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A structural basis for varied αβ TCR usage against an immunodominant EBV antigen restricted to a HLA-B8 molecule.

Gras S, Wilmann PG, Chen Z, Halim H, Liu YC, Kjer-Nielsen L, Purcell AW, Burrows SR, McCluskey J, Rossjohn J
J Immunol 188 311-21 (2012)
Related entries: 3sjv, 3skm, 3skn

Cited: 40 times
EuropePMC logo PMID: 22140258

Abstract

EBV is a ubiquitous and persistent human pathogen, kept in check by the cytotoxic T cell response. In this study, we investigated how three TCRs, which differ in their T cell immunodominance hierarchies and gene usage, interact with the same EBV determinant (FLRGRAYGL), bound to the same Ag-presenting molecule, HLA-B8. We found that the three TCRs exhibit differing fine specificities for the viral Ag. Further, via structural and biophysical approaches, we demonstrated that the viral Ag provides the greatest energetic contribution to the TCR-peptide-HLA interaction, while focusing on a few adjacent HLA-based interactions to further tune fine-specificity requirements. Thus, the TCR engages the peptide-HLA with the viral Ag as the main glue, such that neighboring TCR-MHC interactions are recruited as a supportive adhesive. Collectively, we provide a portrait of how the host's adaptive immune response differentially engages a common viral Ag.

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  1. Crystal structures of MHC class I complexes reveal the elusive intermediate conformations explored during peptide editing. Li L, Peng X, Batliwala M, Bouvier M. Nat Commun 14 5020 (2023)
  2. research-article Unusual crystal structures of MHC class I complexes reveal the elusive intermediate conformations explored during peptide editing in antigen presentation. Li L, Peng X, Batliwala M, Bouvier M. Res Sq rs.3.rs-2500847 (2023)


Reviews citing this publication (11)

  1. T cell antigen receptor recognition of antigen-presenting molecules. Rossjohn J, Gras S, Miles JJ, Turner SJ, Godfrey DI, McCluskey J. Annu Rev Immunol 33 169-200 (2015)
  2. Understanding the drivers of MHC restriction of T cell receptors. La Gruta NL, Gras S, Daley SR, Thomas PG, Rossjohn J. Nat Rev Immunol 18 467-478 (2018)
  3. A structural voyage toward an understanding of the MHC-I-restricted immune response: lessons learned and much to be learned. Gras S, Burrows SR, Turner SJ, Sewell AK, McCluskey J, Rossjohn J. Immunol Rev 250 61-81 (2012)
  4. Using T Cell Receptor Repertoires to Understand the Principles of Adaptive Immune Recognition. Bradley P, Thomas PG. Annu Rev Immunol 37 547-570 (2019)
  5. Emerging Concepts in TCR Specificity: Rationalizing and (Maybe) Predicting Outcomes. Singh NK, Riley TP, Baker SCB, Borrman T, Weng Z, Baker BM. J Immunol 199 2203-2213 (2017)
  6. TCR Recognition of Peptide-MHC-I: Rule Makers and Breakers. Szeto C, Lobos CA, Nguyen AT, Gras S. Int J Mol Sci 22 E68 (2020)
  7. Understanding the complexity and malleability of T-cell recognition. Miles JJ, McCluskey J, Rossjohn J, Gras S. Immunol Cell Biol 93 433-441 (2015)
  8. Mechanisms and Consequences of Antigen Presentation by CD1. Van Kaer L, Wu L, Joyce S. Trends Immunol 37 738-754 (2016)
  9. Transplantation tolerance and its outcome during infections and inflammation. Chong AS, Alegre ML. Immunol Rev 258 80-101 (2014)
  10. The versatility of the αβ T-cell antigen receptor. Bhati M, Cole DK, McCluskey J, Sewell AK, Rossjohn J. Protein Sci 23 260-272 (2014)
  11. Predisposed αβ T cell antigen receptor recognition of MHC and MHC-I like molecules? Eckle SB, Turner SJ, Rossjohn J, McCluskey J. Curr Opin Immunol 25 653-659 (2013)

Articles citing this publication (27)

  1. Recognition of CD1d-sulfatide mediated by a type II natural killer T cell antigen receptor. Patel O, Pellicci DG, Gras S, Sandoval-Romero ML, Uldrich AP, Mallevaey T, Clarke AJ, Le Nours J, Theodossis A, Cardell SL, Gapin L, Godfrey DI, Rossjohn J. Nat Immunol 13 857-863 (2012)
  2. T cell receptor reversed polarity recognition of a self-antigen major histocompatibility complex. Beringer DX, Beringer DX, Kleijwegt FS, Wiede F, van der Slik AR, Loh KL, Petersen J, Dudek NL, Duinkerken G, Laban S, Joosten A, Vivian JP, Chen Z, Uldrich AP, Godfrey DI, McCluskey J, Price DA, Radford KJ, Purcell AW, Nikolic T, Reid HH, Tiganis T, Roep BO, Rossjohn J. Nat Immunol 16 1153-1161 (2015)
  3. Hotspot autoimmune T cell receptor binding underlies pathogen and insulin peptide cross-reactivity. Cole DK, Bulek AM, Dolton G, Schauenberg AJ, Szomolay B, Rittase W, Trimby A, Jothikumar P, Fuller A, Skowera A, Rossjohn J, Zhu C, Miles JJ, Peakman M, Wooldridge L, Rizkallah PJ, Sewell AK. J Clin Invest 126 2191-2204 (2016)
  4. Broad TCR repertoire and diverse structural solutions for recognition of an immunodominant CD8+ T cell epitope. Song I, Gil A, Mishra R, Ghersi D, Selin LK, Stern LJ. Nat Struct Mol Biol 24 395-406 (2017)
  5. Naturally processed non-canonical HLA-A*02:01 presented peptides. Hassan C, Chabrol E, Jahn L, Kester MG, de Ru AH, Drijfhout JW, Rossjohn J, Falkenburg JH, Heemskerk MH, Gras S, van Veelen PA. J Biol Chem 290 2593-2603 (2015)
  6. T cell receptor recognition of CD1b presenting a mycobacterial glycolipid. Gras S, Van Rhijn I, Shahine A, Cheng TY, Bhati M, Tan LL, Halim H, Tuttle KD, Gapin L, Le Nours J, Moody DB, Rossjohn J. Nat Commun 7 13257 (2016)
  7. How structural adaptability exists alongside HLA-A2 bias in the human αβ TCR repertoire. Blevins SJ, Pierce BG, Singh NK, Riley TP, Wang Y, Spear TT, Nishimura MI, Weng Z, Baker BM. Proc Natl Acad Sci U S A 113 E1276-85 (2016)
  8. Differential scanning fluorimetry based assessments of the thermal and kinetic stability of peptide-MHC complexes. Hellman LM, Yin L, Wang Y, Blevins SJ, Riley TP, Belden OS, Spear TT, Nishimura MI, Stern LJ, Baker BM. J Immunol Methods 432 95-101 (2016)
  9. Highly divergent T-cell receptor binding modes underlie specific recognition of a bulged viral peptide bound to a human leukocyte antigen class I molecule. Liu YC, Miles JJ, Neller MA, Gostick E, Price DA, Purcell AW, McCluskey J, Burrows SR, Rossjohn J, Gras S. J Biol Chem 288 15442-15454 (2013)
  10. Divergent T-cell receptor recognition modes of a HLA-I restricted extended tumour-associated peptide. Chan KF, Gully BS, Gras S, Beringer DX, Kjer-Nielsen L, Cebon J, McCluskey J, Chen W, Rossjohn J. Nat Commun 9 1026 (2018)
  11. Structural Basis for Clonal Diversity of the Public T Cell Response to a Dominant Human Cytomegalovirus Epitope. Yang X, Gao M, Chen G, Pierce BG, Lu J, Weng NP, Mariuzza RA. J Biol Chem 290 29106-29119 (2015)
  12. Structural basis for oligoclonal T cell recognition of a shared p53 cancer neoantigen. Wu D, Gallagher DT, Gowthaman R, Pierce BG, Mariuzza RA. Nat Commun 11 2908 (2020)
  13. The energetic basis underpinning T-cell receptor recognition of a super-bulged peptide bound to a major histocompatibility complex class I molecule. Liu YC, Chen Z, Burrows SR, Purcell AW, McCluskey J, Rossjohn J, Gras S. J Biol Chem 287 12267-12276 (2012)
  14. Genetic fine mapping of systemic lupus erythematosus MHC associations in Europeans and African Americans. Hanscombe KB, Morris DL, Noble JA, Dilthey AT, Tombleson P, Kaufman KM, Comeau M, Langefeld CD, Alarcon-Riquelme ME, Gaffney PM, Jacob CO, Sivils KL, Tsao BP, Alarcon GS, Brown EE, Croker J, Edberg J, Gilkeson G, James JA, Kamen DL, Kelly JA, McCune J, Merrill JT, Petri M, Ramsey-Goldman R, Reveille JD, Salmon JE, Scofield H, Utset T, Wallace DJ, Weisman MH, Kimberly RP, Harley JB, Lewis CM, Criswell LA, Vyse TJ. Hum Mol Genet 27 3813-3824 (2018)
  15. Novel Flavivirus Antiviral That Targets the Host Nuclear Transport Importin α/β1 Heterodimer. Yang SNY, Atkinson SC, Fraser JE, Wang C, Maher B, Roman N, Forwood JK, Wagstaff KM, Borg NA, Jans DA. Cells 8 E281 (2019)
  16. A molecular basis for the interplay between T cells, viral mutants, and human leukocyte antigen micropolymorphism. Liu YC, Chen Z, Neller MA, Miles JJ, Purcell AW, McCluskey J, Burrows SR, Rossjohn J, Gras S. J Biol Chem 289 16688-16698 (2014)
  17. The contribution of major histocompatibility complex contacts to the affinity and kinetics of T cell receptor binding. Zhang H, Lim HS, Knapp B, Deane CM, Aleksic M, Dushek O, van der Merwe PA. Sci Rep 6 35326 (2016)
  18. A conserved energetic footprint underpins recognition of human leukocyte antigen-E by two distinct αβ T cell receptors. Sullivan LC, Walpole NG, Farenc C, Pietra G, Sum MJW, Clements CS, Lee EJ, Beddoe T, Falco M, Mingari MC, Moretta L, Gras S, Rossjohn J, Brooks AG. J Biol Chem 292 21149-21158 (2017)
  19. CD8+ T cell landscape in Indigenous and non-Indigenous people restricted by influenza mortality-associated HLA-A*24:02 allomorph. Hensen L, Illing PT, Bridie Clemens E, Nguyen THO, Koutsakos M, van de Sandt CE, Mifsud NA, Nguyen AT, Szeto C, Chua BY, Halim H, Rizzetto S, Luciani F, Loh L, Grant EJ, Saunders PM, Brooks AG, Rockman S, Kotsimbos TC, Cheng AC, Richards M, Westall GP, Wakim LM, Loudovaris T, Mannering SI, Elliott M, Tangye SG, Jackson DC, Flanagan KL, Rossjohn J, Gras S, Davies J, Miller A, Tong SYC, Purcell AW, Kedzierska K. Nat Commun 12 2931 (2021)
  20. Analysis of the CDR3 length repertoire and the diversity of T cell receptor α and β chains in swine CD4+ and CD8+ T lymphocytes. Wang CY, Fang YX, Chen GH, Jia HJ, Zeng S, He XB, Feng Y, Li SJ, Jin QW, Cheng WY, Jing ZZ. Mol Med Rep 16 75-86 (2017)
  21. Structures of the MHC-I molecule BF2*1501 disclose the preferred presentation of an H5N1 virus-derived epitope. Li X, Zhang L, Liu Y, Ma L, Zhang N, Xia C. J Biol Chem 295 5292-5306 (2020)
  22. Nα-terminal acetylation for T cell recognition: molecular basis of MHC class I-restricted nα-acetylpeptide presentation. Sun M, Liu J, Qi J, Tefsen B, Shi Y, Yan J, Gao GF. J Immunol 192 5509-5519 (2014)
  23. Overlapping Peptides Elicit Distinct CD8+ T Cell Responses following Influenza A Virus Infection. Assmus LM, Guan J, Wu T, Farenc C, Sng XYX, Zareie P, Nguyen A, Nguyen AT, Tscharke DC, Thomas PG, Rossjohn J, Gras S, Croft NP, Purcell AW, La Gruta NL. J Immunol 205 1731-1742 (2020)
  24. HLA-B*27:05 alters immunodominance hierarchy of universal influenza-specific CD8+ T cells. Sant S, Quiñones-Parra SM, Koutsakos M, Grant EJ, Loudovaris T, Mannering SI, Crowe J, van de Sandt CE, Rimmelzwaan GF, Rossjohn J, Gras S, Loh L, Nguyen THO, Kedzierska K. PLoS Pathog 16 e1008714 (2020)
  25. Crystal structure of the giant panda MHC class I complex: First insights into the viral peptide presentation profile in the bear family. Yuan H, Ma L, Zhang L, Li X, Xia C. Protein Sci 29 2468-2481 (2020)
  26. High Throughput Screening Targeting the Dengue NS3-NS5 Interface Identifies Antivirals against Dengue, Zika and West Nile Viruses. Yang SNY, Maher B, Wang C, Wagstaff KM, Fraser JE, Jans DA. Cells 11 730 (2022)
  27. Employing non-targeted interactomics approach and subcellular fractionation to increase our understanding of the ghost proteome. Garcia-Del Rio DF, Cardon T, Eyckerman S, Fournier I, Bonnefond A, Gevaert K, Salzet M. iScience 26 105943 (2023)


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