Interface-disrupting amino acids establish specificity between T cell receptors and complexes of major histocompatibility complex and peptide

Nature Immunology

Volumn 7, Issue 11, 2006, Pages 1191-1199

  Huseby, Eric S ^a   Crawford, Frances ^a   White, Janice ^a   Marrack, Philippa ^a,b   Kappler, John W ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CELL SELECTION; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; THYMOCYTE;

AMINO ACIDS; ANIMALS; BINDING SITES; CELL LINE; H-2 ANTIGENS; MICE; MICE, INBRED C57BL; PEPTIDES; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; SPODOPTERA;

EID: 33750113432     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1401     Document Type: Article

References (50)

1. Davis, M.M. & Bjorkman, P.J. T-cell antigen receptor genes and T-cell recognition. Nature 334, 395-402 (1988).
2. Kappler, J.W., Roehm, N. & Marrack, P. T cell tolerance by clonal elimination in the thymus. Cell 49, 273-280 (1987).
3. Sprent, J., Lo, D., Gao, E.K. & Ron, Y. T cell selection in the thymus. Immunol. Rev. 101, 173-190 (1988).
4. Mathis, D. & Benoist, C. Back to central tolerance. Immunity 20, 509-516 (2004).
5. Palmer, E. Negative selection-clearing out the bad apples from the T-cell repertoire. Nat. Rev. Immunol. 3, 383-391 (2003).
6. Starr, T.K., Jameson, S.C. & Hogquist, K.A. Positive and negative selection of T cells. Annu. Rev. Immunol. 21, 139-176 (2003).
7. vonBoehmer, H. et al. Thymic selection revisited: How essential is it? Immunol. Rev. 191, 62-78 (2003).
8. Wilson, D.B. & Nowell, P.C. Quantitative studies on the mixed lymphocyte interaction in rats. IV. Immunologic potentiality of the responding cells. J. Exp. Med. 131, 391-407 (1970).
9. Suchin, E.J. et al. Quantifying the frequency of alloreactive T cells in vivo: New answers to an old question. J. Immunol. 166, 973-981 (2001).
10. Yeh, E.T., Benacerraf, B. & Rock, K.L. Analysis of thymocyte MHC specificity with thymocyte hybridomas. J. Exp. Med. 160, 799-813 (1984).
11. Merkenschlager, M. et al. How many thymocytes audition for selection? J. Exp. Med. 186, 1149-1158 (1997).
12. Zerrahn, J., Held, W. & Raulet, D.H. The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 88, 627-636 (1997).
13. + T cells mature in the absence of MHC class I and class II expression in Ly-6A.2 transgenic mice. J. Immunol. 161, 175-182 (1998).
14. Bevan, M.J. In a radiation chimaera, host H-2 antigens determine immune responsiveness of donor cytotoxic cells. Nature 269, 417-418 (1977).
15. Berg, L.J. et al. Antigen/MHC-specific T cells are preferentially exported from the thymus in the presence of their MHC ligand. Cell 58, 1035-1046 (1989).
16. Scott, B., Bluthmann, H., Teh, H.S. & von Boehmer, H. The generation of mature T cells requires interaction of the αβ T-cell receptor with major histocompatibility antigens. Nature 338, 591-593 (1989).
17. + T cells in the thymus. Cell 73, 1041-1049 (1993).
18. + T cells induced by major histocompatibility complex binding peptides in fetal thymic organ culture. J. Exp. Med. 177, 1469-1473 (1993).
19. Huseby, E.S. et al. How the T cell repertoire becomes peptide and MHC specific. Cell 122, 247-260 (2005).
20. Ignatowicz, L., Kappler, J. & Marrack, P. The repertoire of T cells shaped by a single MHC/peptide ligand. Cell 84, 521-529 (1996).
21. Fung-Leung, W.P. et al. Antigen presentation and T cell development in H2-M-deficient mice. Science 271, 1278-1281 (1996).
22. Martin, W.D. et al. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection. Cell 84, 543-550 (1996).
23. Miyazaki, T. et al. Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway. Cell 84, 531-541 (1996).
24. Clackson, T. & Wells, J.A. A hot spot of binding energy in a hormone-receptor interface. Science 267, 383-386 (1995).
25. DeLano, W.L. Unraveling hot spots in binding interfaces: Progress and challenges. Curr. Opin. Struct. Biol. 12, 14-20 (2002).
26. Crawford, F., Huseby, E., White, J., Marrack, P. & Kappler, J. Mimotopes for alloreactive and conventional T cells in a peptide-MHC display library. PLOS Biol. 2, E90 (2004).
27. Crawford, F., Kozono, H., White, J., Marrack, P. & Kappler, J. Detection of antigenspecific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity 8, 675-682 (1998).
28. Savage, P.A., Boniface, J.J. & Davis, M.M. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10, 485-492 (1999).
29. Liu, X. et al. Alternate interactions define the binding of peptides to the MHC molecule IA(b). Proc. Natl. Acad. Sci. USA 99, 8820-8825 (2002).
30. Jorgensen, J.L., Reay, P.A., Ehrich, E.W. & Davis, M.M. Molecular components of T-cell recognition. Annu. Rev. Immunol. 10, 835-873 (1992).
31. Boehncke, W.H. et al. The importance of dominant negative effects of amino acid side chain substitution in peptide-MHC molecule interactions and T cell recognition. J. Immunol. 150, 331-341 (1993).
32. Alam, S.M. et al. T-cell-receptor affinity and thymocyte positive selection. Nature 381, 616-620 (1996).
33. Lyons, D.S. et al. A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity 5, 53-61 (1996).
34. Sloan-Lancaster, J. & Allen, P.M. Altered peptide ligand-induced partial T cell activation: Molecular mechanisms and role in T cell biology. Annu. Rev. Immunol. 14, 1-27 (1996).
35. Zinkernagel, R.M. & Doherty, P.C. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248, 701-702 (1974).
36. Huseby, E.S., Crawford, F., White, J., Kappler, J. & Marrack, P. Negative selection imparts peptide specificity to the mature T cell repertoire. Proc. Natl. Acad. Sci. USA 100, 11565-11570 (2003).
37. Bhat, T.N. et al. Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc. Natl. Acad. Sci. USA 91, 1089-1093 (1994).
38. Garboczi, D.N. & Biddison, W.E. Shapes of MHC restriction. Immunity 10, 1-7 (1999).
39. Garcia, K.C., Teyton, L. & Wilson, I.A. Structural basis of T cell recognition. Annu. Rev. Immunol. 17, 369-397 (1999).
40. Manning, T.C. et al. Alanine scanning mutagenesis of an αβ T cell receptor: Mapping the energy of antigen recognition. Immunity 8, 413-425 (1998).
41. Baker, B.M., Turner, R.V., Gagnon, S.J., Wiley, D.C. & Biddison, W.E. Identification of a crucial energetic footprint on the α1 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 (2001).
42. Wu, L.C., Tuot, D.S., Lyons, D.S., Garcia, K.C. & Davis, M.M. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 418, 552-556 (2002).
43. Borg, N.A. et al. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nat. Immunol. 6, 171-180 (2005).
44. Davis, M.M. et al. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16, 523-544 (1998).
45. Rudolph, M.G., Luz, J.G. & Wilson, I.A. Structural and thermodynamic correlates of T cell signaling. Annu. Rev. Biophys. Biomol. Struct. 31, 121-149 (2002).
46. Cunningham, B.C. & Wells, J.A. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244, 1081-1085 (1989).
47. Cunningham, B.C., Jhurani, P., Ng, P. & Wells, J.A. Receptor and antibody epitopes in human growth hormone identified by homolog-scanning mutagenesis. Science 243, 1330-1336 (1989).
48. Mason, D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today 19, 395-404 (1998).
49. Gagnon, S.J. et al. 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 (2005).
50. McFarland, B.J., Kortemme, T., Yu, S.F., Baker, D. & Strong, R.K. Symmetry recognizing asymmetry: Analysis of the interactions between the C-type lectin-like immunoreceptor NKG2D and MHC class I-like ligands. Structure 11, 411-422 (2003).