ATLAS: A database linking binding affinities with structures for wild-type and mutant TCR-pMHC complexes

Proteins: Structure, Function and Bioinformatics

Volumn 85, Issue 5, 2017, Pages 908-916

  Borrman, Tyler ^a   Cimons, Jennifer ^b   Cosiano, Michael ^b   Purcaro, Michael ^a   Pierce, Brian G ^c   Baker, Brian M ^b   Weng, Zhiping ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

3D viewer; adaptive immunity; binding energy; protein modeling; Rosetta; scoring functions

Indexed keywords

HLA A2 ANTIGEN; MUTANT PROTEIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRAV PROTEIN; TRBV PROTEIN; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; LIGAND; LYMPHOCYTE ANTIGEN RECEPTOR; PEPTIDE; PROTEIN BINDING;

ALGORITHM; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DATA BASE; ENERGY; HUMAN; HYDROGEN BOND; MAJOR HISTOCOMPATIBILITY COMPLEX; METADATA; NONHUMAN; POINT MUTATION; PREDICTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; SOFTWARE; SOLVATION; STRUCTURAL MODEL; THREE DIMENSIONAL STRUCTURE; VAN DER WAALS ENERGY; WILD TYPE; BINDING SITE; CHEMISTRY; FACTUAL DATABASE; GENETICS; IMMUNOLOGY; INTERNET; MOLECULAR MODEL; MUTATION; PROTEIN CONFORMATION; THERMODYNAMICS;

BINDING SITES; DATABASES, FACTUAL; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERNET; LIGANDS; MODELS, MOLECULAR; MUTATION; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, ANTIGEN, T-CELL; SOFTWARE; THERMODYNAMICS;

EID: 85013270487     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.25260     Document Type: Article

References (40)

1. Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 1974;248:701–710.
2. Babbitt BP, Allen PM, Matsueda G, Haber E, Unanue ER. Binding of immunogenic peptides to Ia histocompatibility molecules. Nature 1985;317:359–361.
3. Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012;12:269–281.
4. Varela-Rohena A, Molloy PE, Dunn SM, Li Y, Suhoski MM, Carroll RG, Milicic A, Mahon T, Sutton DH, Laugel B, Moysey R, Cameron BJ, Vuidepot A, Purbhoo MA, Cole DK, Phillips RE, June CH, Jakobsen BK, Sewell AK, Riley JL. Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 2008;14:1390–1395.
5. Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, Litzky L, Bagg A, Carreno BM, Cimino PJ, Binder-Scholl GK, Smethurst DP, Gerry AB, Pumphrey NJ, Bennett AD, Brewer JE, Dukes J, Harper J, Tayton-Martin HK, Jakobsen BK, Hassan NJ, Kalos M, June CH. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 2013;122:863–871.
6. Morgan RA, Chinnasamy N, Abate-Daga D, Gros A, Robbins PF, Zheng Z, Dudley ME, Feldman SA, Yang JC, Sherry RM, Phan GQ, Hughes MS, Kammula US, Miller AD, Hessman CJ, Stewart AA, Restifo NP, Quezado MM, Alimchandani M, Rosenberg AZ, Nath A, Wang T, Bielekova B, Wuest SC, Akula N, McMahon FJ, Wilde S, Mosetter B, Schendel DJ, Laurencot CM, Rosenberg SA. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 2013;36:133–151.
7. Oates J, Jakobsen BK. ImmTACs. Oncoimmunology 2013;2:e22891.
8. Purcell AW, McCluskey J, Rossjohn J. More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Discov 2007;6:404–414.
9. Chen J-L, Stewart-Jones G, Bossi G, Lissin NM, Wooldridge L, Choi EML, Held G, Dunbar PR, Esnouf RM, Sami M, Boulter JM, Rizkallah P, Renner C, Sewell A, Merwe PAVD, Jakobsen BK, Griffiths G, Jones EY, Cerundolo V. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J Exp Med 2005;201:1243–1255.
10. Cole DK, Edwards ESJ, Wynn KK, Clement M, Miles JJ, Ladell K, Ekeruche J, Gostick E, Adams KJ, Skowera A, Peakman M, Wooldridge L, Price DA, Sewell AK. Modification of MHC anchor residues generates heteroclitic peptides that alter TCR binding and T cell recognition. J Immunol 2010;185:2600–2610.
11. Holler PD, Kranz DM. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 2003;18:255–264.
12. Aleksic M, Dushek O, Zhang H, Shenderov E, Chen JL, Cerundolo V, Coombs D, Merwe PAVD. Dependence of T cell antigen recognition on T cell receptor-peptide MHC confinement time. Immunity 2010;32:163–174.
13. Stone JD, Kranz DM. Role of T cell receptor affinity in the efficacy and specificity of adoptive T cell therapies. Front Immunol 2013;4:244.
14. Sethi DK, Gordo S, Schubert DA, Wucherpfennig KW. Crossreactivity of a human autoimmune TCR is dominated by a single TCR loop. Nat Commun 2013;4:2623.
15. Wooldridge L, Ekeruche-Makinde J, Berg HAVD, Skowera A, Miles JJ, Tan MP, Dolton G, Clement M, Llewellyn-Lacey S, Price DA, Peakman M, Sewell AK. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem 2012;287:1168–1177.
16. Obenaus M, Leitão C, Leisegang M, Chen X, Gavvovidis I, Bruggen P, van der Uckert W, Schendel DJ, Blankenstein T. Identification of human T-cell receptors with optimal affinity to cancer antigens using antigen-negative humanized mice. Nat Biotechnol 2015;33:402–407.
17. Li Y, Moysey R, Molloy PE, Vuidepot A-L, 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.
18. Pierce BG, Hellman LM, Hossain M, Singh NK, Kooi CWV, Weng Z, Baker BM. Computational design of the affinity and specificity of a therapeutic T cell receptor. PLoS Comput Biol 2014;10:e1003478.
19. Zoete V, Irving M, Ferber M, Cuendet MA, Michielin O. Structure-based, rational design of T cell receptors. Front Immunol 2013;4:1–19.
20. Malecek K, Grigoryan A, Zhong S, Gu WJ, Johnson LA, Rosenberg SA, Cardozo T, Krogsgaard M. Specific increase in potency via structure-based design of a TCR. J Immunol 2014;193:2587–2599.
21. Borbulevych OY, Piepenbrink KH, Gloor BE, Scott DR, Sommese RF, Cole DK, Sewell AK, Baker BM. T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility. Immunity 2009;31:885–896.
22. 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.
23. Kastritis PL, Bonvin AM. Are scoring functions in protein–protein docking ready to predict interactomes? Clues Novel Binding Affinity Benchmark 2010;9:2216–2225.
24. Vreven T, Hwang H, Pierce BG, Weng Z. Prediction of protein–protein binding free energies. Protein Sci 2012;21:396–404.
25. Xue LC, Rodrigues JP, Kastritis PL, Bonvin AM, Vangone A. PRODIGY: a web server for predicting the binding affinity of protein–protein complexes. Bioinformatics 2016;32:3676–3678.
26. Geng C, Vangone A, Bonvin AM. Exploring the interplay between experimental methods and the performance of predictors of binding affinity change upon mutations in protein complexes. Protein Eng Des Sel 2016;29:291–299.
27. 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.
28. Vita R, Overton JA, Greenbaum JA, Ponomarenko J, Clark JD, Cantrell JR, Wheeler DK, Gabbard JL, Hix D, Sette A, Peters B. The immune epitope database (IEDB) 3.0. Nucleic Acids Res 2015;43:D405–D412.
29. Toseland CP, Clayton DJ, McSparron H, Hemsley SL, Blythe MJ, Paine K, Doytchinova IA, Guan P, Hattotuwagama CK, Flower DR. AntiJen: a quantitative immunology database integrating functional, thermodynamic, kinetic, biophysical, and cellular data. Immunome Res 2005;1:4.
30. Ehrenmann F, Kaas Q, Lefranc MP. IMGT/3Dstructure-DB and IMGT/DomainGapAlign: a database and a tool for immunoglobulins or antibodies, T cell receptors, MHC, IgSF and MhcSF. Nucleic Acids Res 2010;38:D301–D307.
31. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, Kaufman K, Renfrew PD, Smith CA, Sheffler W, Davis IW, Cooper S, Treuille A, Mandell DJ, Richter F, Ban Y-EA, Fleishman SJ, Corn JE, Kim DE, Lyskov S, Berrondo M, Mentzer S, Popović Z, Havranek JJ, Karanicolas J, Das R, Meiler J, Kortemme T, Gray JJ, Kuhlman B, Baker D, Bradley P. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol 2011;487:545–574.
32. Shapovalov MV, Dunbrack RL. A smoothed backbone-dependent rotamer library for proteins derived from adaptive kernel density estimates and regressions. Structure 2011;19:844–858.
33. Gagnon SJ, Borbulevych OY, Davis-Harrison RL, Turner RV, Damirjian M, Wojnarowicz A, Biddison WE, Baker BM. T cell receptor recognition via cooperative conformational plasticity. J Mol Biol 2006;363:228–243.
34. eiser JB, Grégoire C, Darnault C, Mosser T, Guimezanes A, Schmitt-Verhulst AM, Fontecilla-Camps JC, 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 2002;16:345–354.
35. Reiser J-B, Darnault C, Grégoire C, Mosser T, Mazza G, Kearney A, Merwe PAVD, Fontecilla-Camps JC, Housset D, Malissen B. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat Immunol 2003;4:241–247.
36. Mandell DJ, Kortemme T. Backbone flexibility in computational protein design. Curr Opin Biotechnol 2009;20:420–428.
37. Marco Biasini. pv - WebGL protein viewer : v1.81. 2015. https://doi.org/10.5281/zenodo.12620.
38. Blevins SJ, Pierce BG, Singh NK, Riley TP, Wang Y, Spear TT, Nishimura MI, Weng Z, Baker BM. How structural adaptability exists alongside HLA-A2 bias in the human αβ TCR repertoire. Proc Natl Acad Sci USA 2016;113:1276–1285.
39. Riley TP, Ayres CM, Hellman LM, Singh NK, Cosiano M, Cimons JM, Anderson MJ, Piepenbrink KH, Pierce BG, Weng Z, Baker BM. A generalized framework for computational design and mutational scanning of T-cell receptor binding interfaces. Protein Eng Des Sel 2016;29:1–12.
40. Sirin S, Apgar JR, Bennett EM, Keating AE. AB-Bind: antibody binding mutational database for computational affinity predictions. Protein Sci 2016;25:393–409.