterodimeric form of a highly selected T-cell receptor in its unliganded and liganded state. Acta Crystallogr. D Biol. Crystallogr. 58: 2131-2134. (Pubitemid 35450840)
18. Reid, S. W., S. McAdam, K. J. Smith, P. Klenerman, C. A. O'Callaghan, K. Harlos, B. K. Jakobsen, A. J. McMichael, J. I. Bell, D. I. Stuart, and E. Y. Jones. 1996. Antagonist HIV-1 Gag peptides induce structural changes in HLA B8. J. Exp. Med. 184: 2279-2286. (Pubitemid 27023728)
19. Clements, C. S., L. Kjer-Nielsen, W. A. MacDonald, A. G. Brooks, A. W. Purcell, J. McCluskey, and J. Rossjohn. 2002. The production, purification and crystallization of a soluble heterodimeric form of a highly selected T-cell receptor in its unliganded and liganded state. Acta Crystallogr. D Biol. Crystallogr. 58: 2131-2134. (Pubitemid 35450840)
20. Kabsch, W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26: 795-800.
21. Read, R. J. 2001. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57: 1373-1382. (Pubitemid 36117185)
22. Kjer-Nielsen, L., C. S. Clements, A. G. Brooks, A.W. Purcell, J. McCluskey, and J. Rossjohn. 2002. The 1.5 A crystal structure of a highly selected antiviral T cell receptor provides evidence for a structural basis of immunodominance. Structure 10: 1521-1532. (Pubitemid 35351492)
23. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132. (Pubitemid 41742764)
24. Adams, P. D., R. W. Grosse-Kunstleve, L. W. Hung, T. R. Ioerger, A. J. McCoy, N. W. Moriarty, R. J. Read, J. C. Sacchettini, N. K. Sauter, and T. C. Terwilliger. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58: 1948-1954. (Pubitemid 35337293)
25. Lefranc, M.-P., V. Giudicelli, Q. Kaas, E. Duprat, J. Jabado-Michaloud, D. Scaviner, C. Ginestoux, O. Clément, D. Chaume, and G. Lefranc. 2005. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 33(Database issue): D593-D597. (Pubitemid 40207943)
26. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
27. Lefranc, M. P., V. Giudicelli, C. Ginestoux, J. Jabado-Michaloud, G. Folch, F. Bellahcene, Y. Wu, E. Gemrot, X. Brochet, J. Lane, et al. 2009. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 37(Database issue): D1006-D1012.
28. Callan, M. F., N. Annels, N. Steven, L. Tan, J. Wilson, A. J. McMichael, and A. B. Rickinson. 1998. T cell selection during the evolution of CD8+ T cell memory in vivo. Eur. J. Immunol. 28: 4382-4390. (Pubitemid 28558669)
29. Argaet, V. P., C. W. Schmidt, S. R. Burrows, S. L. Silins, M. G. Kurilla, D. L. Doolan, A. Suhrbier, D. J. Moss, E. Kieff, T. B. Sculley, and I. S. Misko. 1994. Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus. J. Exp. Med. 180: 2335-2340. (Pubitemid 24351615)
30. Zerrahn, J., W. Held, and D. H. Raulet. 1997. The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 88: 627-636. (Pubitemid 27152405)
31. Jameson, S. C., J. Kaye, and N. R. Gascoigne. 1990. A T cell receptor V alpha region selectively expressed in CD4+ cells. J. Immunol. 145: 1324-1331. (Pubitemid 20255033)
32. Sim, B. C., L. Zerva, M. I. Greene, and N. R. J. Gascoigne. 1996. Control of MHC restriction by TCR Valpha CDR1 and CDR2. Science 273: 963-966. (Pubitemid 26275174)
33. Sim, B. C., N. Aftahi, C. Reilly, B. Bogen, R. H. Schwartz, N. R. Gascoigne, and D. Lo. 1998. Thymic skewing of the CD4/CD8 ratio maps with the T-cell receptor alpha-chain locus. Curr. Biol. 8: 701-704. (Pubitemid 28286277)
34. Manning, T. C., E. A. Parke, L. Teyton, and D. M. Kranz. 1999. Effects of complementarity determining region mutations on the affinity of an alpha/beta T cell receptor: measuring the energy associated with CD4/CD8 repertoire skewing. J. Exp. Med. 189: 461-470. (Pubitemid 29187368)
35. Feng, D., C. J. Bond, L. K. Ely, J. Maynard, and K. C. Garcia. 2007. Structural evidence for a germline-encoded T cell receptor-major histocompatibility complex interaction 'codon'. Nat. Immunol. 8: 975-983. (Pubitemid 47300012)
36. Dai, S., E. S. Huseby, K. Rubtsova, J. Scott-Browne, F. Crawford, W. A. Macdonald, P. Marrack, and J. W. Kappler. 2008. Crossreactive T Cells spotlight the germline rules for alphabeta T cell-receptor interactions with MHC molecules. Immunity 28: 324-334.
37. Scott-Browne, J. P., J. White, J. W. Kappler, L. Gapin, and P. Marrack. 2009. Germline-encoded amino acids in the alphabeta T-cell receptor control thymic selection. Nature 458: 1043-1046.
38. Marrack, P., J. P. Scott-Browne, S. Dai, L. Gapin, and J. W. Kappler. 2008. Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu. Rev. Immunol. 26: 171-203. (Pubitemid 351600374)
39. Burrows, S. R., Z. Chen, J. K. Archbold, F. E. Tynan, T. Beddoe, L. Kjer-Nielsen, J. J. Miles, R. Khanna, D. J. Moss, Y. C. Liu, et al. 2010. Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Proc. Natl. Acad. Sci. USA 107: 10608-10613.
40. Godfrey, D. I., J. Rossjohn, and J. McCluskey. 2008. The fidelity, occasional promiscuity, and versatility of T cell receptor recognition. Immunity 28: 304-314. (Pubitemid 351343861)
41. Wu, L. C., D. S. Tuot, D. S. Lyons, K. C. Garcia, and M. M. Davis. 2002. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 418: 552-556. (Pubitemid 34851403)
42. Colf, L. A., A. J. Bankovich, N. A. Hanick, N. A. Bowerman, L. L. Jones, D. M. Kranz, and K. C. Garcia. 2007. How a single T cell receptor recognizes both self and foreign MHC. Cell 129: 135-146. (Pubitemid 46507586)
43. 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. (Pubitemid 41541789)
44. Ding, Y. H., B. M. Baker, D. N. Garboczi, W. E. Biddison, and D. C. Wiley. 1999. Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 11: 45-56.
45. Gras, S., Z. Chen, J. J. Miles, Y. C. Liu, M. J. Bell, L. C. Sullivan, L. Kjer-Nielsen, R. M. Brennan, J. M. Burrows, M. A. Neller, et al. 2010. Allelic polymorphism in the T cell receptor and its impact on immune responses. J. Exp. Med. 207: 1555-1567.
46. Archbold, J. K., W. A. Macdonald, J. J. Miles, R. M. Brennan, L. Kjer-Nielsen, J. McCluskey, S. R. Burrows, and J. Rossjohn. 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. (Pubitemid 46036640)
47. Baker, B. M., R. V. Turner, S. J. Gagnon, D. C. Wiley, and W. E. Biddison. 2001. 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. 193: 551-562. (Pubitemid 32539552)
48. Manning, T. C., C. J. Schlueter, T. C. Brodnicki, E. A. Parke, J. A. Speir, K. C. Garcia, L. Teyton, I. A. Wilson, and D. M. Kranz. 1998. Alanine scanning mutagenesis of an alphabeta T cell receptor: mapping the energy of antigen recognition. Immunity 8: 413-425. (Pubitemid 28196796)
49. Sethi, D. K., D. A. Schubert, A.-K. Anders, A. Heroux, D. A. Bonsor, C. P. Thomas, E. J. Sundberg, J. Pyrdol, and K. W. Wucherpfennig. 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.
50. Ishizuka, J., G. B. Stewart-Jones, A. van der Merwe, J. I. Bell, A. J. McMichael, and E. Y. Jones. 2008. The structural dynamics and energetics of an immunodominant T cell receptor are programmed by its Vbeta domain. Immunity 28: 171-182. (Pubitemid 351215238)
51. Gagnon, S. J., O. Y. Borbulevych, R. L. Davis-Harrison, T. K. Baxter, J. R. Clemens, K. M. Armstrong, R. V. Turner, M. Damirjian, W. E. Biddison, and B. M. Baker. 2005. Unraveling a hotspot for TCR recognition on HLA-A2: evidence against the existence of peptide-independent TCR binding determinants. J. Mol. Biol. 353: 556-573. (Pubitemid 41417737)
52. Gras, S., L. Kjer-Nielsen, S. R. Burrows, J. McCluskey, and J. Rossjohn. 2008. T-cell receptor bias and immunity. Curr. Opin. Immunol. 20: 119-125.
53. 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. (Pubitemid 41668738)
54. Beddoe, T., Z. Chen, C. S. Clements, L. K. Ely, S. R. Bushell, J. P. Vivian, L. Kjer-Nielsen, S. S. Pang, M. A. Dunstone, Y. C. Liu, et al. 2009. Antigen ligation triggers a conformational change within the constant domain of the alphabeta T cell receptor. Immunity 30: 777-788.