How a Single T Cell Receptor Recognizes Both Self and Foreign MHC

Cell

Volumn 129, Issue 1, 2007, Pages 135-146

  Colf, Leremy A ^a   Bankovich, Alexander J ^a   Hanick, Nicole A ^a   Bowerman, Natalie A ^b   Jones, Lindsay L ^b   Kranz, David M ^b   Garcia, K Christopher ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; BINDING PROTEIN; GLUTAMINYLLEUCYLSERYLPROLYLPHENYLALANYLPROLYLPHENYLALANYLASPARTYLLEUCINE; GLUTAMYLGLUTAMINYLTYROSYLLYSYLPHENYLALANYLTYROSYLSERYLVALINE; H2 ANTIGEN; LEUCINE; LYSINE; MAJOR HISTOCOMPATIBILITY ANTIGEN; PEPTIDE; PEPTIDE FRAGMENT; PROTEIN CDR3ALPHA; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CONTROLLED STUDY; CROSS REACTION; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN VARIANT; RECEPTOR BINDING;

EID: 33947726614     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.01.048     Document Type: Article

References (63)

1. Anikeeva N., Lebedeva T., Krogsgaard M., Tetin S.Y., Martinez-Hackert E., Kalams S.A., Davis M.M., and Sykulev Y. Distinct molecular mechanisms account for the specificity of two different T-cell receptors. Biochemistry 42 (2003) 4709-4716
2. Archbold J.K., Macdonald W.A., Miles J.J., Brennan R.M., Kjer-Nielsen L., McCluskey J., Burrows S.R., and Rossjohn J. Alloreactivity between disparate cognate and allogeneic pMHC-I complexes is resultant of highly focused, peptide-dependent structural mimicry. J. Biol. Chem. 281 (2006) 34324-34332
3. Balendiran G.K., Solheim J.C., Young A.C., Hansen T.H., Nathenson S.G., and Sacchettini J.C. The three-dimensional structure of an H-2Ld-peptide complex explains the unique interaction of Ld with beta-2 microglobulin and peptide. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 6880-6885
4. Bevan M.J. High determinant density may explain the phenomenon of alloreactivity. Immunol. Today 5 (1984) 128
5. Borg N.A., Ely L.K., Beddoe T., Macdonald W.A., Reid H.H., Clements C.S., Purcell A.W., Kjer-Nielsen L., Miles J.J., Burrows S.R., et al. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nat. Immunol. 6 (2005) 171-180
6. Boulanger M.J., Bankovich A.J., Kortemme T., Baker D., and Garcia K.C. Convergent mechanisms for recognition of divergent cytokines by the shared signaling receptor gp130. Mol. Cell 12 (2003) 577-589
7. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
8. Buslepp J., Wang H., Biddison W.E., Appella E., and Collins E.J. A correlation between TCR Valpha docking on MHC and CD8 dependence: implications for T cell selection. Immunity 19 (2003) 595-606
9. Chen J., Eisen H.N., and Kranz D.M. A model T-cell receptor system for studying memory T-cell development. Microbes Infect. 5 (2003) 233-240
10. - strains. Proc. Natl. Acad. Sci. USA 91 (1994) 11482-11486
11. Daniel C., Horvath S., and Allen P.M. A basis for alloreactivity: MHC helical residues broaden peptide recognition by the TCR. Immunity 8 (1998) 543-552
12. Davis M.M., and Bjorkman P.J. T-cell antigen receptor genes and T-cell recognition. Nature 334 (1988) 395-402
13. 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. 346 (2005) 533-550
14. Degano M., Garcia K.C., Apostolopoulos V., Rudolph M.G., Teyton L., and Wilson I.A. A functional hot spot for antigen recognition in a superagonist TCR/MHC complex. Immunity 12 (2000) 251-261
15. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA, USA
16. Ely L.K., Beddoe T., Clements C.S., Matthews J.M., Purcell A.W., Kjer-Nielsen L., McCluskey J., and Rossjohn J. Disparate thermodynamics governing T cell receptor-MHC-I interactions implicate extrinsic factors in guiding MHC restriction. Proc. Natl. Acad. Sci. USA 103 (2006) 6641-6646
17. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
18. Garcia K.C., and Adams E.J. How the T cell receptor sees antigen-a structural view. Cell 122 (2005) 333-336
19. Garcia K.C., Degano M., Pease L.R., Huang M., Peterson P., Teyton L., and Wilson I.A. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279 (1998) 1166-1172
20. Garcia K.C., Tallquist M.D., Pease L.R., Brunmark A., Scott C.A., Degano M., Stura E.A., Peterson P.A., Wilson I.A., and Teyton L. Alphabeta T cell receptor interactions with syngeneic and allogeneic ligands: affinity measurements and crystallization. Proc. Natl. Acad. Sci. USA 94 (1997) 13838-13843
21. Ge Q., Holler P.D., Mahajan V.S., Nuygen T., Eisen H.N., and Chen J. Development of CD4+ T cells expressing a nominally MHC class I-restricted T cell receptor by two different mechanisms. Proc. Natl. Acad. Sci. USA 103 (2006) 1822-1827
22. Hahn M., Nicholson M.J., Pyrdol J., and Wucherpfennig K.W. Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor. Nat. Immunol. 6 (2005) 490-496
23. Hansen T., Balendiran G., Solheim J., Ostrov D., and Nathenson S. Structural features of MHC class I molecules that might facilitate alternative pathways of presentation. Immunol. Today 21 (2000) 83-88
24. Holler P.D., and Kranz D.M. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18 (2003) 255-264
25. Holler P.D., Holman P.O., Shusta E.V., O'Herrin S., Wittrup K.D., and Kranz D.M. In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc. Natl. Acad. Sci. USA 97 (2000) 5387-5392
26. Hornell T.M., Solheim J.C., Myers N.B., Gillanders W.E., Balendiran G.K., Hansen T.H., and Connolly J.M. Alloreactive and syngeneic CTL are comparably dependent on interaction with MHC class I alpha-helical residues. J. Immunol. 163 (1999) 3217-3225
27. Housset D., and Malissen B. What do TCR-pMHC crystal structures teach us about MHC restriction and alloreactivity?. Trends Immunol. 24 (2003) 429-437
28. Huseby E., Kappler J., and Marrack P. TCR-MHC/peptide interactions: kissing-cousins or a shotgun wedding?. Eur. J. Immunol. 34 (2004) 1243-1250
29. 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. 7 (2006) 1191-1199
30. Jerne N.K. The somatic generation of immune recognition. Eur. J. Immunol. 1 (1971) 1-9
31. Jones L.L., Brophy S.E., Bankovich A.J., Colf L.A., Hanick N.A., Garcia K.C., and Kranz D.M. Engineering and characterization of a stabilized alpha1/alpha2 module of the class I major histocompatibility complex product Ld. J. Biol. Chem. 281 (2006) 25734-25744
32. Kieke M.C., Shusta E.V., Boder E.T., Teyton L., Wittrup K.D., and Kranz D.M. Selection of functional T cell receptor mutants from a yeast surface- display library. Proc. Natl. Acad. Sci. USA 96 (1999) 5651-5656
33. Kranz D.M., Sherman D.H., Sitkovsky M.V., Pasternack M.S., and Eisen H.N. Immunoprecipitation of cell surface structure of cloned cytotoxic T lymphocytes by clone-specific antisera. Proc. Natl. Acad. Sci. USA 81 (1984) 573-577
34. Krogsgaard M., Prado N., Adams E.J., He X.L., Chow D.C., Wilson D.B., Garcia K.C., and Davis M.M. Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol. Cell 12 (2003) 1367-1378
35. Lee P.U., Churchill H.R., Daniels M., Jameson S.C., and Kranz D.M. Role of 2C T cell receptor residues in the binding of self- and allo- major histocompatibility complexes. J. Exp. Med. 191 (2000) 1355-1364
36. Luz J.G., Huang M., Garcia K.C., Rudolph M.G., Apostolopoulos V., Teyton L., and Wilson I.A. 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 (2002) 1175-1186
37. Manning T.C., Schlueter C.J., Brodnicki T.C., Parke E.A., Speir J.A., Garcia K.C., Teyton L., Wilson I.A., and Kranz D.M. Alanine scanning mutagenesis of an alphabeta T cell receptor: mapping the energy of antigen recognition. Immunity 8 (1998) 413-425
38. Maynard J., Petersson K., Wilson D.H., Adams E.J., Blondelle S.E., Boulanger M.J., Wilson D.B., and Garcia K.C. Structure of an autoimmune T cell receptor complexed with class II peptide-MHC: insights into MHC bias and antigen specificity. Immunity 22 (2005) 81-92
39. McFarland B.J., and Strong R.K. Thermodynamic analysis of degenerate recognition by the NKG2D immunoreceptor: not induced fit but rigid adaptation. Immunity 19 (2003) 803-812
40. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276 (1997) 307-326
41. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57 (2001) 1373-1382
42. Reiser J.B., Darnault C., Guimezanes A., Gregoire C., Mosser T., Schmitt-Verhulst A.M., Fontecilla-Camps J.C., Malissen B., Housset D., and Mazza G. Crystal structure of a T cell receptor bound to an allogeneic MHC molecule. Nat. Immunol. 1 (2000) 291-297
43. Reiser J.B., Gregoire C., Darnault C., Mosser T., Guimezanes A., Schmitt-Verhulst A.M., Fontecilla-Camps J.C., Mazza G., Malissen B., and Housset D. A T cell receptor CDR3beta loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. Immunity 16 (2002) 345-354
44. Reiser J.B., Darnault C., Gregoire C., Mosser T., Mazza G., Kearney A., van der Merwe P.A., Fontecilla-Camps J.C., Housset D., and Malissen B. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat. Immunol. 4 (2003) 241-247
45. Rodewald H.R., Koszinowski U.H., Eichmann K., and Melchers I. Predominant utilization of V beta 8+ T cell receptor genes in the H-2Ld- restricted cytotoxic T cell response against the immediate-early protein pp89 of the murine cytomegalovirus. J. Immunol. 143 (1989) 4238-4243
46. Rudolph M.G., Stanfield R.L., and Wilson I.A. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24 (2006) 419-466
47. Santori F.R., Kieper W.C., Brown S.M., Lu Y., Neubert T.A., Johnson K.L., Naylor S., Vukmanovic S., Hogquist K.A., and Jameson S.C. Rare, structurally homologous self-peptides promote thymocyte positive selection. Immunity 17 (2002) 131-142
48. d and the T cell receptor. J. Immunol. 157 (1996) 4478-4485
49. Sha W.C., Nelson C.A., Newberry R.D., Kranz D.M., Russell J.H., and Loh D.Y. Positive and negative selection of an antigen receptor on T cells in transgenic mice. Nature 336 (1988) 73-76
50. Sherman L.A., and Chattopadhyay S. The molecular basis of allorecognition. Annu. Rev. Immunol. 11 (1993) 385-402
51. Shusta E.V., Holler P.D., Kieke M.C., Kranz D.M., and Wittrup K.D. Directed evolution of a stable scaffold for T-cell receptor engineering. Nat. Biotechnol. 18 (2000) 754-759
52. Speir J.A., Garcia K.C., Brunmark A., Degano M., Peterson P.A., Teyton L., and Wilson I.A. Structural basis of 2C TCR allorecognition of H-2Ld peptide complexes. Immunity 8 (1998) 553-562
53. Starr T.K., Jameson S.C., and Hogquist K.A. Positive and negative selection of T cells. Annu. Rev. Immunol. 21 (2003) 139-176
54. Sykulev Y., Brunmark A., Tsomides T.J., Kageyama S., Jackson M., Peterson P.A., and Eisen H.N. High-affinity reactions between antigen-specific T-cell receptors and peptides associated with allogeneic and syngeneic major histocompatibility complex class I proteins. Proc. Natl. Acad. Sci. USA 91 (1994) 11487-11491
55. Tallquist M.D., Weaver A.J., and Pease L.R. Degenerate recognition of alloantigenic peptides on a positive- selecting class I molecule. J. Immunol. 160 (1998) 802-809
56. d complex. Mol. Immunol. 31 (1994) 705-711
57. Turner S.J., Doherty P.C., McCluskey J., and Rossjohn J. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6 (2006) 883-894
58. Tynan F.E., Burrows S.R., Buckle A.M., Clements C.S., Borg N.A., Miles J.J., Beddoe T., Whisstock J.C., Wilce M.C., Silins S.L., et al. T cell receptor recognition of a 'super-bulged' major histocompatibility complex class I-bound peptide. Nat. Immunol. 6 (2005) 1114-1122
59. Udaka K., Tsomides T.J., and Eisen H.N. A naturally occurring peptide recognized by alloreactive CD8+ cytotoxic T lymphocytes in association with a class I MHC protein. Cell 69 (1992) 989-998
60. Udaka K., Wiesmuller K., Kienle S., Jung G., and Walden P. Self-MHC-restricted peptides recognized by an alloreactive T-lymphocyte clone. J. Immunol. 157 (1996) 670-678
61. Willcox B.E., Gao G.F., Wyer J.R., Ladbury J.E., Bell J.I., Jakobsen B.K., and Anton van der Merwe P.A. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 10 (1999) 357-365
62. Wucherpfennig K.W., and Strominger J.L. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 80 (1995) 695-705
63. Zerrahn J., Held W., and Raulet D.H. The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 88 (1997) 627-636