Early Relaxation Dynamics in the LC 13 T Cell Receptor in Reaction to 172 Altered Peptide Ligands: A Molecular Dynamics Simulation Study

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Knapp, Bernhard ^a,b   Dorffner, Georg ^a   Schreiner, Wolfgang ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERED PEPTIDE LIGAND; LIGAND; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR; PEPTIDE; PROTEIN BINDING;

ARTICLE; CHEMICAL REACTION; IMMUNOGENICITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR DYNAMICS; RELAXATION DYNAMICS; STATISTICAL ANALYSIS; BINDING SITE; CHEMISTRY; HUMAN; IMMUNOLOGY; MOLECULAR DOCKING; THERMODYNAMICS;

BINDING SITES; HUMANS; LIGANDS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; PEPTIDES; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; THERMODYNAMICS;

EID: 84878773470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064464     Document Type: Article

References (64)

1. Rudolph MG, Stanfield RL, Wilson IA, (2006) How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol 24: 419-466.
2. Choudhuri K, van der Merwe PA, (2007) Molecular mechanisms involved in T cell receptor triggering. Semin Immunol 19: 255-261.
3. Wucherpfennig KW, Allen PM, Celada F, Cohen IR, De BR, et al. (2007) Polyspecificity of T cell and B cell receptor recognition. Semin Immunol 19: 216-224.
4. Hemmer B, Vergelli M, Gran B, Ling N, Conlon P, et al. (1998) Predictable TCR antigen recognition based on peptide scans leads to the identification of agonist ligands with no sequence homology. J Immunol 160: 3631-3636.
5. Guy CS, Vignali DA, (2009) Organization of proximal signal initiation at the TCR:CD3 complex. Immunol Rev 232: 7-21.
6. Krogsgaard M, Prado N, Adams EJ, He XL, Chow DC, et al. (2003) Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol Cell 12: 1367-1378.
7. Frankild S, de Boer RJ, Lund O, Nielsen M, Kesmir C, (2008) Amino acid similarity accounts for T cell cross-reactivity and for "holes" in the T cell repertoire. PLoS ONE 3: e1831.
8. Tung CW, Ziehm M, Kamper A, Kohlbacher O, Ho SY, (2011) POPISK: T-cell reactivity prediction using support vector machines and string kernels. BMC Bioinformatics 12: 446.
9. Tung CW, Ho SY, (2007) POPI: predicting immunogenicity of MHC class I binding peptides by mining informative physicochemical properties. Bioinformatics 23: 942-949.
10. Myers EW, Miller W, (1988) Optimal alignments in linear space. Comput Appl Biosci 4: 11-17.
11. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
12. Tong JC, Tan TW, Ranganathan S, (2007) Methods and protocols for prediction of immunogenic epitopes. Brief Bioinform 8: 96-108.
13. Mishra S, Sinha S, (2009) Immunoinformatics and modeling perspective of T cell epitope-based cancer immunotherapy: a holistic picture. J Biomol Struct Dyn 27: 293-306.
14. Yewdell JW, Bennink JR, (1999) Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17: 51-88.
15. Hansson T, Oostenbrink C, Van Gunsteren WF, (2002) Molecular dynamics simulations. Curr Opin Struct Biol 12: 190-196.
16. Cuendet MA, Michielin O, (2008) Protein-protein interaction investigated by steered molecular dynamics: the TCR-pMHC complex. Biophys J 95: 3575-3590.
17. Yaneva R, Springer S, Zacharias M, (2009) Flexibility of the MHC class II peptide binding cleft in the bound, partially filled, and empty states: A molecular dynamics simulation study. Biopolymers 91: 14-27.
18. Wan S, Coveney PV, Flower DR, (2005) Molecular basis of peptide recognition by the TCR: affinity differences calculated using large scale computing. J Immunol 175: 1715-1723.
19. Painter CA, Cruz A, Lopez GE, Stern LJ, Zavala-Ruiz Z, (2008) Model for the peptide-free conformation of class II MHC proteins. PLoS ONE 3: e2403.
20. Zacharias M, Springer S, (2004) Conformational flexibility of the MHC class I alpha1-alpha2 domain in peptide bound and free states: a molecular dynamics simulation study. Biophys J 87: 2203-2214.
21. Wan S, Flower DR, Coveney PV, (2008) Toward an atomistic understanding of the immune synapse: Large-scale molecular dynamics simulation of a membrane-embedded TCR-pMHC-CD4 complex. Molecular Immunology 45: 1221-1230.
22. Rognan D, Stryhn A, Fugger L, Lyngbaek S, Engberg J, et al. (2000) Modeling the interactions of a peptide-major histocompatibility class I ligand with its receptors. I. Recognition by two alpha beta T cell receptors. J Comput Aided Mol Des 14: 53-69.
23. Haidar JN, Pierce B, Yu Y, Tong W, Li M, et al. (2009) Structure-based design of a T-cell receptor leads to nearly 100-fold improvement in binding affinity for pepMHC. Proteins 74: 948-960.
24. Camacho CJ, Katsumata Y, Ascherman DP, (2008) Structural and thermodynamic approach to peptide immunogenicity. PLoS Comput Biol 4: e1000231.
25. De Rosa MC, Giardina B, Bianchi C, Carelli AC, Pirolli D, et al. (2010) Modeling the ternary complex TCR-Vbeta/CollagenII(261-273)/HLA-DR4 associated with rheumatoid arthritis. PLoS ONE 5: e11550.
26. Stavrakoudis A, (2011) Insights into the structure of the LC13 TCR/HLA-B8-EBV peptide complex with molecular dynamics simulations. Cell Biochem Biophys 60: 283-295.
27. Cuendet MA, Zoete V, Michielin O, (2011) How T cell receptors interact with peptide-MHCs: a multiple steered molecular dynamics study. Proteins 79: 3007-3024.
28. Narzi D, Becker CM, Fiorillo MT, Uchanska-Ziegler B, Ziegler A, et al. (2012) Dynamical characterization of two differentially disease associated MHC class I proteins in complex with viral and self-peptides. J Mol Biol 415: 429-442.
29. Knapp B, Omasits U, Bohle B, Maillere B, Ebner C, et al. (2009) 3-Layer-based analysis of peptide-MHC-interaction: in silico prediction, peptide binding affinity and T cell activation in a relevant allergen-specific model. Molecular Immunology 46: 1839-1844.
30. Knapp B, Fischer G, Van HD, Fae I, Maillere B, et al. (2012) Association of HLA-DR1 with the allergic response to the major mugwort pollen allergen: molecular background. BMC Immunol 13: 43.
31. Knapp B, Omasits U, Schreiner W, Epstein MM, (2010) A comparative approach linking molecular dynamics of altered peptide ligands and MHC with in vivo immune responses. PLoS ONE 5: e11653.
32. Armstrong KM, Piepenbrink KH, Baker BM, (2008) Conformational changes and flexibility in T-cell receptor recognition of peptide-MHC complexes. Biochem J 415: 183-196.
33. Bergman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
34. Kjer-Nielsen L, Clements CS, Purcell AW, Brooks AG, Whisstock JC, et al. (2003) A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 18: 53-64.
35. Kjer-Nielsen L, Clements CS, Brooks AG, Purcell AW, McCluskey J, et al. (2002) The 1.5 A crystal structure of a highly selected antiviral T cell receptor provides evidence for a structural basis of immunodominance. Structure 10: 1521-1532.
36. Kjer-Nielsen L, Clements CS, Brooks AG, Purcell AW, Fontes MR, et al. (2002) The structure of HLA-B8 complexed to an immunodominant viral determinant: peptide-induced conformational changes and a mode of MHC class I dimerization. J Immunol 169: 5153-5160.
37. Burrows SR, Silins SL, Cross SM, Peh CA, Rischmueller M, et al. (1997) Human leukocyte antigen phenotype imposes complex constraints on the antigen-specific cytotoxic T lymphocyte repertoire. Eur J Immunol 27: 178-182.
38. Rognan D, Zimmermann N, Jung G, Folkers G, (1992) Molecular dynamics study of a complex between the human histocompatibility antigen HLA-A2 and the IMP58-66 nonapeptide from influenza virus matrix protein. Eur J Biochem 208: 101-113.
39. Zoete V, Michielin O, (2007) Comparison between computational alanine scanning and per-residue binding free energy decomposition for protein-protein association using MM-GBSA: Application to the TCR-p-MHC complex. Proteins 67: 1026-1047.
40. Gregoire C, Lin SY, Mazza G, Rebai N, Luescher IF, et al. (1996) Covalent assembly of a soluble T cell receptor-peptide-major histocompatibility class I complex. Proc Natl Acad Sci U S A 93: 7184-7189.
41. Toh H, Kamikawaji N, Tana T, Muta S, Sasazuki T, et al. (2000) 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. Protein Eng 13: 423-429.
42. Omasits U, Knapp B, Neumann M, Steinhauser O, Stockinger H, et al. (2008) Analysis of Key Parameters for Molecular Dynamics of pMHC Molecules. Mol Simulat 34: 781-793.
43. Wan S, Coveney PV, Flower DR, (2004) Large-scale molecular dynamics simulations of HLA-A*0201 complexed with a tumor-specific antigenic peptide: can the alpha3 and beta2m domains be neglected? J Comput Chem 25: 1803-1813.
44. Canutescu AA, Shelenkov AA, Dunbrack RL, (2003) A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci 12: 2001-2014.
45. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
46. Knapp B, Omasits U, Schreiner W, (2008) Side chain substitution benchmark for peptide/MHC interaction. Protein Sci 17: 977-982.
47. Knapp B, Omasits U, Frantal S, Schreiner W, (2009) A critical cross-validation of high throughput structural binding prediction methods for pMHC. J Comput Aided Mol Des 23: 301-307.
48. Hess B, Kutzner C, vanderSpoel D, Lindahl E, (2008) GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J Chem Theory Comput 4: 435-447.
49. Mazur AK, (1998) Hierarchy of Fast Motions in Protein Dynamics. J Phys Chem B 102: 473-479.
50. Feenstra KA, Hess B, Berendsen HJ (1999) Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. J Comput Chem 768-798.
51. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38.
52. Borg NA, Ely LK, Beddoe T, Macdonald WA, Reid HH, et al. (2005) The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nat Immunol 6: 171-180.
53. Manning TC, Schlueter CJ, Brodnicki TC, Parke EA, Speir JA, et al. (1998) Alanine scanning mutagenesis of an alphabeta T cell receptor: mapping the energy of antigen recognition. Immunity 8: 413-425.
54. Beddoe T, Chen Z, Clements CS, Ely LK, Bushell SR, et al. (2009) Antigen ligation triggers a conformational change within the constant domain of the alphabeta T cell receptor. Immunity 30: 777-788.
55. Ma Z, Janmey PA, Finkel TH, (2008) The receptor deformation model of TCR triggering. FASEB J 22: 1002-1008.
56. Ma Z, Finkel TH, (2010) T cell receptor triggering by force. Trends Immunol 31: 1-6.
57. Kim ST, Takeuchi K, Sun ZY, Touma M, Castro CE, et al. (2009) The alphabeta T cell receptor is an anisotropic mechanosensor. J Biol Chem 284: 31028-31037.
58. Karplus M, McCammon JA, (2002) Molecular dynamics simulations of biomolecules. Nat Struct Biol 9: 646-652.
59. Vitkup D, Ringe D, Petsko GA, Karplus M, (2000) Solvent mobility and the protein 'glass' transition. Nat Struct Biol 7: 34-38.
60. Ma J, Sigler PB, Xu Z, Karplus M, (2000) A dynamic model for the allosteric mechanism of GroEL. J Mol Biol 302: 303-313.
61. Young MA, Gonfloni S, Superti-Furga G, Roux B, Kuriyan J, (2001) Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105: 115-126.
62. Tai K, Shen T, Borjesson U, Philippopoulos M, McCammon JA, (2001) Analysis of a 10-ns molecular dynamics simulation of mouse acetylcholinesterase. Biophys J 81: 715-724.
63. Shaw DE, Maragakis P, Lindorff-Larsen K, Piana S, Dror RO, et al. (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330: 341-346.
64. Schamel WW, Reth M, (2007) The TCR binding site does move. Proc Natl Acad Sci U S A 104: 16398-16399.