An Engineered Switch in T Cell Receptor Specificity Leads to an Unusual but Functional Binding Geometry

Structure

Volumn 24, Issue 7, 2016, Pages 1142-1154

  Harris, Daniel T ^a   Singh, Nishant K ^b   Cai, Qi ^a   Smith, Sheena N ^a   Vander Kooi, Craig W ^c   Procko, Erik ^a   Kranz, David M ^a   Baker, Brian M ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; HLA A2 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; GEOMETRY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR DOCKING; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; ANTIBODY COMBINING SITE; CHEMISTRY; GENETICS; HUMAN; IMMUNOLOGY; MUTATION;

ANIMALS; BINDING SITES, ANTIBODY; HLA-A2 ANTIGEN; HUMANS; MICE; MOLECULAR DOCKING SIMULATION; MUTATION; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL;

EID: 84969850318     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2016.04.011     Document Type: Article

References (29)

1. Adams, J.J., Narayanan, S., Liu, B., Birnbaum, M.E., Kruse, A.C., Bowerman, N.A., Chen, W., Levin, A.M., Connolly, J.M., Zhu, C., et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 35 (2011), 681–693.
2. Adams, J.J., Narayanan, S., Birnbaum, M.E., Sidhu, S.S., Blevins, S.J., Gee, M.H., Sibener, L.V., Baker, B.M., Kranz, D.M., Garcia, K.C., Structural interplay between germline interactions and adaptive recognition determines the bandwidth of TCR-peptide-MHC cross-reactivity. Nat. Immunol. 17 (2016), 87–94.
3. Aggen, D.H., Chervin, A.S., Insaidoo, F.K., Piepenbrink, K.H., Baker, B.M., Kranz, D.M., Identification and engineering of human variable regions that allow expression of stable single-chain T cell receptors. Protein Eng. Des. Sel. 24 (2011), 361–372.
4. Baker, B.M., Scott, D.R., Blevins, S.J., Hawse, W.F., Structural and dynamic control of T-cell receptor specificity, cross-reactivity, and binding mechanism. Immunol. Rev. 250 (2012), 10–31.
5. Beringer, D.X., Kleijwegt, F.S., Wiede, F., van der Slik, A.R., Loh, K.L., Petersen, J., Dudek, N.L., Duinkerken, G., Laban, S., Joosten, A., et al. T cell receptor reversed polarity recognition of a self-antigen major histocompatibility complex. Nat. Immunol. 16 (2015), 1153–1161.
6. Blevins, S.J., Pierce, B.G., Singh, N.K., Riley, T.P., Wang, Y., Spear, T.T., Nishimura, M.I., Weng, Z., Baker, B.M., How structural adaptability exists alongside HLA-A2 bias in the human αβ TCR repertoire. Proc. Natl. Acad. Sci. USA 113 (2016), E1276–E1285.
7. Boder, E.T., Midelfort, K.S., Wittrup, K.D., Directed evolution of antibody fragments with monovalent femtomolar antigen-binding affinity. Proc. Natl. Acad. Sci. USA 97 (2000), 10701–10705.
8. Borbulevych, O.Y., Piepenbrink, K.H., Gloor, B.E., Scott, D.R., Sommese, R.F., Cole, D.K., Sewell, A.K., Baker, B.M., T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility. Immunity 31 (2009), 885–896.
9. Borbulevych, O.Y., Santhanagopolan, S.M., Hossain, M., Baker, B.M., TCRs used in cancer gene therapy cross-react with MART-1/Melan-A tumor antigens via distinct mechanisms. J. Immunol. 187 (2011), 2453–2463.
10. Cole, D.K., Yuan, F., Rizkallah, P.J., Miles, J.J., Gostick, E., Price, D.A., Gao, G.F., Jakobsen, B.K., Sewell, A.K., Germline-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J. Biol. Chem. 284 (2009), 27281–27289.
11. Cole, D.K., Malkit, S., Scott, D.R., Rizkallah, P.J., Borbulevych, O.Y., Todorov, P.T., Moysey, R.K., Jakobsen, B.K., Boulter, J.M., Baker, B.M., Li, Y., Increased peptide contacts govern high affinity binding of a modified TCR whilst maintaining a native pMHC docking mode. Front. Immunol., 4, 2013, 168.
12. Ding, Y.H., Baker, B.M., Garboczi, D.N., Biddison, W.E., Wiley, D.C., Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 11 (1999), 45–56.
13. Fowler, D.M., Stephany, J.J., Fields, S., Measuring the activity of protein variants on a large scale using deep mutational scanning. Nat. Protoc. 9 (2014), 2267–2284.
14. Gagnon, S.J., Borbulevych, O.Y., Davis-Harrison, R.L., Turner, R.V., Damirjian, M., Wojnarowicz, A., Biddison, W.E., Baker, B.M., T cell receptor recognition via cooperative conformational plasticity. J. Mol. Biol. 363 (2006), 228–243.
15. Holler, P.D., Kranz, D.M., Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18 (2003), 255–264.
16. Holler, P.D., Holman, P.O., Shusta, E.V., O'Herrin, S., Wittrup, K.D., Kranz, D.M., In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc. Natl. Acad. Sci. USA 97 (2000), 5387–5392.
17. Linette, G.P., Stadtmauer, E.A., Maus, M.V., Rapoport, A.P., Levine, B.L., Emery, L., Litzky, L., Bagg, A., Carreno, B.M., Cimino, P.J., et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122 (2013), 863–871.
18. Miles, J.J., McCluskey, J., Rossjohn, J., Gras, S., Understanding the complexity and malleability of T-cell recognition. Immunol. Cell Biol. 93 (2015), 433–441.
19. Piepenbrink, K.H., Blevins, S.J., Scott, D.R., Baker, B.M., The basis for limited specificity and MHC restriction in a T cell receptor interface. Nat. Commun., 4, 2013, 1948.
20. Pierce, B.G., Weng, Z., A flexible docking approach for prediction of T cell receptor–peptide–MHC complexes. Protein Sci. 22 (2013), 35–46.
21. Pierce, B.G., Hellman, L.M., Hossain, M., Singh, N.K., Vander Kooi, C.W., Weng, Z., Baker, B.M., Computational design of the affinity and specificity of a therapeutic T Cell receptor. PLoS Comput. Biol., 10, 2014, e1003478.
22. Procko, E., Hedman, R., Hamilton, K., Seetharaman, J., Fleishman, S.J., Su, M., Aramini, J., Kornhaber, G., Hunt, J.F., Tong, L., et al. Computational design of a protein-based enzyme inhibitor. J. Mol. Biol. 425 (2013), 3563–3575.
23. Rodenko, B., Toebes, M., Hadrup, S.R., van Esch, W.J.E., Molenaar, A.M., Schumacher, T.N.M., Ovaa, H., Generation of peptide-MHC class I complexes through UV-mediated ligand exchange. Nat. Protoc. 1 (2006), 1120–1132.
24. Rudolph, M.G., Stanfield, R.L., Wilson, I.A., How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24 (2006), 419–466.
25. 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.
26. Sliz, P., Michielin, O., Cerottini, J.-C., Luescher, I., Romero, P., Karplus, M., Wiley, D.C., Crystal structures of two closely related but antigenically distinct HLA-A2/Melanocyte-melanoma tumor-antigen peptide complexes. J. Immunol. 167 (2001), 3276–3284.
27. Smith, S.N., Sommermeyer, D., Piepenbrink, K.H., Blevins, S.J., Bernhard, H., Uckert, W., Baker, B.M., Kranz, D.M., Plasticity in the contribution of T Cell receptor variable region residues to binding of peptide–HLA-A2 complexes. J. Mol. Biol. 425 (2013), 4496–4507.
28. Smith, S.N., Wang, Y., Baylon, J.L., Singh, N.K., Baker, B.M., Tajkhorshid, E., Kranz, D.M., Changing the peptide specificity of a human T-cell receptor by directed evolution. Nat. Commun., 5, 2014, 5223.
29. Stone, J.D., Harris, D.T., Soto, C.M., Chervin, A.S., Aggen, D.H., Roy, E.J., Kranz, D.M., A novel T cell receptor single-chain signaling complex mediates antigen-specific T cell activity and tumor control. Cancer Immunol. Immunother. 63 (2014), 1163–1176.