Structure of an autoimmune T cell receptor complexed with class II peptide-MHC: Insights into MHC bias and antigen specificity

Immunity

Volumn 22, Issue 1, 2005, Pages 81-92

  Maynard, Jennifer ^a   Petersson, Karin ^a   Wilson, Dianne H ^b   Adams, Erin J ^a   Blondelle, Sylvie E ^b   Boulanger, Marty J ^a   Wilson, Darcy B ^b   Garcia, K Christopher ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN BASIC PROTEIN; PEPTIDE; T LYMPHOCYTE RECEPTOR;

ALPHA CHAIN; ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; COMBINATORIAL LIBRARY; COMPLEMENTARITY DETERMINING REGION; COMPLEX FORMATION; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; LYMPHOCYTE CLONE; LYMPHOCYTE FUNCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; T LYMPHOCYTE;

ANIMALS; AUTOIMMUNITY; CELLS, CULTURED; CLONE CELLS; CRYSTALLIZATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HYDROGEN BONDING; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MYELIN BASIC PROTEINS; PEPTIDE FRAGMENTS; PEPTIDE LIBRARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL; SENSITIVITY AND SPECIFICITY;

EID: 12444298109     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2004.11.015     Document Type: Article

References (74)

1. Acha-Orbea H., Mitchell D.J., Timmermann L., Wraith D.C., Tausch G.S., Waldor M.K., Zamvil S.S., McDevitt H.O., Steinman L. Limited heterogeneity of T cell receptors from lymphocytes mediating autoimmune encephalomyelitis allows specific immune intervention. Cell. 54:1988;263-273
2. Anderton S.M., Manickasingham S.P., Burkhart C., Luckcuck T.A., Holland S.J., Lamont A.G., Wraith D.C. Fine specificity of the myelin-reactive T cell repertoire. implications for TCR antagonism in autoimmunity J. Immunol. 161:1998;3357-3364
3. Anderton S.M., Radu C.G., Lowrey P.A., Ward E.S., Wraith D.C. Negative selection during the peripheral immune response to antigen. J. Exp. Med. 193:2001;1-11
4. Bankovich A.J., Garcia K.C. Not just any T cell receptor will do. Immunity. 18:2003;7-11
5. Basu D., Horvath S., Matsumoto I., Fremont D.H., Allen P.M. Molecular basis for recognition of an arthritic peptide and a foreign epitope on distinct MHC molecules by a single TCR. J. Immunol. 164:2000;5788-5796
6. Bhardwaj V., Kumar V., Geysen H.M., Sercarz E.E. Degenerate recognition of a dissimilar antigenic peptide by myelin basic protein-reactive T cells. Implications for thymic education and autoimmunity. J. Immunol. 151:1993;5000-5010
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., 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. CCP4 The CCP4 (Collaborative Computational Project Number 4) suite. programs for protein crystallography Acta Crystallogr. D. Biol. Crystallogr. 50:1994;760-763
10. Crawford, F., Huseby, E., White, J., Marrack, P., and Kappler, J.W. (2004). Mimotopes for alloreactive and conventional T cells in a peptide-MHC display library. PLoS Biol. 2(4).
11. Daniel C., Horvath S., 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., Bjorkman P.J. T-cell antigen receptor genes and T-cell recognition. Nature. 334:1988;395-402
13. Degano M., Garcia K.C., Apostolopoulos V., Rudolph M.G., Teyton L., Wilson I.A. A functional hot spot for antigen recognition in a superagonist TCR/MHC complex. Immunity. 12:2000;251-261
14. Delano W.L. The PyMOL Molecular Graphics System. 2002;DeLano Scientific, San Carlos, CA
15. Ding Y.H., Smith K.J., Garboczi D.N., Utz U., Biddison W.E., Wiley D.C. Two human T cell receptors bind in a similar diagonal mode to the HLA- A2/Tax peptide complex using different TCR amino acids. Immunity. 8:1998;403-411
16. Fairchild P.J., Wildgoose R., Atherton E., Webb S., Wraith D.C. An autoantigenic T cell epitope forms unstable complexes with class II MHC. a novel route for escape from tolerance induction Int. Immunol. 5:1993;1151-1158
17. Fugger L., Liang J., Gautam A., Rothbard J.B., McDevitt H.O. Quantitative analysis of peptides from myelin basic protein binding to the MHC class II protein, I-Au, which confers susceptibility to experimental allergic encephalomyelitis. Mol. Med. 2:1996;181-188
18. 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-MHC antigen. Science. 279:1998;1166-1172
19. Garcia K.C., Radu C.G., Ho J., Ober R.J., Ward E.S. Kinetics and thermodynamics of T cell receptor-autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 98:2001;6818-6823
20. Gautam A.M., Lock C.B., Smilek D.E., Pearson C.I., Steinman L., McDevitt H.O. Minimum structural requirements for peptide presentation by major histocompatibility complex class II molecules. implications in induction of autoimmunity Proc. Natl. Acad. Sci. USA. 91:1994;767-771
21. Gautam A.M., Liblau R., Chelvanayagam G., Steinman L., Boston T. A viral peptide with limited homology to a self peptide can induce clinical signs of experimental autoimmune encephalomyelitis. J. Immunol. 161:1998;60-64
22. Germain R.N. Immunology. Making a molecular match. Nature. 344:1990;19-22
23. Goverman J. Tolerance and autoimmunity in TCR transgenic mice specific for myelin basic protein. Immunol. Rev. 169:1999;147-159
24. Goverman J., Woods A., Larson L., Weiner L.P., Hood L., Zaller D.M. Transgenic mice that express a myelin basic protein-specific T cell receptor develop spontaneous autoimmunity. Cell. 72:1993;551-560
25. Grogan J.L., Kramer A., Nogai A., Dong L., Ohde M., Schneider-Mergener J., Kamradt T. Cross-reactivity of myelin basic protein-specific T cells with multiple microbial peptides. experimental autoimmune encephalomyelitis induction in TCR transgenic mice J. Immunol. 163:1999;3764-3770
26. Hagerty D.T., Allen P.M. Intramolecular mimicry. Identification and analysis of two cross- reactive T cell epitopes within a single protein. J. Immunol. 155:1995;2993-3001
27. He X.L., Radu C., Sidney J., Sette A., Ward E.S., Garcia K.C. Structural snapshot of aberrant antigen presentation linked to autoimmunity. the immunodominant epitope of MBP complexed with I-Au Immunity. 17:2002;83-94
28. Hemmer B., Vergelli M., Gran B., Ling N., Conlon P., Pinilla C., Houghten R., McFarland H.F., Martin R. Predictable TCR antigen recognition based on peptide scans leads to the identification of agonist ligands with no sequence homology. J. Immunol. 160:1998;3631-3636. a
29. Hemmer B., Vergelli M., Pinilla C., Houghten R., Martin R. Probing degeneracy in T-cell recognition using peptide combinatorial libraries. Immunol. Today. 19:1998;163-168. b
30. Hennecke J., Wiley D.C. T cell receptor-MHC interactions up close. Cell. 104:2001;1-4
31. Hennecke J., Carfi A., Wiley D.C. Structure of a covalently stabilized complex of a human alphabeta T-cell receptor, influenza HA peptide and MHC class II molecule, HLA-DR1. EMBO J. 19:2000;5611-5624
32. Holler P.D., Kranz D.M. T cell receptors. affinities, cross-reactivities, and a conformer model Mol. Immunol. 40:2004;1027-1031
33. Houghten R.A. General method for the rapid solid-phase synthesis of large numbers of peptides. specificity of antigen-antibody interaction at the level of individual amino acids Proc. Natl. Acad. Sci. USA. 82:1985;5131-5135
34. Housset D., Malissen B. What do TCR-pMHC crystal structures teach us about MHC restriction and alloreactivity? Trends Immunol. 24:2003;429-437
35. Ignatowicz L., Rees W., Pacholczyk R., Ignatowicz H., Kushnir E., Kappler J., Marrack P. T cells can be activated by peptides that are unrelated in sequence to their selecting peptide. Immunity. 7:1997;179-186
36. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard 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
37. Judkowski V., Pinilla C., Schroder K., Tucker L., Sarvetnick N., Wilson D.B. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J. Immunol. 166:2001;908-917
38. Kersh G.J., Allen P.M. Essential flexibility in the T-cell recognition of antigen. Nature. 380:1996;495-498. a
39. 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. b
40. Kersh G.J., Kersh E.N., Fremont D.H., Allen P.M. High- and low-potency ligands with similar affinities for the TCR. the importance of kinetics in TCR signaling Immunity. 9:1998;817-826
41. Krebber A., Bornhauser S., Burmester J., Honegger A., Willuda J., Bosshard H.R., Pluckthun A. Reliable cloning of functional antibody variable domains from hybridomas and spleen cell repertoires employing a reengineered phage display system. J. Immunol. Methods. 201:1997;35-55
42. Krogsgaard M., Prado N., Adams E.J., He X.L., Chow D.C., Wilson D.B., Garcia K.C., 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
43. Lang H.L., Jacobsen H., Ikemizu S., Andersson C., Harlos K., Madsen L., Hjorth P., Sondergaard L., Svejgaard A., Wucherpfennig K., et al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat. Immunol. 3:2002;940-943
44. 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
45. Loftus D.J., Chen Y., Covell D.G., Engelhard V.H., Appella E. Differential contact of disparate class I/peptide complexes as the basis for epitope cross-recognition by a single T cell receptor. J. Immunol. 158:1997;3651-3658
46. Loftus C., Huseby E., Gopaul P., Beeson C., Goverman J. Highly cross-reactive T cell responses to myelin basic protein epitopes reveal a nonpredictable form of TCR degeneracy. J. Immunol. 162:1999;6451-6457
47. Madden D. The three-dimensional structure of peptide-MHC complexes. Annu. Rev. Immunol. 13:1995;587-622
48. Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today. 19:1998;395-404
49. Mason K., Denney D.W. Jr., McConnell H.M. Kinetics of the reaction of a myelin basic protein peptide with soluble IAu. Biochemistry. 34:1995;14874-14878
50. Mateu M.G. Antibody recognition of picornaviruses and escape from neutralization. a structural view Virus Res. 1:1995;1-24
51. Nikolic-Zugic J., Bevan M.J. Role of self-peptides in positively selecting the T-cell repertoire. Nature. 344:1990;65-67
52. Pinilla C., Appel J.R., Houghten R.A. Investigation of antigen-antibody interactions using a soluble, non-support-bound synthetic decapeptide library composed of four trillion (4 x 10(12) sequences. Biochem. J. 301:1994;847-853
53. Pinilla C., Martin R., Gran B., Appel J.R., Boggiano C., Wilson D.B., Houghten R.A. Exploring immunological specificity using synthetic peptide combinatorial libraries. Curr. Opin. Immunol. 11:1999;193-202
54. Radu C.G., Ober B.T., Colantonio L., Qadri A., Ward E.S. Expression and characterization of recombinant soluble peptide. I-A complexes associated with murine experimental autoimmune diseases J. Immunol. 160:1998;5915-5921
55. Rammensee H.G., Friede T., Stevanoviic S. MHC ligands and peptide motifs. first listing Immunogenetics. 41:1995;178-228
56. Reinherz E.L., Tan K., Tang L., Kern P., Liu J., Xiong Y., Hussey R.E., Smolyar A., Hare B., Zhang R., et al. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science. 286:1999;1913-1921
57. 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
58. Rudolph M.G., Wilson I.A. The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 14:2002;52-65
59. Shih F.F., Allen P.M. T cells are not as degenerate as you think, once you get to know them. Mol. Immunol. 40:2004;1041-1046
60. Shusta E.V., Kieke M.C., Parke E., Kranz D.M., Wittrup K.D. Yeast polypeptide fusion surface display levels predict thermal stability and soluble secretion efficiency. J. Mol. Biol. 292:1999;949-956
61. Stefanova I., Dorfman J.R., Germain R.N. Self-recognition promotes the foreign antigen sensitivity of naive T lymphocytes. Nature. 420:2002;429-434
62. Sykulev Y., Brunmark A., Tsomides T.J., Kageyama S., Jackson M., Peterson P.A., 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
63. Sykulev Y., Joo M., Vturina I., Tsomides T.J., Eisen H.N. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity. 4:1996;565-571
64. Sykulev Y., Vugmeyster Y., Brunmark A., Ploegh H.L., Eisen H.N. Peptide antagonism and T cell receptor interactions with peptide-MHC complexes. Immunity. 9:1998;475-483
65. Urban J.L., Kumar V., Kono D.H., Gomez C., Horvath S.J., Clayton J., Ando D.G., Sercarz E.E., Hood L. Restricted use of T cell receptor V genes in murine autoimmune encephalomyelitis raises possibilities for antibody therapy. Cell. 54:1988;577-592
66. Willcox B.E., Gao G.F., Wyer J.R., Ladbury J.E., Bell J.I., Jakobsen B.K., Anton van der Merwe P. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity. 10:1999;357-365
67. 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
68. Wilson D.B., Wilson D.H., Schroder K., Pinilla C., Blondelle S., Houghten R.A., Garcia K.C. Specificity and degeneracy of T cells. Mol. Immunol. 40:2004;1047-1055
69. Wraith D.C., Bruun B., Fairchild P.J. Cross-reactive antigen recognition by an encephalitogenic T cell receptor. Implications for T cell biology and autoimmunity. J. Immunol. 149:1992;3765-3770
70. 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
71. Wucherpfennig K.W. T cell receptor crossreactivity as a general property of T cell recognition. Mol. Immunol. 40:2004;1009-1017
72. Wucherpfennig K.W., 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
73. Zamvil S.S., Steinman L. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 8:1990;579-621
74. Zamvil S.S., Mitchell D.J., Moore A.C., Schwarz A.J., Stiefel W., Nelson P.A., Rothbard J.B., Steinman L. T cell specificity for class II (I-A) and the encephalitogenic N- terminal epitope of the autoantigen myelin basic protein. J. Immunol. 139:1987;1075-1079