Disparate degrees of hypervariable loop flexibility control T-cell receptor cross-reactivity, specificity, and binding mechanism

Journal of Molecular Biology

Volumn 414, Issue 3, 2011, Pages 385-400

  Scott, Daniel R ^a   Borbulevych, Oleg Y ^a,b   Piepenbrink, Kurt H ^a,c   Corcelli, Steven A ^a   Baker, Brian M ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b QUANTUMBIO INC   (United States)

^c INSTITUTE OF HUMAN VIROLOGY   (United States)

Author keywords

conformational selection; cross reactivity; immune recognition; induced fit; specificity

Indexed keywords

T LYMPHOCYTE RECEPTOR;

ARTICLE; BINDING SITE; CROSS REACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

EID: 82555168290     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.10.006     Document Type: Article

References (46)

1. Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor Immunol. Today 19 1998 395 404 (Pubitemid 28392279)
2. Armstrong K.M., Piepenbrink K.H., and Baker B.M. Conformational changes and flexibility in T-cell receptor recognition of peptide-MHC complexes Biochem. J. 415 2008 183 196
3. Jones L.L., Colf L.A., Stone J.D., Garcia K.C., and Kranz D.M. Distinct CDR3 conformations in TCRs determine the level of cross-reactivity for diverse antigens, but not the docking orientation J. Immunol. 181 2008 6255 6264
4. Mazza C., Auphan-Anezin N., Gregoire C., Guimezanes A., Kellenberger C., and Roussel A. How much can a T-cell antigen receptor adapt to structurally distinct antigenic peptides? EMBO J. 26 2007 1972 1983 (Pubitemid 46628583)
5. Reiser J.B., Darnault C., Gregoire C., Mosser T., Mazza G., and Kearney A. CDR3 loop flexibility contributes to the degeneracy of TCR recognition Nat. Immunol. 4 2003 241 247 (Pubitemid 36322133)
6. Burrows S.R., Chen Z., Archbold J.K., Tynan F.E., Beddoe T., and Kjer-Nielsen L. Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability Proc. Natl Acad. Sci. 107 2010 10608 10613
7. Wu L.C., Tuot D.S., Lyons D.S., Garcia K.C., and Davis M.M. Two-step binding mechanism for T-cell receptor recognition of peptide MHC Nature 418 2002 552 556 (Pubitemid 34851403)
8. Csermely P., Palotai R., and Nussinov R. Induced fit, conformational selection and independent dynamic segments: an extended view of binding events Trends Biochem. Sci. 35 2010 539 546
9. Boehr D.D., Nussinov R., and Wright P.E. The role of dynamic conformational ensembles in biomolecular recognition Nat. Chem. Biol. 5 2009 789 796
10. Holler P.D., and Kranz D.M. T cell receptors: affinities, cross-reactivities, and a conformer model Mol. Immunol. 40 2004 1027 1031 (Pubitemid 38221182)
11. Hammes G.G., Chang Y.C., and Oas T.G. Conformational selection or induced fit: a flux description of reaction mechanism Proc. Natl Acad. Sci. USA 106 2009 13737 13741
12. Hare B.J., Wyss D.F., Osburne M.S., Kern P.S., Reinherz E.L., and Wagner G. Structure, specificity and CDR mobility of a class II restricted single-chain T-cell receptor Nat. Struct. Biol. 6 1999 574 581 (Pubitemid 29252840)
13. Gakamsky D.M., Lewitzki E., Grell E., Saulquin X., Malissen B., and Montero-Julian F. Kinetic evidence for a ligand-binding-induced conformational transition in the T cell receptor Proc. Natl Acad. Sci. USA 104 2007 16639 16644 (Pubitemid 350211069)
14. Armstrong K.M., Insaidoo F.K., and Baker B.M. Thermodynamics of T-cell receptor-peptide/MHC interactions: progress and opportunities J. Mol. Recognit. 21 2008 275 287 (Pubitemid 352019057)
15. Garcia K.C., and Adams E.J. How the T cell receptor sees antigen-a structural view Cell 122 2005 333 336 (Pubitemid 41127136)
16. Garboczi D.N., Ghosh P., Utz U., Fan Q.R., Biddison W.E., and Wiley D.C. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2 Nature 384 1996 134 141 (Pubitemid 26386462)
17. Borbulevych O.Y., Piepenbrink K.H., and Baker B.M. Conformational melding permits a conserved binding geometry in TCR recognition of foreign and self molecular mimics J. Immunol. 186 2011 2950 2958
18. Borbulevych O.Y., Piepenbrink K.H., Gloor B.E., Scott D.R., Sommese R.F., and Cole D.K. T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility Immunity 31 2009 885 896
19. Ding Y.H., Baker B.M., Garboczi D.N., Biddison W.E., and 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 (Pubitemid 29359956)
20. Gagnon S.J., Borbulevych O.Y., Davis-Harrison R.L., Turner R.V., Damirjian M., and Wojnarowicz A. T cell receptor recognition via cooperative conformational plasticity J. Mol. Biol. 363 2006 228 243 (Pubitemid 44414855)
21. Piepenbrink K.H., Borbulevych O.Y., Sommese R.F., Clemens J., Armstrong K.M., and Desmond C. Fluorine substitutions in an antigenic peptide selectively modulate T-cell receptor binding in a minimally perturbing manner Biochem. J. 423 2009 353 361
22. Boyd A.E., Dunlop C.S., Wong L., Radic Z., Taylor P., and Johnson D.A. Nanosecond dynamics of acetylcholinesterase near the active center gorge J. Biol. Chem. 279 2004 26612 26618 (Pubitemid 38798818)
23. Hibbs R.E., Radic Z., Taylor P., and Johnson D.A. Influence of agonists and antagonists on the segmental motion of residues near the agonist binding pocket of the acetylcholine-binding protein J. Biol. Chem. 281 2006 39708 39718 (Pubitemid 46041930)
24. Shi J., Tai K., McCammon J.A., Taylor P., and Johnson D.A. Nanosecond dynamics of the mouse acetylcholinesterase Cys69-Cys96 omega loop J. Biol. Chem. 278 2003 30905 30911 (Pubitemid 36994602)
25. Lakowicz J.R. Principles of Fluorescence Spectroscopy 3rd edit. 2006 Springer New York, NY
26. Davis-Harrison R.L., Insaidoo F.K., and Baker B.M. T cell receptor binding transition states and recognition of peptide/MHC Biochemistry 46 2007 1840 1850
27. Davis-Harrison R.L., Armstrong K.M., and Baker B.M. Two different T cell receptors use different thermodynamic strategies to recognize the same peptide/MHC ligand J. Mol. Biol. 346 2005 533 550
28. Armstrong K.M., and Baker B.M. A comprehensive calorimetric investigation of an entropically driven T cell receptor-peptide/major histocompatibility complex interaction Biophys. J. 93 2007 597 609 (Pubitemid 47057824)
29. Weikl T.R., and von Deuster C. Selected-fit versus induced-fit protein binding: kinetic differences and mutational analysis Proteins 75 2009 104 110
30. Hausmann S., Biddison W.E., Smith K.J., Ding Y.H., Garboczi D.N., and Utz U. Peptide recognition by two HLA-A2/Tax11-19-specific T cell clones in relationship to their MHC/peptide/TCR crystal structures J. Immunol. 162 1999 5389 5397 (Pubitemid 29307147)
31. Baker B.M., Turner R.V., Gagnon S.J., Wiley D.C., and 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 2001 551 562 (Pubitemid 32539552)
32. Baxter T.K., Gagnon S.J., Davis-Harrison R.L., Beck J.C., Binz A.K., and Turner R.V. Strategic mutations in the class I MHC HLA-A2 independently affect both peptide binding and T cell receptor recognition J. Biol. Chem. 279 2004 29175 29184 (Pubitemid 38915791)
33. Gagnon S.J., Borbulevych O.Y., Davis-Harrison R.L., Baxter T.K., Clemens J.R., and Armstrong K.M. Unraveling a hotspot for TCR recognition on HLA-A2: evidence against the existence of peptide-independent TCR binding determinants J. Mol. Biol. 353 2005 556
34. Wlodarski T., and Zagrovic B. Conformational selection and induced fit mechanism underlie specificity in noncovalent interactions with ubiquitin Proc. Natl Acad. Sci. USA 106 2009 19346 19351
35. Garcia K.C., Degano M., Pease L.R., Huang M., Peterson P.A., Teyton L., and Wilson I.A. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen Science 279 1998 1166 1172 (Pubitemid 28164360)
36. Colf L.A., Bankovich A.J., Hanick N.A., Bowerman N.A., Jones L.L., Kranz D.M., and Garcia K.C. How a single T cell receptor recognizes both self and foreign MHC Cell 129 2007 135 146 (Pubitemid 46507586)
37. Kjer-Nielsen L., Clements C.S., Brooks A.G., Purcell A.W., McCluskey J., and Rossjohn J. The 1.5 Å crystal structure of a highly selected antiviral T cell receptor provides evidence for a structural basis of immunodominance Structure 10 2002 1521 1532 (Pubitemid 35351492)
38. Newell E.W., Ely L.K., Kruse A.C., Reay P.A., Rodriguez S.N., and Lin A.E. Structural basis of specificity and cross-reactivity in T cell receptors specific for cytochrome c-I-E J. Immunol. 186 2011 5823 5832
39. McBeth C., Seamons A., Pizarro J.C., Fleishman S.J., Baker D., and Kortemme T. A new twist in TCR diversity revealed by a forbidden [alpha][beta] TCR J. Mol. Biol. 375 2008 1306 1319
40. Tsai C.J., Ma B., and Nussinov R. Protein-protein interaction networks: how can a hub protein bind so many different partners? Trends Biochem. Sci. 34 2009 594 600
41. Boulter J.M., Glick M., Todorov P.T., Baston E., Sami M., Rizkallah P., and Jakobsen B.K. Stable, soluble T-cell receptor molecules for crystallization and therapeutics Protein Eng. 16 2003 707 711 (Pubitemid 37314399)
42. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
43. Chen V.B., Arendall III.W.B., Headd J.J., Keedy D.A., Immormino R.M., and Kapral G.J. MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 12 21
44. Case D.A., Cheatham T.E., Darden T., Gohlke H., Luo R., and Merz K.M. The Amber biomolecular simulation programs J. Comput. Chem. 26 2005 1668 1688 (Pubitemid 43076180)
45. Hornak V., Abel R., Okur A., Strockbine B., Roitberg A., and Simmerling C. Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65 2006 712 725 (Pubitemid 44583220)
46. Furse K.E., and Corcelli S.A. The dynamics of water at DNA interfaces: computational studies of Hoechst 33258 bound to DNA J. Am. Chem. Soc. 130 2008 13103 13109