Structural bases for the affinity-driven selection of a public TCR against a dominant human cytomegalovirus epitope

Journal of Immunology

Volumn 183, Issue 1, 2009, Pages 430-437

  Gras, Stéphanie ^a,d   Saulquin, Xavier ^b   Reiser, Jean Baptiste ^a   Debeaupuis, Emilie ^b   Echasserieau, Klara ^b   Kissenpfennig, Adrien ^c,e   Legoux, François ^b   Chouquet, Anne ^a   Le Gorrec, Madalen ^a   Machillot, Paul ^a   Neveu, Bérangère ^b   Thielens, Nicole ^a   Malissen, Bernard ^c   Bonneville, Marc ^b   Housset, Dominique ^a  

^a CEA GRENOBLE   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d MONASH UNIVERSITY   (Australia)

^e QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOMEGALOVIRUS MATRIX PROTEIN 65KDA; EPITOPE; HLA A ANTIGEN; HLA A*0201 ANTIGEN; HLA-A*0201 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; MATRIX PROTEIN; PEPTIDE; PHOSPHOPROTEIN;

ARTICLE; CELL CLONE; CHEMISTRY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PROTEIN BINDING; PROTEIN MOTIF; VIRUS ACTIVATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; CLONE CELLS; CRYSTALLOGRAPHY, X-RAY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; EPITOPES, T-LYMPHOCYTE; HLA-A ANTIGENS; HUMANS; IMMUNODOMINANT EPITOPES; LYMPHOCYTE ACTIVATION; PEPTIDES; PHOSPHOPROTEINS; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; VIRAL MATRIX PROTEINS; VIRUS ACTIVATION;

EID: 68949108186     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900556     Document Type: Article

References (41)

1. Sissons, J. G., M. Bain, and M. R. Wills. 2002. Latency and reactivation of human cytomegalovirus. J. Infect. 44: 73-77.
2. Borysiewicz, L. K., J. K. Hickling, S. Graham, J. Sinclair, M. P. Cranage, G. L. Smith, and J. G. Sissons. 1988. Human cytomegalovirus-specific cytotoxic T cells: relative frequency of stage-specific CTL recognizing the 72-kD immediate early protein and glycoprotein B expressed by recombinant vaccinia viruses. J. Exp. Med. 168: 919-931.
3. Quinnan, G. V., Jr., W. H. Burns, N. Kirmani, A. H. Rook, J. Manischewitz, L. Jackson, G. W. Santos, and R. Saral. 1984. HLA-restricted cytotoxic T lymphocytes are an early immune response and important defense mechanism in cytomegalovirus infections. Rev. Infect. Dis. 6: 156-163.
4. McLaughlin-Taylor, E., H. Pande, S. J. Forman, B. Tanamachi, C. R. Li, J. A. Zaia, P. D. Greenberg, and S. R. Riddell. 1994. Identification of the major late human cytomegalovirus matrix protein pp65 as a target antigen for CD8+ virus-specific cytotoxic T lymphocytes. J. Med. Virol. 43: 103-110. (Pubitemid 24146353)
5. Wills, M. R., A. J. Carmichael, K. Mynard, X. Jin, M. P. Weekes, B. Plachter, and J. G. Sissons. 1996. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J. Virol. 70: 7569-7579.
6. Saulquin, X., C. Ibisch, M. A. Peyrat, E. Scotet, M. Hourmant, H. Vie, M. Bonneville, and E. Houssaint. 2000. A global appraisal of immunodominant CD8 T cell responses to Epstein-Barr virus and cytomegalovirus by bulk screening. Eur. J. Immunol. 30: 2531-2539.
7. Kern, F., I. P. Surel, N. Faulhaber, C. Frommel, J. Schneider-Mergener, C. Schonemann, P. Reinke, and H. D. Volk. 1999. Target structures of the CD8(+)-T-cell response to human cytomegalovirus: the 72-kilodalton major immediate-early protein revisited. J. Virol. 73: 8179-8184. (Pubitemid 29441679)
8. Khan, N., M. Cobbold, R. Keenan, and P. A. Moss. 2002. Comparative analysis of CD8+ T cell responses against human cytomegalovirus proteins pp65 and immediate early 1 shows similarities in precursor frequency, oligoclonality, and phenotype. J. Infect. Dis. 185: 1025-1034.
9. Engstrand, M., C. Tournay, M. A. Peyrat, B. M. Eriksson, J. Wadstrom, B. Z. Wirgart, F. Romagne, M. Bonneville, T. H. Totterman, and O. Korsgren. 2000. Characterization of CMVpp65-specific CD8+ T lymphocytes using MHC tetramers in kidney transplant patients and healthy participants. Transplantation 69: 2243-2250.
10. Diamond, D. J., J. York, J. Y. Sun, C. L. Wright, and S. J. Forman. 1997. Development of a candidate HLA A*0201 restricted peptide-based vaccine against human cytomegalovirus infection. Blood 90: 1751-1767.
11. Peggs, K., S. Verfuerth, A. Pizzey, J. Ainsworth, P. Moss, and S. Mackinnon. 2002. Characterization of human cytomegalovirus peptide-specific CD8(+) T-cell repertoire diversity following in vitro restimulation by antigen-pulsed dendritic cells. Blood 99: 213-223.
12. Weekes, M. P., M. R. Wills, K. Mynard, A. J. Carmichael, and J. G. Sissons. 1999. The memory cytotoxic T-lymphocyte (CTL) response to human cytomegalovirus infection contains individual peptide-specific CTL clones that have undergone extensive expansion in vivo. J. Virol. 73: 2099-2108.
13. Trautmann, L., M. Rimbert, K. Echasserieau, X. Saulquin, B. Neveu, J. Dechanet, V. Cerundolo, and M. Bonneville. 2005. Selection of T cell clones expressing high-affinity public TCRs within human cytomegalovirus-specific CD8 T cell responses. J. Immunol. 175: 6123-6132.
14. Stewart-Jones, G. B., A. J. McMichael, J. I. Bell, D. I. Stuart, and E. Y. Jones. 2003. A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 4: 657-663.
15. 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 αβ T cell receptors in antiviral immunity. Immunity 18: 53-64.
16. Garboczi, D. N., D. T. Hung, and D. C. Wiley. 1992. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc. Natl. Acad. Sci. USA 89: 3429-3433.
17. Bodinier, M., M. A. Peyrat, C. Tournay, F. Davodeau, F. Romagne, M. Bonneville, and F. Lang. 2000. Efficient detection and immunomagnetic sorting of specific T cells using multimers of MHC class I and peptide with reduced CD8 binding. Nat. Med. 6: 707-710.
18. Neveu, B., K. Echasserieau, T. Hill, K. Kuus-Reichel, E. Houssaint, M. Bonneville, and X. Saulquin. 2006. Impact of CD8-MHC class I interaction in detection and sorting efficiencies of antigen-specific T cells using MHC class I/peptide multimers: contribution of pMHC valency. Int. Immunol. 18: 1139-1145.
19. Kabsch, W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26: 795-800.
20. Navaza, J. 1994. AMoRe: an automated package for molecular replacement. Acta Crystallogr. A. 50: 157-163.
21. Hillig, R. C., P. G. Coulie, V. Stroobant, W. Saenger, A. Ziegler, and M. Hulsmeyer. 2001. High-resolution structure of HLA-A*0201 in complex with a tumour-specific antigenic peptide encoded by the MAGE-A4 gene. J. Mol. Biol. 310: 1167-1176.
22. 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.
23. Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D. 50: 760-763.
24. Jones, T. A., J. Y. Zou, S. W. Cowan, and Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47: 110-119.
25. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D. 60: 2126-2132.
26. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanovic. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
27. Lefranc, M. P. 2001. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 29: 207-209.
28. Rudolph, M. G., R. L. Stanfield, and I. A. Wilson. 2006. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24: 419-466.
29. 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.
30. 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.
31. Gakamsky, D. M., E. Lewitzki, E. Grell, X. Saulquin, B. Malissen, F. Montero-Julian, M. Bonneville, and I. Pecht. 2007. Kinetic evidence for a ligand-binding-induced conformational transition in the T cell receptor. Proc. Natl. Acad. Sci. USA 104: 16639-16644.
32. Venturi, V., D. A. Price, D. C. Douek, and M. P. Davenport. 2008. The molecular basis for public T-cell responses? Nat. Rev. Immunol. 8: 231-238.
33. 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.
34. 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.
35. Hennecke, J., A. Carfi, and D. C. Wiley. 2000. Structure of a covalently stabilized complex of a human αβ T-cell receptor, influenza HA peptide and MHC class II molecule, HLA-DR1. EMBO J. 19: 5611-5624.
36. Lehner, P. J., E. C. Wang, P. A. Moss, S. Williams, K. Platt, S. M. Friedman, J. I. Bell, and L. K. Borysiewicz. 1995. Human HLA-A0201-restricted cytotoxic T lymphocyte recognition of influenza A is dominated by T cells bearing the V β 17 gene segment. J. Exp. Med. 181: 79-91.
37. Moss, P. A., R. J. Moots, W. M. Rosenberg, S. J. Rowland-Jones, H. C. Bodmer, A. J. McMichael, and J. I. Bell. 1991. Extensive conservation of α and β chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. USA 88: 8987-8990.
38. 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.
39. 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.
40. 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.
41. 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.