Evidence that Structural Rearrangements and/or Flexibility during TCR Binding Can Contribute to T Cell Activation

Molecular Cell

Volumn 12, Issue 6, 2003, Pages 1367-1378

  Krogsgaard, Michelle ^a   Prado, Nelida ^a   Adams, Erin J ^a   He, Xiao Lin ^a   Chow, Dar Chone ^a,c   Wilson, Darcy B ^b   Garcia, K Christopher ^a   Davis, Mark M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

^c University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR;

ACCURACY; ARTICLE; CONFORMATIONAL TRANSITION; GENE REARRANGEMENT; HEAT TOLERANCE; MAJOR HISTOCOMPATIBILITY COMPLEX; PREDICTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; RECEPTOR BINDING; STRUCTURE ANALYSIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THERMODYNAMICS;

EID: 0348047600     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00474-X     Document Type: Article

References (63)

1. Aivaizian D., Stern L.J. Phosphorylation of T cell receptor ξ is regulated by a lipid dependent folding transition. Nat. Struct. Biol. 7:2000;1023-1026.
2. Anikeeva N., Lebedeva T., Krogsgaard M., Tetin S.Y., Martinez-Hackert E., Kalams S.A., Davis M.M., Sykulev Y. Distinct molecular mechanisms account for the specificity of two different T-cell receptors. Biochemistry. 42:2003;4709-4716.
3. Backstrom B.T., Milia E., Peter A., Jaureguiberry B., Baldari C.T., Palmer E. A motif within the T cell receptor alpha chain constant region connecting peptide domain controls antigen responsiveness. Immunity. 5:1996;437-447.
4. Berg L.J., Pullen A.M., Fazekas de St., Groth B., Mathis D., Benoist C., Davis M.M. Antigen/MHC-specific T cells are preferentially exported from the thymus in the presence of their MHC ligand. Cell. 58:1989;1035-1046.
5. Boniface J.J., Reich Z., Lyons D.S., 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. 96:1999;11446-11451.
6. 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. 54:1998;905-921.
7. Call M.E., Pyrdol J., Wiedmann M., Wucherpfennig K.W. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell. 111:2002;967-979.
8. CCP4 Collaborative Computational Project, Number 4) The CCP4 suite. programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50:1994;760-763.
9. Davis M.M. A new trigger for T cells. Cell. 110:2002;285-287.
10. Davis M.M., Boniface J.J., Reich Z., Lyons D., Hampl J., Arden B., Chien Y.H. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16:1998;523-544.
11. Davis M.M., Krogsgaard M., Huppa J.B., Sumen C., Purbhoo M.A., Irvine D.J., Wu L.C., Ehrlich L. Dynamics of cell surface molecules during T-cell recognition. Annu. Rev. Biochem. 72:2003;717-742.
12. Degano M., Garcia K.C., Apostolopoulos V., Rudolph M.G., Teyton L., Wilson I.A. A functional hotspot for antigen recognition in a superagonist TCR/MHC complex. Immunity. 12:2000;251-261.
13. Ding Y.H., Baker B.M., Garboczi D.N., Biddison W.E., Wiley D.C. Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity. 11:1999;45-56.
14. k. J. Exp. Med. 195:2002;1043-1052.
15. Frisch C., Fersht A.R., Schreiber G. Experimental assignment of the structure of the transition state for the association of barnase and barstar. J. Mol. Biol. 308:2001;69-77.
16. Garcia K.C., Degano M., Stanfield R.L., Brunmark A., Jackson M.R., Peterson P.A., Teyton L., Wilson I.A. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science. 274:1996;209-219.
17. Garcia K.C., Degano M., Pease L.R., Huang M., Peterson P.A., Teyton L., Wilson I.A. Structural basis of plasticity in T cell receptor recognition of a self peptide-antigen. Science. 279:1998;1166-1172.
18. Garcia K.C., Radu C.G., Ho J., Ober R.J., Ward S.E. Kinetics and thermodynamics of T cell receptor-autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 98:2001;6818-6823.
19. Germain R.N., Stefanova I. The dynamics of T cell receptor signalling. complex orchestration and the key roles of tempo and cooperation Annu. Rev. Immunol. 17:1999;467-522.
20. Gil D., Schamel W.A., Montoya M., Sanchez-Madrid F., Alarcon B. Recruitment of Nck by CD3 reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell. 109:2002;901-912.
21. Hare B.J., Wyss D.F., Osburne M.S., Kern P.S., Reinherz E.L., Wagner G. Structure, specificity and CDR mobility of a class II restricted single-chain T-cell receptor. Nat. Struct. Biol. 6:1999;574-581.
22. Holler P.D., Kranz D.M. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity. 18:2003;255-264.
23. - T cell transfectants that express a high affinity T cell receptor exhibit enhanced peptide-dependent activation. J. Exp. Med. 194:2002;1043-1052.
24. Horn J.R., Russell D., Lewis E.A., Murphy K.P. Van't Hoff and calorimetric entalpies from isothermal titration calorimetry. are there significant discrepancies? Biochemistry. 40:2001;1774-1778.
25. Janeway C.A. Jr. Ligands for the T-cell receptor. hard times for avidity models Immunol. Today. 16:1995;223-225.
26. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:1991;110-119.
27. Jorgensen J.L., Esser U., Fazekas de St Groth B., Reay P.A., Davis M.M. Mapping T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature. 355:1992;224-230.
28. Kersh G.J., Allen P.M. Structural basis for T cell recognition of altered peptide ligands. a single T cell receptor can productively recognize a large continuum of related ligands J. Exp. Med. 184:1996;1259-1268.
29. Kjer-Nielsen L., Clements C.S., Purcell A.W., Brooks A.G., Whisstock J.C., Burrows S.R., McCluskey J., Rossjohn J. A structural basis for the selection of dominant αβ T cell receptors in antiviral immunity. Immunity. 18:2003;53-64.
30. Krogsgaard M., Wucherpfennig K.W., Cannella B., Hansen B.E., Svejgaard A., Pyrdol J., Ditzel H., Raine C., Engberg J., Fugger L. Visualization of myelin basic protein (MBP) T cell epitopes in multiple sclerosis lesions using a monoclonal antibody specific for the human histocompatibility leukocyte antigen (HLA)-DR2-MBP 85-99 complex. J. Exp. Med. 191:2000;1395-1412.
31. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. Procheck. a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26:1993;283-291.
32. Li Y., Li H., Yang F., Smith-Gill S.J., Mariuzza R.A. X-ray snapshots of the maturation of an antibody response to a protein antigen. Nat. Struct. Biol. 10:2003;482-488.
33. Liggins J.R., Privalov P.L. Energetics of the specific binding interaction of the first three zinc fingers of the transcription factor TFIIIA with its cognate DNA sequence. Proteins Suppl. 4:2000;50-62.
34. Maenaka K., Juji T., Wyer J.R., Gao G.F., Maenaka T., Zaccai N.R., Kikuchi A., Yabe T., Tokunaga K., Tadokaro K.et al. Killer cell immunoglobulin receptors and T cell receptors bind peptide-major histocompability complex class I with distinct thermodynamic and kinetic properties. J. Biol. Chem. 274:1999;28329-28334.
35. Maenaka K., van der Merwe P.A., Stuart D.I., Jones E.Y., Sondermann P. The human low affinity Fcγ receptors IIa, IIb, and III bind IgG with fast kinetics and distinct thermodynamic properties. J. Biol. Chem. 276:2001;44898-44904.
36. Mariuzza R.A., Poljak R.J. The basics of binding. mechanisms of antigen recognition and mimicry by antibodies Curr. Opin. Immunol. 5:1993;50-55.
37. k complexes. correlation of the dissociation rate with T-cell responsiveness Proc. Natl. Acad. Sci. USA. 91:1994;12862-12866.
38. Murphy K.P. Predicting binding energetics from structure. looking beyond DeltaG degrees Med. Res. Rev. 19:1999;333-339.
39. Murphy K.P., Freire E. Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv. Protein Chem. 43:1992;313-361.
40. Murphy K.P., Xie D., Garcia K.C., Amzel L.M., Freire E. Structural energetics of peptide recognition. angiotensin II/antibody binding Proteins. 15:1993;113-120.
41. Myszka D.G., Sweet R.W., Hensley P., Brigham-Burke M., Kwong P.D., Hendrickson W.A., Wyatt R., Sodroski J., Doyle M.L. Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. USA. 97:2000;9026-9031.
42. Ottemann K.M., Xiao W., Shin Y., Koshland D.E. A piston model for transmembrane signaling of the aspartate receptor. Science. 285:1999;1751-1754.
43. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
44. Petri V., Hsieh M., Brenowitz M. Thermodynamic and kinetic characterization of the binding of the TATA binding protein to the adenovirus E4 promoter. Biochemistry. 8:1995;9977-9984.
45. Privalov P.L., Jelesarov I., Read C.M., Dragan A.I., Crane-Robinson C. The energetics of HMG box interactions with DNA. thermodynamics of the DNA binding of the HMG box from mouse sox-5 J. Mol. Biol. 294:1999;997-1013.
46. Reay P.A., Kantor R.M., Davis M.M. Use of global amino acid replacements to define the requirements for MHC binding and T cell recognition of moth cytochrome c (93-103). J. Immunol. 152:1994;3946-3957.
47. Reiser J.B., Gregoire C., Darnault C., Moser T., Guimezanes A., Schmitt-Verhulst A.M., Fontecilla-Camps J.C., Mazza G., Malissen B., Housset D. A T cell receptor CDR3β loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. Immunity. 16:2002;345-354.
48. Reiser J.B., Darnault C., Gregoire C., Mosser T., Mazza G., Kearney A., van der Merwe P.A., Fontecilla-Camps J.C., Housset D., Malissen B. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat. Immunol. 4:2003;241-247.
49. Rudolph M.G., Wilson I.A. The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 14:2002;52-65.
50. Savage P.A., Boniface J.J., Davis M.M. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity. 10:1999;485-492.
51. Spolar R.S., Record M.T. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:1994;777-784.
52. Stewart-Jones G.B., McMichael A.J., Bell J.I., Stuart D.I., Jones E.Y. A structural basis for immunodominant human T cell receptor recognition. Nat. Immunol. 4:2003;657-663.
53. Stites W.E. Protein-protein interactions. interface structure, binding thermodynamics, and mutational analysis Chem. Rev. 97:1997;1233-1250.
54. Sun Z.J., Kim K.S., Wagner G., Reinherz E.L. Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3 ε γ heterodimer. Cell. 105:2001;913-923.
55. Tallquist M.D., Weaver A.J., Pease L.R. Degenerate recognition of alloantigenic peptides on a positive-selecting class I molecule. J. Immunol. 160:1998;802-809.
56. van der Merwe P.A. The TCR triggering puzzle. Immunity. 14:2001;665-668.
57. van der Merwe P.A., Davis S.J. Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21:2003;659-684.
58. Wedemayer G.J., Patten P.A., Wang L.H., Schultz P.G., Stevens R.C. Structural insights into the evolution of an antibody combining site. Science. 276:1997;1665-1669.
59. Werlen G., Palmer E. The T-cell receptor signalosome. a dynamic structure with expanding complexity Curr. Opin. Immunol. 14:2002;299-305.
60. Willcox B.E., Gao G.F., Wyer J.R., Ladbury J.E., Bell J.I., Jacobsen B.K., van der Merwe P.A. TCR binding to peptide-MCS stabilizes a flexible recognition interface. Immunity. 10:1999;357-365.
61. Wilson I.A., Stanfield R.L. Antibody-antigen interactions. new structures and new conformational changes Curr. Opin. Struct. Biol. 4:1994;857-867.
62. Wilson D.B., Pinilla C., Wilson D.H., Schroder K., Boggiano C., Judkowski V., Kaye J., Hemmer B., Martin R., Houghten R.A. Immunogenicity. I. Use of peptide libraries to identify epitopes that activate clonotypic CD4+ T cells and induce T cell responses to native peptide ligands. J. Immunol. 163:1999;6424-6434.
63. 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. 418:2002;552-556.