Structure-based design of a T-cell receptor leads to nearly 100-fold improvement in binding affinity for pepMHC

Proteins: Structure, Function and Bioinformatics

Volumn 74, Issue 4, 2009, Pages 948-960

  Haidar, Jaafar N ^a   Pierce, Brian ^b   Yu, Yong ^a   Tong, Weiwei ^a   Li, Michael ^b   Weng, Zhiping ^a,b,c  

^a Boston University   (United States)

^b BOSTON UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

MHC; Rosetta; SPR; Structure based design; TCR; ZRANK

Indexed keywords

T LYMPHOCYTE RECEPTOR; HISTOCOMPATIBILITY ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; PEPTIDE;

ARTICLE; BINDING AFFINITY; MAJOR HISTOCOMPATIBILITY COMPLEX; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; ALGORITHM; BINDING SITE; CHEMISTRY; GENETICS; HUMAN; IMMUNOLOGY; KINETICS; STRUCTURE ACTIVITY RELATION;

ALGORITHMS; BINDING SITES; HISTOCOMPATIBILITY ANTIGENS; HUMANS; KINETICS; MAJOR HISTOCOMPATIBILITY COMPLEX; PEPTIDES; POINT MUTATION; RECEPTORS, ANTIGEN, T-CELL; STRUCTURE-ACTIVITY RELATIONSHIP; SURFACE PLASMON RESONANCE;

EID: 61449234107     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22203     Document Type: Article

References (44)

1. Janeway CA Jr, Travers P, Walport M, Shlomchik M. Immunobiology: The immune system in health and disease. New York: Garland Publishing; 2004.
2. Holler PD, Holman PO, Shusta EV, O'Herrin S, Wittrup KD, Kranz DM. In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc Natl Acad Sci USA 2000;97:5387-5392.
3. Li Y, Moysey R, Molloy PE, Vuidepot AL, Mahon T, Baston E, Dunn S, Liddy N, Jacob J, Jakobsen BK, Boulter JM. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat Biotechnol 2005;23:349-354.
4. Dunn SM, Rizkallah PJ, Baston E, Mahon T, Cameron B, Moysey R, Gao F, Sami M, Boulter J, Li Y, Jakobsen BK. Directed evolution of human T cell receptor CDR2 residues by phage display dramatically enhances affinity for cognate peptide-MHC without increasing apparent cross-reactivity. Protein Sci 2006;15:710-721.
5. Chlewicki LK, Holler PD, Monti BC, Clutter MR, Kranz DM. High-affinity, peptide-specific T cell receptors can be generated by mutations in CDR1. CDR2 or CDR3. J Mol Biol 2005;346:223-239.
6. Dufner P, Jermutus L, Minter RR. Harnessing phage and ribosome display for antibody optimisation. Trends Biotechnol 2006;24:523-529.
7. Selzer T, Albeck S, Schreiber G. Rational design of faster associating and tighter binding protein complexes. Nat Struct Biol 2000;7:537-541.
8. Song G, Lazar GA, Kortemme T, Shimaoka M, Desjarlais JR, Baker D, Springer TA. Rational design of intercellular adhesion molecule-1 (ICAM-1) variants for antagonizing integrin lymphocyte function-associated antigen-1-dependent adhesion. J Biol Chem 2006;281:5042-5049.
9. Joachimiak LA, Kortemme T, Stoddard BL, Baker D. Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein-protein interface. J Mol Biol 2006;361:195-208.
10. Kortemme T, Joachimiak LA, Bullock AN, Schuler AD, Stoddard BL, Baker D. Computational redesign of protein-protein interaction specificity. Nat Struct Mol Biol 2004;11:371-379.
11. Cole DK, Rizkallah PJ, Boulter JM, Sami M, Vuidepot AL, Glick M, Gao F, Bell JI, Jakobsen BK, Gao GF. Computational design and crystal structure of an enhanced affinity mutant human CD8 alphaalpha coreceptor. Proteins 2007;67:65-74.
12. Clark LA, Boriack-Sjodin PA, Eldredge J, Fitch C, Friedman B, Hanf KJ, Jarpe M, Liparoto SF, Li Y, Lugovskoy A, Miller S, Rushe M, Sherman W, Simon K, Van Vlijmen H. Affinity enhancement of an in vivo matured therapeutic antibody using structure-based computational design. Protein Sci 2006;15:949-960.
13. Lippow SM, Wittrup KD, Tidor B. Computational design of antibody-affinity improvement beyond in vivo maturation. Nat Biotechnol 2007;25:1171-1176.
14. Baker BM, Ding YH, Garboczi DN, Biddison WE, Wiley DC. Structural, biochemical, and biophysical studies of HLA-A2/altered peptide ligands binding to viral-peptide-specific human T-cell receptors. Cold Spring Harb Symp Quant Biol 1999;64:235-241.
15. Davis-Harrison RL, Insaidoo FK, Baker BM. T cell receptor binding transition states and recognition of peptide/MHC. Biochemistry 2007;46:1840-1850.
16. Garboczi DN, Ghosh P, Utz U, Fan QR, Biddison WE, Wiley DC. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996;384:134-141.
17. Bruccoleri RE. Application of Systematic Conformational Search to Protein Modeling. Mol Simul 1993;10:151-174.
18. Bruccoleri RE, Karplus M. Prediction of the folding of short polypeptide segments by uniform conformational sampling. Biopolymers 1987;26:137-168.
19. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 1983;4:187-217.
20. Kortemme T, Baker D. A simple physical model for binding energy hot spots in protein-protein complexes. Proc Natl Acad Sci USA 2002;99:14116-14121.
21. Pierce B, Weng Z. ZRANK: reranking protein docking predictions with an optimized energy function. Proteins 2007;67:1078-1086.
22. Neria E, Fischer S, Karplus M. Simulation of activation free energies in molecular systems. J Chem Phys 1996;105:1902-1921.
23. Gray JJ, Moughon S, Wang C, Schueler-Furman O, Kuhlman B, Rohl CA, Baker D. Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J Mol Biol 2003;331:281-299.
24. Zhang C, Vasmatzis G, Cornette JL, DeLisi C. Determination of atomic desolvation energies from the structures of crystallized proteins. J Mol Biol 1997;267:707-726.
25. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000;28:235-242.
26. Li L, Chen R, Weng Z. RDOCK: refinement of rigid-body protein docking predictions. Proteins 2003;53:693-707.
27. Murphy J, Gatchell DW, Prasad JC, Vajda S. Combination of scoring functions improves discrimination in protein-protein docking. Proteins 2003;53:840-854.
28. Lazaridis T, Karplus M. Effective energy function for proteins in solution. Proteins: Struct Funct Genet 1999;35:133-152.
29. Mintseris J, Pierce B, Wiehe K, Anderson R, Chen R, Weng Z. Integrating statistical pair potentials into protein complex prediction. Proteins 2007;69:511-520.
30. Liu S, Zhang C, Zhou H, Zhou Y. A physical reference state unifies the structure-derived potential of mean force for protein folding and binding. Proteins 2004;56:93-101.
31. Garboczi DN, Utz U, Ghosh P, Seth A, Kim J, VanTienhoven EA, Biddison WE, Wiley DC. Assembly, specific binding, and crystallization of a human TCR-alphabeta with an antigenic Tax peptide from human T lymphotropic virus type 1 and the class I MHC molecule HLA-A2. J Immunol 1996;157:5403-5410.
32. Garboczi DN, Hung DT, Wiley DC. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc Natl Acad Sci USA 1992;89:3429-3433.
33. Borg NA, Ely LK, Beddoe T, Macdonald WA, Reid HH, Clements CS, Purcell AW, Kjer-Nielsen L, Miles JJ, Burrows SR, McCluskey J, Rossjohn J. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nat Immunol 2005;6:171-180.
34. Ding YH, Baker BM, Garboczi DN, Biddison WE, Wiley DC. Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 1999;11:45-56.
35. Looger LL, Dwyer MA, Smith JJ, Hellinga HW. Computational design of receptor and sensor proteins with novel functions. Nature 2003;423:185-190.
36. Ma B, Nussinov R. Trp/Met/Phe hot spots in protein-protein interactions: potential targets in drug design. Curr Top Med Chem 2007;7:999-1005.
37. Lee LP, Tidor B. Barstar is electrostatically optimized for tight binding to barnase. Nat Struct Biol 2001;8:73-76.
38. Levy RM, Zhang LY, Gallicchio E, Felts AK. On the nonpolar hydration free energy of proteins: surface area and continuum solvent models for the solute-solvent interaction energy. J Am Chem Soc 2003;125:9523-9530.
39. Sammond DW, Eletr ZM, Purbeck C, Kimple RJ, Siderovski DP, Kuhlman B. Structure-based protocol for identifying mutations that enhance protein-protein binding affinities. J Mol Biol 2007;371:1392-1404.
40. Cole DK, Pumphrey NJ, Boulter JM, Sami M, Bell JI, Gostick E, Price DA, Gao GF, Sewell AK, Jakobsen BK. Human TCR-binding affinity is governed by MHC class restriction. J Immunol 2007;178:5727-5734.
41. Moza B, Buonpane RA, Zhu P, Herfst CA, Rahman AK, McCormick JK, Kranz DM, Sundberg EJ. Long-range cooperative binding effects in a T cell receptor variable domain. Proc Natl Acad Sci USA 2006;103:9867-9872.
42. Laugel B, Boulter JM, Lissin N, Vuidepot A, Li Y, Gostick E, Crotty LE, Douek DC, Hemelaar J, Price DA, Jakobsen BK, Sewell AK. Design of soluble recombinant T cell receptors for antigen targeting and T cell inhibition. J Biol Chem 2005;280:1882-1892.
43. Cho S, Swaminathan CP, Yang J, Kerzic MC, Guan R, Kieke MC, Kranz DM, Mariuzza RA, Sundberg EJ. Structural basis of affinity maturation and intramolecular cooperativity in a protein-protein interaction. Structure 2005;13:1775-1787.
44. Sami M, Rizkallah PJ, Dunn S, Molloy P, Moysey R, Vuidepot A, Baston E, Todorov P, Li Y, Gao F, Boulter JM, Jakobsen BK. Crystal structures of high affinity human T-cell receptors bound to peptide major histocompatibility complex reveal native diagonal binding geometry. Protein Eng Des Sel 2007;20:397-403.