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Structural bases for the affinity-driven selection of a public TCR against a dominant human cytomegalovirus epitope.

Gras S, Saulquin X, Reiser JB, Debeaupuis E, Echasserieau K, Kissenpfennig A, Legoux F, Chouquet A, Le Gorrec M, Machillot P, Neveu B, Thielens N, Malissen B, Bonneville M, Housset D
J Immunol 183 430-7 (2009)
Related entries: 3gsn, 3gso, 3gsq, 3gsu, 3gsv, 3gsw, 3gsx

Cited: 59 times
EuropePMC logo PMID: 19542454

Abstract

Protective T cell responses elicited along chronic human CMV (HCMV) infections are sometimes dominated by CD8 T cell clones bearing highly related or identical public TCR in unrelated individuals. To understand the principles that guide emergence of these public T cell responses, we have performed structural, biophysical, and functional analyses of an immunodominant public TCR (RA14) directed against a major HLA-A*0201-restricted HCMV Ag (pp65(495-503)) and selected in vivo from a diverse repertoire after chronic stimulations. Unlike the two immunodominant public TCRs crystallized so far, which focused on one peptide hotspot, the HCMV-specific RA14 TCR interacts with the full array of available peptide residues. The conservation of some peptide-MHC complex-contacting amino acids by lower-affinity TCRs suggests a shared TCR-peptide-MHC complex docking mode and supports an Ag-driven selection of optimal TCRs. Therefore, the emergence of a public TCR of an oligoclonal Ag-specific response after repeated viral stimulations is based on a receptor displaying a high structural complementarity with the entire peptide and focusing on three peptide hotspots. This highlights key parameters underlying the selection of a protective T cell response against HCMV infection, which remains a major health issue in patients undergoing bone marrow transplantation.

Articles - 3gsr mentioned but not cited (4)

  1. 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)
  2. Predicting HLA class I non-permissive amino acid residues substitutions. Binkowski TA, Marino SR, Joachimiak A. PLoS One 7 e41710 (2012)
  3. Human Cytomegalovirus variant peptides adapt by decreasing their total coordination upon binding to a T cell receptor. Antipas GS, Germenis AE. Data Brief 4 492-499 (2015)
  4. Snowflake: A deep learning-based human leukocyte antigen matching algorithm considering allele-specific surface accessibility. Niemann M, Matern BM, Spierings E. Front Immunol 13 937587 (2022)


Reviews citing this publication (9)

  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. Bias in the αβ T-cell repertoire: implications for disease pathogenesis and vaccination. Miles JJ, Douek DC, Price DA. Immunol Cell Biol 89 375-387 (2011)
  3. Structural and biophysical determinants of αβ T-cell antigen recognition. Bridgeman JS, Sewell AK, Miles JJ, Price DA, Cole DK. Immunology 135 9-18 (2012)
  4. 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)
  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. Understanding the complexity and malleability of T-cell recognition. Miles JJ, McCluskey J, Rossjohn J, Gras S. Immunol Cell Biol 93 433-441 (2015)
  7. Main Strategies for the Identification of Neoantigens. Gopanenko AV, Kosobokova EN, Kosorukov VS. Cancers (Basel) 12 E2879 (2020)
  8. 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)
  9. TCR Recognition of Peptide-MHC-I: Rule Makers and Breakers. Szeto C, Lobos CA, Nguyen AT, Gras S. Int J Mol Sci 22 (2020)

Articles citing this publication (46)

  1. MR1 presents microbial vitamin B metabolites to MAIT cells. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, Bhati M, Chen Z, Kostenko L, Reantragoon R, Williamson NA, Purcell AW, Dudek NL, McConville MJ, O'Hair RA, Khairallah GN, Godfrey DI, Fairlie DP, Rossjohn J, McCluskey J. Nature 491 717-723 (2012)
  2. Structural basis for the killing of human beta cells by CD8(+) T cells in type 1 diabetes. Bulek AM, Cole DK, Skowera A, Dolton G, Gras S, Madura F, Fuller A, Miles JJ, Gostick E, Price DA, Drijfhout JW, Knight RR, Huang GC, Lissin N, Molloy PE, Wooldridge L, Jakobsen BK, Rossjohn J, Peakman M, Rizkallah PJ, Sewell AK. Nat Immunol 13 283-289 (2012)
  3. T cell receptor αβ diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Wang GC, Dash P, McCullers JA, Doherty PC, Thomas PG. Sci Transl Med 4 128ra42 (2012)
  4. Genetic and structural basis for selection of a ubiquitous T cell receptor deployed in Epstein-Barr virus infection. Miles JJ, Bulek AM, Cole DK, Gostick E, Schauenburg AJ, Dolton G, Venturi V, Davenport MP, Tan MP, Burrows SR, Wooldridge L, Price DA, Rizkallah PJ, Sewell AK. PLoS Pathog 6 e1001198 (2010)
  5. Molecular basis for universal HLA-A*0201-restricted CD8+ T-cell immunity against influenza viruses. Valkenburg SA, Josephs TM, Clemens EB, Grant EJ, Nguyen TH, Wang GC, Price DA, Miller A, Tong SY, Thomas PG, Doherty PC, Rossjohn J, Gras S, Kedzierska K. Proc Natl Acad Sci U S A 113 4440-4445 (2016)
  6. Conformational melding permits a conserved binding geometry in TCR recognition of foreign and self molecular mimics. Borbulevych OY, Piepenbrink KH, Baker BM. J Immunol 186 2950-2958 (2011)
  7. Sequence and Structural Analyses Reveal Distinct and Highly Diverse Human CD8+ TCR Repertoires to Immunodominant Viral Antigens. Chen G, Yang X, Ko A, Sun X, Gao M, Zhang Y, Shi A, Mariuzza RA, Weng NP. Cell Rep 19 569-583 (2017)
  8. Degenerate T-cell recognition of peptides on MHC molecules creates large holes in the T-cell repertoire. Calis JJ, de Boer RJ, Keşmir C. PLoS Comput Biol 8 e1002412 (2012)
  9. 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)
  10. Naive CD8⁺ T-cell precursors display structured TCR repertoires and composite antigen-driven selection dynamics. Neller MA, Ladell K, McLaren JE, Matthews KK, Gostick E, Pentier JM, Dolton G, Schauenburg AJ, Koning D, Fontaine Costa AI, Watkins TS, Venturi V, Smith C, Khanna R, Miners K, Clement M, Wooldridge L, Cole DK, van Baarle D, Sewell AK, Burrows SR, Price DA, Miles JJ. Immunol Cell Biol 93 625-633 (2015)
  11. Structural basis for enabling T-cell receptor diversity within biased virus-specific CD8+ T-cell responses. Day EB, Guillonneau C, Gras S, La Gruta NL, Vignali DA, Doherty PC, Purcell AW, Rossjohn J, Turner SJ. Proc Natl Acad Sci U S A 108 9536-9541 (2011)
  12. T-cell receptor specificity maintained by altered thermodynamics. Madura F, Rizkallah PJ, Miles KM, Holland CJ, Bulek AM, Fuller A, Schauenburg AJ, Miles JJ, Liddy N, Sami M, Li Y, Hossain M, Baker BM, Jakobsen BK, Sewell AK, Cole DK. J Biol Chem 288 18766-18775 (2013)
  13. 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)
  14. Identification of SARS-CoV-2 Vaccine Epitopes Predicted to Induce Long-Term Population-Scale Immunity. Yarmarkovich M, Warrington JM, Farrel A, Maris JM. Cell Rep Med 1 100036 (2020)
  15. Single insulin-specific CD8+ T cells show characteristic gene expression profiles in human type 1 diabetes. Luce S, Lemonnier F, Briand JP, Coste J, Lahlou N, Muller S, Larger E, Rocha B, Mallone R, Boitard C. Diabetes 60 3289-3299 (2011)
  16. Minimal conformational plasticity enables TCR cross-reactivity to different MHC class II heterodimers. Holland CJ, Rizkallah PJ, Vollers S, Calvo-Calle JM, Madura F, Fuller A, Sewell AK, Stern LJ, Godkin A, Cole DK. Sci Rep 2 629 (2012)
  17. Public TCR use by herpes simplex virus-2-specific human CD8 CTLs. Dong L, Li P, Oenema T, McClurkan CL, Koelle DM. J Immunol 184 3063-3071 (2010)
  18. 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)
  19. Quantitative Prediction of the Landscape of T Cell Epitope Immunogenicity in Sequence Space. Ogishi M, Yotsuyanagi H. Front Immunol 10 827 (2019)
  20. Broad CD8+ T cell cross-recognition of distinct influenza A strains in humans. Grant EJ, Josephs TM, Loh L, Clemens EB, Sant S, Bharadwaj M, Chen W, Rossjohn J, Gras S, Kedzierska K. Nat Commun 9 5427 (2018)
  21. Germline bias dictates cross-serotype reactivity in a common dengue-virus-specific CD8+ T cell response. Culshaw A, Ladell K, Gras S, McLaren JE, Miners KL, Farenc C, van den Heuvel H, Gostick E, Dejnirattisai W, Wangteeraprasert A, Duangchinda T, Chotiyarnwong P, Limpitikul W, Vasanawathana S, Malasit P, Dong T, Rossjohn J, Mongkolsapaya J, Price DA, Screaton GR. Nat Immunol 18 1228-1237 (2017)
  22. TCR-mimic bispecific antibodies targeting LMP2A show potent activity against EBV malignancies. Ahmed M, Lopez-Albaitero A, Pankov D, Santich BH, Liu H, Yan S, Xiang J, Wang P, Hasan AN, Selvakumar A, O'Reilly RJ, Liu C, Cheung NV. JCI Insight 3 (2018)
  23. An extensive antigenic footprint underpins immunodominant TCR adaptability against a hypervariable viral determinant. Nivarthi UK, Gras S, Kjer-Nielsen L, Berry R, Lucet IS, Miles JJ, Tracy SL, Purcell AW, Bowden DS, Hellard M, Rossjohn J, McCluskey J, Bharadwaj M. J Immunol 193 5402-5413 (2014)
  24. Partial Dissociation of Truncated Peptides Influences the Structural Dynamics of the MHCI Binding Groove. Fisette O, Wingbermühle S, Schäfer LV. Front Immunol 8 408 (2017)
  25. TCRs with Distinct Specificity Profiles Use Different Binding Modes to Engage an Identical Peptide-HLA Complex. Coles CH, Mulvaney RM, Malla S, Walker A, Smith KJ, Lloyd A, Lowe KL, McCully ML, Martinez Hague R, Aleksic M, Harper J, Paston SJ, Donnellan Z, Chester F, Wiederhold K, Robinson RA, Knox A, Stacey AR, Dukes J, Baston E, Griffin S, Jakobsen BK, Vuidepot A, Harper S. J Immunol 204 1943-1953 (2020)
  26. Analysis of relationships between peptide/MHC structural features and naive T cell frequency in humans. Reiser JB, Legoux F, Gras S, Trudel E, Chouquet A, Léger A, Le Gorrec M, Machillot P, Bonneville M, Saulquin X, Housset D. J Immunol 193 5816-5826 (2014)
  27. Lack of Heterologous Cross-reactivity toward HLA-A*02:01 Restricted Viral Epitopes Is Underpinned by Distinct αβT Cell Receptor Signatures. Grant EJ, Josephs TM, Valkenburg SA, Wooldridge L, Hellard M, Rossjohn J, Bharadwaj M, Kedzierska K, Gras S. J Biol Chem 291 24335-24351 (2016)
  28. Role of the MHC restriction during maturation of antigen-specific human T cells in the thymus. Hesnard L, Legoux F, Gautreau L, Moyon M, Baron O, Devilder MC, Bonneville M, Saulquin X. Eur J Immunol 46 560-569 (2016)
  29. Targeted suppression of autoreactive CD8+ T-cell activation using blocking anti-CD8 antibodies. Clement M, Pearson JA, Gras S, van den Berg HA, Lissina A, Llewellyn-Lacey S, Willis MD, Dockree T, McLaren JE, Ekeruche-Makinde J, Gostick E, Robertson NP, Rossjohn J, Burrows SR, Price DA, Wong FS, Peakman M, Skowera A, Wooldridge L. Sci Rep 6 35332 (2016)
  30. Immune parameters to consider when choosing T-cell receptors for therapy. Burrows SR, Miles JJ. Front Immunol 4 229 (2013)
  31. Predicting interactions between T cell receptors and MHC-peptide complexes. Roomp K, Domingues FS. Mol Immunol 48 553-562 (2011)
  32. Assessing the capability of in silico mutation protocols for predicting the finite temperature conformation of amino acids. Ochoa R, Soler MA, Laio A, Cossio P. Phys Chem Chem Phys 20 25901-25909 (2018)
  33. Human cytomegalovirus-specific T-cell receptor engineered for high affinity and soluble expression using mammalian cell display. Wagner EK, Qerqez AN, Stevens CA, Nguyen AW, Delidakis G, Maynard JA. J Biol Chem 294 5790-5804 (2019)
  34. DynaDom: structure-based prediction of T cell receptor inter-domain and T cell receptor-peptide-MHC (class I) association angles. Hoffmann T, Marion A, Antes I. BMC Struct Biol 17 2 (2017)
  35. CD8+ T cells specific for an immunodominant SARS-CoV-2 nucleocapsid epitope cross-react with selective seasonal coronaviruses. Lineburg KE, Grant EJ, Swaminathan S, Chatzileontiadou DSM, Szeto C, Sloane H, Panikkar A, Raju J, Crooks P, Rehan S, Nguyen AT, Lekieffre L, Neller MA, Tong ZWM, Jayasinghe D, Chew KY, Lobos CA, Halim H, Burrows JM, Riboldi-Tunnicliffe A, Chen W, D'Orsogna L, Khanna R, Short KR, Smith C, Gras S. Immunity 54 1055-1065.e5 (2021)
  36. Inability To Detect Cross-Reactive Memory T Cells Challenges the Frequency of Heterologous Immunity among Common Viruses. Rowntree LC, Nguyen THO, Halim H, Purcell AW, Rossjohn J, Gras S, Kotsimbos TC, Mifsud NA. J Immunol 200 3993-4003 (2018)
  37. Amino-terminal extended peptide single-chain trimers are potent synthetic agonists for memory human CD8+ T cells. Carreno BM, Becker-Hapak M, Chan M, Lie WR, Wang X, Hansen TH, Linette GP. J Immunol 188 5839-5849 (2012)
  38. Assessing Anti-HCMV Cell Mediated Immune Responses in Transplant Recipients and Healthy Controls Using a Novel Functional Assay. Houldcroft CJ, Jackson SE, Lim EY, Sedikides GX, Davies EL, Atkinson C, McIntosh M, Remmerswaal EBM, Okecha G, Bemelman FJ, Stanton RJ, Reeves M, Wills MR. Front Cell Infect Microbiol 10 275 (2020)
  39. Molecular Basis of a Dominant SARS-CoV-2 Spike-Derived Epitope Presented by HLA-A*02:01 Recognised by a Public TCR. Szeto C, Nguyen AT, Lobos CA, Chatzileontiadou DSM, Jayasinghe D, Grant EJ, Riboldi-Tunnicliffe A, Smith C, Gras S. Cells 10 2646 (2021)
  40. Opening opportunities for Kd determination and screening of MHC peptide complexes. Kopicki JD, Saikia A, Niebling S, Günther C, Anjanappa R, Garcia-Alai M, Springer S, Uetrecht C. Commun Biol 5 488 (2022)
  41. Backbone Modifications of HLA-A2-Restricted Antigens Induce Diverse Binding and T Cell Activation Outcomes. Gibadullin R, Randall CJ, Sidney J, Sette A, Gellman SH. J Am Chem Soc 143 6470-6481 (2021)
  42. Characterization of amino acid residues of T-cell receptors interacting with HLA-A*02-restricted antigen peptides. Zhu Y, Huang C, Su M, Ge Z, Gao L, Shi Y, Wang X, Chen J. Ann Transl Med 9 495 (2021)
  43. Expression, Purification, and Crystallization of the Vγ9Vδ2 T-cell Receptor Recognizing Protein/Peptide Antigens. Cheng C, Zhao Z, Liu G. Protein J 42 778-791 (2023)
  44. Homologous peptides derived from influenza A, B and C viruses induce variable CD8+ T cell responses with cross-reactive potential. Nguyen AT, Lau HMP, Sloane H, Jayasinghe D, Mifsud NA, Chatzileontiadou DS, Grant EJ, Szeto C, Gras S. Clin Transl Immunology 11 e1422 (2022)
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  46. Structural and Mechanistic Implications of Rearrangement Frequencies within Human TCRBV Genes. Yassai MB, Demos W, Gorski J. J Immunol 199 1142-1152 (2017)


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