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Science 20 February 1998:
Vol. 279. no. 5354, pp. 1166 - 1172
DOI: 10.1126/science.279.5354.1166
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Research Articles

Structural Basis of Plasticity in T Cell Receptor Recognition of a Self Peptide-MHC Antigen

K. Christopher Garcia, * Massimo Degano, * Larry R. Pease, Mingdong Huang, Per A. Peterson, Luc Teyton, Ian A. Wilson dagger

The T cell receptor (TCR) inherently has dual specificity. T cells must recognize self-antigens in the thymus during maturation and then discriminate between foreign pathogens in the periphery. A molecular basis for this cross-reactivity is elucidated by the crystal structure of the alloreactive 2C TCR bound to self peptide-major histocompatibility complex (pMHC) antigen H-2Kb-dEV8 refined against anisotropic 3.0 angstrom resolution x-ray data. The interface between peptide and TCR exhibits extremely poor shape complementarity, and the TCR beta  chain complementarity-determining region 3 (CDR3) has minimal interaction with the dEV8 peptide. Large conformational changes in three of the TCR CDR loops are induced upon binding, providing a mechanism of structural plasticity to accommodate a variety of different peptide antigens. Extensive TCR interaction with the pMHC alpha  helices suggests a generalized orientation that is mediated by the Valpha domain of the TCR and rationalizes how TCRs can effectively "scan" different peptides bound within a large, low-affinity MHC structural framework for those that provide the slight additional kinetic stabilization required for signaling.

K. C. Garcia, M. Degano, M. Huang, and I. A. Wilson are in the Department of Molecular Biology and the Skaggs Institute of Chemical Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA. L. R. Pease is in the Department of Immunology, Mayo Clinic, Rochester, MN 55905, USA. P. A. Peterson is at the R. W. Johnson Pharmaceutical Research Institute-La Jolla, 3535 General Atomic Court, San Diego, CA 92121, USA. L. Teyton is in the Department of Immunology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
*   These authors contributed equally to this work.

dagger    To whom correspondence should be addressed. E-mail: wilson{at}scripps.edu

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   Abstract »    Full Text »    PDF »
Psoriatic Arthritis Joint Fluids Are Characterized by CD8 and CD4 T Cell Clonal Expansions that Appear Antigen Driven.
P. J. Costello, R. J. Winchester, S. A. Curran, K. S. Peterson, D. J. Kane, B. Bresnihan, and O. M. FitzGerald (2001)
J. Immunol. 166, 2878-2886
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Differences in antigen recognition and cytolytic activity of CD8+ and CD8- T cells that express the same antigen-specific receptor.
B. K. Cho, K.-C. Lian, P. Lee, A. Brunmark, C. McKinley, J. Chen, D. M. Kranz, and H. N. Eisen (2001)
PNAS 98, 1723-1727
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Genetic control of peripheral TCRAV usage by representation in the preselection repertoire and MHC allele-specific overselection.
N. Torres-Nagel, B. Mehling, A.-F. LeRolle, E. Joly, and T. Hunig (2001)
Int. Immunol. 13, 63-73
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Distinct T Cell Interactions with HLA Class II Tetramers Characterize a Spectrum of TCR Affinities in the Human Antigen-Specific T Cell Response.
S. Reichstetter, R. A. Ettinger, A. W. Liu, J. A. Gebe, G. T. Nepom, and W. W. Kwok (2000)
J. Immunol. 165, 6994-6998
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T Cell Receptor (TCR)-mediated Repertoire Selection and Loss of TCR V{beta} Diversity during the Initiation of a CD4+ T Cell Response In Vivo.
M. Fasso, N. Anandasabapathy, F. Crawford, J. Kappler, C. G. Fathman, and W. M. Ridgway (2000)
J. Exp. Med. 192, 1719-1730
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Antigen contacts by Ni-reactive TCR: typical {alpha}{beta} chain cooperation versus {alpha} chain-dominated specificity.
J. Vollmer, H. U. Weltzien, K. Gamerdinger, S. Lang, Y. Choleva, and C. Moulon (2000)
Int. Immunol. 12, 1723-1731
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Antibodies Directed Against the MHC-I Molecule H-2Dd Complexed with an Antigenic Peptide: Similarities to a T Cell Receptor with the Same Specificity.
K. Polakova, D. Plaksin, D. H. Chung, I. M. Belyakov, J. A. Berzofsky, and D. H. Margulies (2000)
J. Immunol. 165, 5703-5712
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Supra-Agonist Peptides Enhance the Reactivation of Memory CTL Responses.
F. Micheletti, A. Canella, S. Vertuani, M. Marastoni, L. Tosi, S. Volinia, S. Traniello, and R. Gavioli (2000)
J. Immunol. 165, 4264-4271
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Molecular Recognition of Human CD1b Antigen Complexes: Evidence for a Common Pattern of Interaction with {alpha}{beta} TCRs.
A. Melian, G. F. M. Watts, A. Shamshiev, G. De Libero, A. Clatworthy, M. Vincent, M. B. Brenner, S. Behar, K. Niazi, R. L. Modlin, et al. (2000)
J. Immunol. 165, 4494-4504
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Nonstandard Peptide Binding Revealed by Crystal Structures of HLA-B*5101 Complexed with HIV Immunodominant Epitopes.
K. Maenaka, T. Maenaka, H. Tomiyama, M. Takiguchi, D. I. Stuart, and E. Y. Jones (2000)
J. Immunol. 165, 3260-3267
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The HLA System- First of Two Parts.
J. Klein and A. Sato (2000)
N. Engl. J. Med. 343, 702-709
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Affinity of thymic self-peptides for the TCR determines the selection of CD8+ T lymphocytes in the thymus.
B. T. Ober, Q. Hu, J. T. Opferman, S. Hagevik, N. Chiu, C.-R. Wang, and P. G. Ashton-Rickardt (2000)
Int. Immunol. 12, 1353-1363
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Structural requirements for antigen presentation by mouse CD1.
N. Burdin, L. Brossay, M. Degano, H. Iijima, M. Gui, I. A. Wilson, and M. Kronenberg (2000)
PNAS 97, 10156-10161
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The Alloreactive and Self-Restricted CD4+ T Cell Response Directed Against a Single MHC Class II/Peptide Combination.
J.-P. Kovalik, N. Singh, S. K. Mendiratta, W. D. Martin, L. Ignatowicz, and L. Van Kaer (2000)
J. Immunol. 165, 1285-1293
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Altered Peptide Ligand-Mediated TCR Antagonism Can Be Modulated by a Change in a Single Amino Acid Residue Within the CDR3{beta} of an MHC Class I-Restricted TCR.
A. M. Kalergis and S. G. Nathenson (2000)
J. Immunol. 165, 280-285
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Magnitude of structural changes of the T-cell receptor binding regions determine the strength of T-cell antagonism: molecular dynamics simulations of HLA-DR4 (DRB1*0405) complexed with analogue peptide.
H. Toh, N. Kamikawaji, T. Tana, S. Muta, T. Sasazuki, and S. Kuhara (2000)
Protein Eng. Des. Sel. 13, 423-429
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Molecular Basis for Recognition of an Arthritic Peptide and a Foreign Epitope on Distinct MHC Molecules by a Single TCR.
D. Basu, S. Horvath, I. Matsumoto, D. H. Fremont, and P. M. Allen (2000)
J. Immunol. 164, 5788-5796
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A Contig Map of the Mhc Class I Genomic Region in the Zebrafish Reveals Ancient Synteny.
V. Michalova, B. W. Murray, H. Sultmann, and J. Klein (2000)
J. Immunol. 164, 5296-5305
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Role of 2C T Cell Receptor Residues in the Binding of Self- and Allo-Major Histocompatibility Complexes.
P. U.Y. Lee, H. R.O. Churchill, M. Daniels, S. C. Jameson, and D. M. Kranz (2000)
J. Exp. Med. 191, 1355-1364
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The Role of Peptides in T Cell Alloreactivity Is Determined by Self-Major Histocompatibility Complex Molecules.
R. Obst, N. Netuschil, K. Klopfer, S. Stevanovi, and H.-G. Rammensee (2000)
J. Exp. Med. 191, 805-812
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