Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor

Nature Immunology

Volumn 6, Issue 5, 2005, Pages 490-496

  Hahn, Michael ^a   Nicholson, Melissa J ^a   Pyrdol, Jason ^a   Wucherpfennig, Kai W ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; PEPTIDE; T LYMPHOCYTE RECEPTOR; AUTOANTIGEN; EPITOPE; HLA ANTIGEN CLASS 2; LYMPHOCYTE ANTIGEN RECEPTOR; MYELIN BASIC PROTEIN; MYELIN BASIC PROTEIN 83 99; MYELIN BASIC PROTEIN 83-99; PEPTIDE FRAGMENT;

AMINO TERMINAL SEQUENCE; ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOIMMUNITY; CELL STRUCTURE; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; PROTEIN INTERACTION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANTIGENS, CD4; AUTOANTIGENS; AUTOIMMUNITY; COMPLEMENTARITY DETERMINING REGIONS; CRYSTALLOGRAPHY, X-RAY; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYELIN BASIC PROTEINS; PEPTIDE FRAGMENTS; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 18244392426     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1187     Document Type: Article

References (49)

1. Steinman, L. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 85, 299-302 (1996).
2. Davis, M.M. & Chien, Y.-H. T-cell antigen receptors, in Fundamental Immunology (ed. Paul, W.E.) 227-258 (Lippincott Williams & Wilkins, Philadelphia, 2003).
3. Kisielow, P., Teh, H.S., von Bluthmann, H. & Boehmer, H. Positive selection of antigen-specific T cells in thymus by restricting MHC molecules. Nature 335, 730-733 (1988).
4. Kappler, J.W., Roehm, N. & Marrack, P. T cell tolerance by clonal elimination in the thymus. Cell 49, 273-280 (1987).
5. Alam, S.M. et al. T-cell-receptor affinity and thymocyte positive selection. Nature 381, 616-620 (1996).
6. Derbinski, J., Schulte, A., Kyewski, B. & Klein, L. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat. Immunol. 2, 1032-1039 (2001).
7. The Finnish-German APECED Consortium. Autoimmune Polyendocrinopathy- Candidiasis-Ectodermal Dystrophy. An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Nat. Genet. 17, 399-403 (1997).
8. Anderson, M.S. et al. Projection of an immunological self shadow within the thymus by the aire protein. Science 298, 1395-1401 (2002).
9. Harrington, C.J. et al. Differential tolerance is induced in T cells recognizing distinct epitopes of myelin basic protein. Immunity 8, 571-580 (1998).
10. Anderson, A.C. et al. High frequency of autoreactive myelin proteolipid protein-specific T cells in the periphery of naive mice: mechanisms of selection of the self-reactive repertoire. J. Exp. Med. 191, 761-770 (2000).
11. Wucherpfennig, K.W. et al. Structural requirements for binding of an immunodominant myelin basic protein peptide to DR2 isotypes and for its recognition by human T cell clones. J. Exp. Med. 179, 279-290 (1994).
12. Pribyl, T.M., Campagnoni, C., Kampf, K., Handley, V.W. & Campagnoni, A.T. The major myelin protein genes are expressed in the human thymus. J. Neurosci. Res. 45, 812-819 (1996).
13. Sakaguchi, N. et al. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 426, 454-460 (2003).
14. Garboczi, D.N. et al. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141 (1996).
15. Garcia, K.C. et al. An αβ T cell receptor structure at 2.5 Å and its orientation in the TCR-MHC complex. Science 274, 209-219 (1996).
16. Garcia, K.C. et al. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279, 1166-1172 (1998).
17. Ding, Y.H. et al. 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, 403-411 (1998).
18. 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, 657-663 (2003).
19. Reinherz, E.L. et al. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286, 1913-1921 (1999).
20. Reiser, J.B. et al. A T cell receptor CDR3β loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. Immunity 16, 345-354 (2002).
21. Reiser, J.B. et al. Crystal structure of a T cell receptor bound to an allogeneic MHC molecule. Nat. Immunol. 1, 291-297 (2000).
22. Sun, R. et al. Evidence that the antigen receptors of cytotoxic T lymphocytes interact with a common recognition pattern on the H-2Kb molecule. Immunity 3, 573-582 (1995).
23. 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).
24. Hennecke, J., Carfi, A. & Wiley, D.C. 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 (2000).
25. Wucherpfennig, K.W. et al. Clonal expansion and persistence of human T cells specific for an immunodominant myelin basic protein peptide. J. Immunol. 152, 5581-5592 (1994).
26. Ota, K. et al. T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis. Nature 346, 183-187 (1990).
27. Pette, M. et al. Myelin autoreactivity in multiple sclerosis: recognition of myelin basic protein in the context of HLA-DR2 products by T lymphocytes of multiple-sclerosis patients and healthy donors. Proc. Natl. Acad. Sci. USA 87, 7968-7972 (1990).
28. Krogsgaard, M. et al. 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, 1395-1412 (2000).
29. Madsen, L.S. et al. A humanized model for multiple sclerosis using HLA-DR2 and a human T-cell receptor. Nat. Genet. 23, 343-347 (1999).
30. Hausmann, S., Martin, M., Gauthier, L. & Wucherpfennig, K.W. Structural features of autoreactive TCR that determine the degree of degeneracy in peptide recognition. J. Immunol. 162, 338-344 (1999).
31. Nakagawa, T. et al. Cathepsin L: critical role in li degradation and CD4 T cell selection in the thymus. Science 280, 450-453 (1998).
32. 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).
33. Wang, J.H. et al. Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc. Natl. Acad. Sci. USA 98, 10799-10804 (2001).
34. Sim, B.C., Zerva, L., Greene, M.I. & Gascoigne, N.R. Control of MHC restriction by TCR Vα CDR1 and CDR2. Science 273, 963-966 (1996).
35. Savage, P.A. & Davis, M.M. A kinetic window constricts the T cell receptor repertoire in the thymus. Immunity 14, 243-252 (2001).
36. Busch, D.H. & Pamer, E.G. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189, 701-710 (1999).
37. Appel, H., Gauthier, L., Pyrdol, J. & Wucherpfennig, K.W. Kinetics of T-cell receptor binding by bivalent HLA-DR peptide complexes that activate antigen-specific human T-cells. J. Biol. Chem. 275, 312-321 (2000).
38. Monks, C.R., Freiberg, B.A., Kupfer, H., Sciaky, N. & Kupfer, A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86 (1998).
39. Grakoui, A. et al. The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227 (1999).
40. Ehrlich, L.I., Ebert, P.J., Krummel, M.F., Weiss, A. & Davis, M.M. Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation. Immunity 17, 809-822 (2002).
41. Richie, L.I. et al. Imaging synapse formation during thymocyte selection: inability of CD3ζ to form a stable central accumulation during negative selection. Immunity 16, 595-606 (2002).
42. 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, 695-705 (1995).
43. Maynard, J. et al. Structure of an autoimmune T cell receptor complexed with class II peptide-MHC; insights into MHC bias and antigen specificity. Immunity 22, 81-92 (2005).
44. Smith, K.J., Pyrdol, J., Gauthier, L., Wiley, D.C. & Wucherpfennig, K.W. Crystal structure of HLA-DR2 (DRA*0101, DRB1*1501) complexed with a peptide from human myelin basic protein. J. Exp. Med. 188, 1511-1520 (1998).
45. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Meth. Enzymol. 276, 307-326 (1997).
46. Storoni, L.C., McCoy, A.J. & Read, R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438 (2004).
47. Sundberg, E.J. et al. Structures of two streptococcal superantigens bound to TCR beta chains reveal diversity in the architecture of T cell signaling complexes. Structure (Camb.) 10, 687-699 (2002).
48. Brunger, A.T. et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
49. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).