How structural adaptability exists alongside HLA-A2 bias in the human αβ TCR repertoire

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 9, 2016, Pages E1276-E1285

  Blevins, Sydney J ^a   Pierce, Brian G ^b   Singh, Nishant K ^a   Riley, Timothy P ^a   Wang, Yuan ^a   Spear, Timothy T ^c,d   Nishimura, Michael I ^c,d   Weng, Zhiping ^e   Baker, Brian M ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d LOYOLA UNIVERSITY HEALTH SYSTEM   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Binding; MHC bias; Peptide MHC; Structure; T cell receptor

Indexed keywords

HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHABETA CHAIN; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR;

ALPHA HELIX; ARTICLE; ENERGY TRANSFER; ENTROPY; GERM LINE; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; RECEPTOR BINDING; STATIC ELECTRICITY; CHEMISTRY; HUMAN; PROTEIN CONFORMATION;

HLA-A2 ANTIGEN; HUMANS; PROTEIN CONFORMATION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; STATIC ELECTRICITY;

EID: 84959550142     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1522069113     Document Type: Article

References (83)

1. Zinkernagel RM, Doherty PC (1974) Immunological surveillance against altered self components by sensitised T lymphocytes in lymphocytic choriomeningitis. Nature 251(5475):547-548.
2. Garboczi DN, et al. (1996) Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384(6605):134-141.
3. Garcia KC, et al. (1996) An alphabeta T cell receptor structure at 2.5 Å and its orientation in the TCR-MHC complex. Science 274(5285):209-219.
4. Zerrahn J, Held W, Raulet DH (1997) The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 88(5):627-636.
5. Garcia KC, Adams JJ, Feng D, Ely LK (2009) The molecular basis of TCR germline bias for MHC is surprisingly simple. Nat Immunol 10(2):143-147.
6. Van Laethem F, et al. (2007) Deletion of CD4 and CD8 coreceptors permits generation of alphabetaT cells that recognize antigens independently of the MHC. Immunity 27(5):735-750.
7. Tikhonova AN, et al. (2012) αβ T cell receptors that do not undergo major histocompatibility complex-specific thymic selection possess antibody-like recognition specificities. Immunity 36(1):79-91.
8. Mazza C, Malissen B (2007) What guides MHC-restricted TCR recognition? Semin Immunol 19(4):225-235.
9. Rangarajan S, Mariuzza RA (2014) T cell receptor bias for MHC: Co-evolution or coreceptors? Cell Mol Life Sci 71(16):3059-3068.
10. Van Laethem F, Tikhonova AN, Singer A (2012) MHC restriction is imposed on a diverse T cell receptor repertoire by CD4 and CD8 co-receptors during thymic selection. Trends Immunol 33(9):437-441.
11. Garcia KC (2012) Reconciling views on T cell receptor germline bias for MHC. Trends Immunol 33(9):429-436.
12. Miles JJ, McCluskey J, Rossjohn J, Gras S (2015) Understanding the complexity and malleability of T-cell recognition. Immunol Cell Biol 93(5):433-441.
13. Borbulevych OY, Santhanagopolan SM, Hossain M, Baker BM (2011) TCRs used in cancer gene therapy cross-react with MART-1/Melan-A tumor antigens via distinct mechanisms. J Immunol 187(5):2453-2463.
14. Adams JJ, et al. (2011) T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 35(5):681-693.
15. Stadinski BD, et al. (2011) A role for differential variable gene pairing in creating T cell receptors specific for unique major histocompatibility ligands. Immunity 35(5): 694-704.
16. Stadinski BD, et al. (2014) Effect of CDR3 sequences and distal V gene residues in regulating TCR-MHC contacts and ligand specificity. J Immunol 192(12): 6071-6082.
17. Deng L, Langley RJ, Wang Q, Topalian SL, Mariuzza RA (2012) Structural insights into the editing of germ-line-encoded interactions between T-cell receptor and MHC class II by Vα CDR3. Proc Natl Acad Sci USA 109(37):14960-14965.
18. Burrows SR, et al. (2010) Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Proc Natl Acad Sci USA 107(23):10608-10613.
19. Dai S, et al. (2008) Crossreactive T cells spotlight the germline rules for alphabeta T cell-receptor interactions with MHC molecules. Immunity 28(3):324-334.
20. Reinherz EL, et al. (1999) The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286(5446):1913-1921.
21. Feng D, Bond CJ, Ely LK, Maynard J, Garcia KC (2007) Structural evidence for a germline-encoded T cell receptor-major histocompatibility complex interaction "codon." Nat Immunol 8(9):975-983.
22. Marrack P, Scott-Browne JP, Dai S, Gapin L, Kappler JW (2008) Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu Rev Immunol 26:171-203.
23. Magarian-Blander J, Ciborowski P, Hsia S, Watkins SC, Finn OJ (1998) Intercellular and intracellular events following the MHC-unrestricted TCR recognition of a tumor-specific peptide epitope on the epithelial antigen MUC1. J Immunol 160(7):3111-3120.
24. Castro CD, Luoma AM, Adams EJ (2015) Coevolution of T-cell receptors with MHC and non-MHC ligands. Immunol Rev 267(1):30-55.
25. Beringer DX, et al. (2015) T cell receptor reversed polarity recognition of a self-antigen major histocompatibility complex. Nat Immunol 16(11):1153-1161.
26. Honig B, Nicholls A (1995) Classical electrostatics in biology and chemistry. Science 268(5214):1144-1149.
27. Hendsch ZS, Tidor B (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci 3(2):211-226.
28. Bosshard HR, Marti DN, Jelesarov I (2004) Protein stabilization by salt bridges: Concepts, experimental approaches and clarification of some misunderstandings. J Mol Recognit 17(1):1-16.
29. Collis AVJ, Brouwer AP, Martin ACR (2003) Analysis of the antigen combining site: Correlations between length and sequence composition of the hypervariable loops and the nature of the antigen. J Mol Biol 325(2):337-354.
30. Chen KY, Liu J, Ren EC (2012) Structural and functional distinctiveness of HLA-A2 allelic variants. Immunol Res 53(1-3):182-190.
31. Baker BM, Turner RV, Gagnon SJ, Wiley DC, Biddison WE (2001) 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(5):551-562.
32. Gagnon SJ, et al. (2005) Unraveling a hotspot for TCR recognition on HLA-A2: Evidence against the existence of peptide-independent TCR binding determinants. J Mol Biol 353(3):556-573.
33. Baxter TK, et al. (2004) Strategic mutations in the class I major histocompatibility complex HLA-A2 independently affect both peptide binding and T cell receptor recognition. J Biol Chem 279(28):29175-29184.
34. Stewart JJ, et al. (1997) A Shannon entropy analysis of immunoglobulin and T cell receptor. Mol Immunol 34(15):1067-1082.
35. Holland SJ, et al. (2012) The T-cell receptor is not hardwired to engage MHC ligands. Proc Natl Acad Sci USA 109(45):E3111-E3118.
36. Scott-Browne JP, White J, Kappler JW, Gapin L, Marrack P (2009) Germline-encoded amino acids in the alphabeta T-cell receptor control thymic selection. Nature 458(7241):1043-1046.
37. Lawrence MC, Colman PM (1993) Shape complementarity at protein/protein interfaces. J Mol Biol 234(4):946-950.
38. Liu YC, et al. (2013) Highly divergent T-cell receptor binding modes underlie specific recognition of a bulged viral peptide bound to a human leukocyte antigen class I molecule. J Biol Chem 288(22):15442-15454.
39. Hassan C, et al. (2015) Naturally processed non-canonical HLA-A∗02:01 presented peptides. J Biol Chem 290(5):2593-2603.
40. Piepenbrink KH, Blevins SJ, Scott DR, Baker BM (2013) The basis for limited specificity and MHC restriction in a T cell receptor interface. Nat Commun 4:1948.
41. Horovitz A (1996) Double-mutant cycles: A powerful tool for analyzing protein structure and function. Fold Des 1(6):R121-R126.
42. Cole DK, et al. (2014) T-cell receptor (TCR)-peptide specificity overrides affinity-enhancing TCR-major histocompatibility complex interactions. J Biol Chem 289(2):628-638.
43. Sheinerman FB, Honig B (2002) On the role of electrostatic interactions in the design of protein-protein interfaces. J Mol Biol 318(1):161-177.
44. Buslepp J, Wang H, Biddison WE, Appella E, Collins EJ (2003) A correlation between TCR Valpha docking on MHC and CD8 dependence: Implications for T cell selection. Immunity 19(4):595-606.
45. Day EB, et al. (2011) Structural basis for enabling T-cell receptor diversity within biased virus-specific CD8+ T-cell responses. Proc Natl Acad Sci USA 108(23):9536-9541.
46. Flajnik MF, Kasahara M (2010) Origin and evolution of the adaptive immune system: Genetic events and selective pressures. Nat Rev Genet 11(1):47-59.
47. Birtalan S, et al. (2008) The intrinsic contributions of tyrosine, serine, glycine and arginine to the affinity and specificity of antibodies. J Mol Biol 377(5):1518-1528.
48. Shiroishi M, et al. (2007) Structural consequences of mutations in interfacial Tyr residues of a protein antigen-antibody complex. The case of HyHEL-10-HEL. J Biol Chem 282(9):6783-6791.
49. Dunbar J, Knapp B, Fuchs A, Shi J, Deane CM (2014) Examining variable domain orientations in antigen receptors gives insight into TCR-like antibody design. PLoS Comput Biol 10(9):e1003852.
50. Bontrop RE, Otting N, Slierendregt BL, Lanchbury JS (1995) Evolution of major histocompatibility complex polymorphisms and T-cell receptor diversity in primates. Immunol Rev 143(1):33-62.
51. Robinson J, et al. (2011) The IMGT/HLA database. Nucleic Acids Res 39(Database issue): D1171-D1176.
52. Ding YH, et al. (1998) Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 8(4): 403-411.
53. Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14(6):1188-1190.
54. Firoz A, Malik A, Afzal O, Jha V (2010) ContPro: A Web tool for calculating amino acid contact distances in protein from 3D-structures at different distance threshold. Bioinformation 5(2):55-57.
55. Kass I, Buckle AM, Borg NA (2014) Understanding the structural dynamics of TCRpMHC complex interactions. Trends Immunol 35(12):604-612.
56. Hawse WF, et al. (2014) TCR scanning of peptide/MHC through complementary matching of receptor and ligand molecular flexibility. J Immunol 192(6):2885-2891.
57. Yang X, et al. (2015) Structural basis for clonal diversity of the public T cell response to a dominant human cytomegalovirus epitope. J Biol Chem 290(48):29106-29119.
58. Rudolph MG, Stanfield RL, Wilson IA (2006) How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol 24:419-466.
59. Pierce BG, Weng Z (2013) A flexible docking approach for prediction of T cell receptor- peptide-MHC complexes. Protein Sci 22(1):35-46.
60. Fitch CA, et al. (2002) Experimental pK(a) values of buried residues: Analysis with continuum methods and role of water penetration. Biophys J 82(6):3289-3304.
61. Khan AR, Baker BM, Ghosh P, Biddison WE, Wiley DC (2000) The structure and stability of an HLA-A∗0201/octameric tax peptide complex with an empty conserved peptide-N-terminal binding site. J Immunol 164(12):6398-6405.
62. Motozono C, et al. (2014) Molecular basis of a dominant T cell response to an HIV reverse transcriptase 8-mer epitope presented by the protective allele HLA-B∗51:01. J Immunol 192(7):3428-3434.
63. Davis-Harrison RL, Armstrong KM, Baker BM (2005) Two different T cell receptors use different thermodynamic strategies to recognize the same peptide/MHC ligand. J Mol Biol 346(2):533-550.
64. Boulter JM, et al. (2003) Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng 16(9):707-711.
65. Pierce BG, et al. (2014) Computational design of the affinity and specificity of a therapeutic T cell receptor. PLoS Comput Biol 10(2):e1003478.
66. Ding YH, Baker BM, Garboczi DN, Biddison WE, Wiley DC (1999) Four A6-TCR/peptide/ HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 11(1):45-56.
67. Chen J-L, et al. (2005) Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J Exp Med 201(8):1243-1255.
68. Gras S, et al. (2009) Structural bases for the affinity-driven selection of a public TCR against a dominant human cytomegalovirus epitope. J Immunol 183(1):430-437.
69. Bulek AM, et al. (2012) Structural basis for the killing of human beta cells by CD8+ T cells in type 1 diabetes. Nat Immunol 13(3):283-289.
70. Stewart-Jones GB, McMichael AJ, Bell JI, Stuart DI, Jones EY (2003) A structural basis for immunodominant human T cell receptor recognition. Nat Immunol 4(7):657-663.
71. Cole DK, et al. (2009) Germ line-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J Biol Chem 284(40):27281-27289.
72. Miles JJ, et al. (2010) Genetic and structural basis for selection of a ubiquitous T cell receptor deployed in Epstein-Barr virus infection. PLoS Pathog 6(11):e1001198.
73. Liu YC, et al. (2014) A molecular basis for the interplay between T cells, viral mutants, and human leukocyte antigen micropolymorphism. J Biol Chem 289(24):16688-16698.
74. Nivarthi UK, et al. (2014) An extensive antigenic footprint underpins immunodominant TCR adaptability against a hypervariable viral determinant. J Immunol 193(11):5402-5413.
75. Ladell K, et al. (2013) A molecular basis for the control of preimmune escape variants by HIV-specific CD8+ T cells. Immunity 38(3):425-436.
76. Shimizu A, et al. (2013) Structure of TCR and antigen complexes at an immunodominant CTL epitope in HIV-1 infection. Sci Rep 3:3097.
77. Gras S, et al. (2012) A structural basis for varied αβ TCR usage against an immunodominant EBV antigen restricted to a HLA-B8 molecule. J Immunol 188(1): 311-321.
78. Macdonald WA, et al. (2009) T cell allorecognition via molecular mimicry. Immunity 31(6):897-908.
79. Gras S, et al. (2009) The shaping of T cell receptor recognition by self-tolerance. Immunity 30(2):193-203.
80. Stewart-Jones GB, et al. (2012) Structural features underlying T-cell receptor sensitivity to concealed MHC class I micropolymorphisms. Proc Natl Acad Sci USA 109(50): E3483-E3492.
81. Archbold JK, et al. (2009) Natural micropolymorphism in human leukocyte antigens provides a basis for genetic control of antigen recognition. J Exp Med 206(1):209-219.
82. Tynan FE, et al. (2007) A T cell receptor flattens a bulged antigenic peptide presented by a major histocompatibility complex class I molecule. Nat Immunol 8(3):268-276.
83. Tynan FE, et al. (2005) T cell receptor recognition of a "super-bulged" major histocompatibility complex class I-bound peptide. Nat Immunol 6(11):1114-1122.