3dxa › Citations

Natural micropolymorphism in human leukocyte antigens provides a basis for genetic control of antigen recognition.

Figure 1.
Figure 2.
Figure 3.
Archbold JK, Macdonald WA, Gras S, Ely LK, Miles JJ, Bell MJ, Brennan RM, Beddoe T, Wilce MC, Clements CS, Purcell AW, McCluskey J, Burrows SR, Rossjohn J
OpenAccess logo J Exp Med 206 209-19 (2009)
Related entries: 3dx6, 3dx7, 3dx8, 3dx9

Cited: 75 times
EuropePMC logo PMID: 19139173

Abstract

Human leukocyte antigen (HLA) gene polymorphism plays a critical role in protective immunity, disease susceptibility, autoimmunity, and drug hypersensitivity, yet the basis of how HLA polymorphism influences T cell receptor (TCR) recognition is unclear. We examined how a natural micropolymorphism in HLA-B44, an important and large HLA allelic family, affected antigen recognition. T cell-mediated immunity to an Epstein-Barr virus determinant (EENLLDFVRF) is enhanced when HLA-B*4405 was the presenting allotype compared with HLA-B*4402 or HLA-B*4403, each of which differ by just one amino acid. The micropolymorphism in these HLA-B44 allotypes altered the mode of binding and dynamics of the bound viral epitope. The structure of the TCR-HLA-B*4405(EENLLDFVRF) complex revealed that peptide flexibility was a critical parameter in enabling preferential engagement with HLA-B*4405 in comparison to HLA-B*4402/03. Accordingly, major histocompatibility complex (MHC) polymorphism can alter the dynamics of the peptide-MHC landscape, resulting in fine-tuning of T cell responses between closely related allotypes.

Reviews - 3dxa mentioned but not cited (4)

  1. Coevolution of T-cell receptors with MHC and non-MHC ligands. Castro CD, Luoma AM, Adams EJ. Immunol Rev 267 30-55 (2015)
  2. 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)
  3. TCR Recognition of Peptide-MHC-I: Rule Makers and Breakers. Szeto C, Lobos CA, Nguyen AT, Gras S. Int J Mol Sci 22 (2020)
  4. The perception and response of T cells to a changing environment are based on the law of initial value. Huseby ES, Teixeiro E. Sci Signal 15 eabj9842 (2022)

Articles - 3dxa mentioned but not cited (13)

  1. Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Burrows SR, Chen Z, Archbold JK, Tynan FE, Beddoe T, Kjer-Nielsen L, Miles JJ, Khanna R, Moss DJ, Liu YC, Gras S, Kostenko L, Brennan RM, Clements CS, Brooks AG, Purcell AW, McCluskey J, Rossjohn J. Proc Natl Acad Sci U S A 107 10608-10613 (2010)
  2. Natural micropolymorphism in human leukocyte antigens provides a basis for genetic control of antigen recognition. Archbold JK, Macdonald WA, Gras S, Ely LK, Miles JJ, Bell MJ, Brennan RM, Beddoe T, Wilce MC, Clements CS, Purcell AW, McCluskey J, Burrows SR, Rossjohn J. J Exp Med 206 209-219 (2009)
  3. A single T cell receptor bound to major histocompatibility complex class I and class II glycoproteins reveals switchable TCR conformers. Yin L, Huseby E, Scott-Browne J, Rubtsova K, Pinilla C, Crawford F, Marrack P, Dai S, Kappler JW. Immunity 35 23-33 (2011)
  4. Human T cell receptor occurrence patterns encode immune history, genetic background, and receptor specificity. DeWitt WS, Smith A, Schoch G, Hansen JA, Matsen FA, Bradley P. Elife 7 e38358 (2018)
  5. 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)
  6. Towards a better understanding of the novel avian-origin H7N9 influenza A virus in China. Wang Y, Dai Z, Cheng H, Liu Z, Pan Z, Deng W, Gao T, Li X, Yao Y, Ren J, Xue Y. Sci Rep 3 2318 (2013)
  7. 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)
  8. Quantitative Analysis of the Association Angle between T-cell Receptor Vα/Vβ Domains Reveals Important Features for Epitope Recognition. Hoffmann T, Krackhardt AM, Antes I. PLoS Comput Biol 11 e1004244 (2015)
  9. T-cell receptors binding orientation over peptide/MHC class I is driven by long-range interactions. Ferber M, Zoete V, Michielin O. PLoS One 7 e51943 (2012)
  10. Molecular docking analysis of 2009-H1N1 and 2004-H5N1 influenza virus HLA-B*4405-restricted HA epitope candidates: implications for TCR cross-recognition and vaccine development. Su CT, Schönbach C, Kwoh CK. BMC Bioinformatics 14 Suppl 2 S21 (2013)
  11. Development of immune-specific interaction potentials and their application in the multi-agent-system VaccImm. Woelke AL, von Eichborn J, Murgueitio MS, Worth CL, Castiglione F, Preissner R. PLoS One 6 e23257 (2011)
  12. Interactions of 3-deoxyanthocyanins with gum arabic and sodium alginate contributing to improved pigment aqueous stability. Herrman DA, Brantsen JF, Awika JM. Food Chem 372 131233 (2022)
  13. Structural Basis for Unusual TCR CDR3β Usage Against an Immunodominant HIV-1 Gag Protein Peptide Restricted to an HLA-B*81:01 Molecule. Liu Y, Lei J, San D, Yang Y, Paek C, Xia Z, Chen Y, Yin L. Front Immunol 13 822210 (2022)


Reviews citing this publication (13)

  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. Recognition of CD1d-restricted antigens by natural killer T cells. Rossjohn J, Pellicci DG, Patel O, Gapin L, Godfrey DI. Nat Rev Immunol 12 845-857 (2012)
  3. HLA and infectious diseases. Blackwell JM, Jamieson SE, Burgner D. Clin Microbiol Rev 22 370-85, Table of Contents (2009)
  4. Drug hypersensitivity and human leukocyte antigens of the major histocompatibility complex. Bharadwaj M, Illing P, Theodossis A, Purcell AW, Rossjohn J, McCluskey J. Annu Rev Pharmacol Toxicol 52 401-431 (2012)
  5. Antigen recognition by CD1d-restricted NKT T cell receptors. Godfrey DI, Pellicci DG, Patel O, Kjer-Nielsen L, McCluskey J, Rossjohn J. Semin Immunol 22 61-67 (2010)
  6. 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)
  7. 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)
  8. 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)
  9. Individual and joint action of environmental factors and risk of MS. van der Mei IA, Simpson S, Stankovich J, Taylor BV. Neurol Clin 29 233-255 (2011)
  10. The structural bases of direct T-cell allorecognition: implications for T-cell-mediated transplant rejection. Gras S, Kjer-Nielsen L, Chen Z, Rossjohn J, McCluskey J. Immunol Cell Biol 89 388-395 (2011)
  11. Understanding the complexity and malleability of T-cell recognition. Miles JJ, McCluskey J, Rossjohn J, Gras S. Immunol Cell Biol 93 433-441 (2015)
  12. Crucial Role of Viral Reactivation in the Development of Severe Drug Eruptions: a Comprehensive Review. Shiohara T, Ushigome Y, Kano Y, Takahashi R. Clin Rev Allergy Immunol 49 192-202 (2015)
  13. Understanding human T-cell-mediated immunoregulation through herpesviruses. Burrows SR, Moss DJ, Khanna R. Immunol Cell Biol 89 352-358 (2011)

Articles citing this publication (45)

  1. T cell allorecognition via molecular mimicry. Macdonald WA, Chen Z, Gras S, Archbold JK, Tynan FE, Clements CS, Bharadwaj M, Kjer-Nielsen L, Saunders PM, Wilce MC, Crawford F, Stadinsky B, Jackson D, Brooks AG, Purcell AW, Kappler JW, Burrows SR, Rossjohn J, McCluskey J. Immunity 31 897-908 (2009)
  2. A molecular basis underpinning the T cell receptor heterogeneity of mucosal-associated invariant T cells. Eckle SB, Birkinshaw RW, Kostenko L, Corbett AJ, McWilliam HE, Reantragoon R, Chen Z, Gherardin NA, Beddoe T, Liu L, Patel O, Meehan B, Fairlie DP, Villadangos JA, Godfrey DI, Kjer-Nielsen L, McCluskey J, Rossjohn J. J Exp Med 211 1585-1600 (2014)
  3. T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility. Borbulevych OY, Piepenbrink KH, Gloor BE, Scott DR, Sommese RF, Cole DK, Sewell AK, Baker BM. Immunity 31 885-896 (2009)
  4. Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. Reantragoon R, Kjer-Nielsen L, Patel O, Chen Z, Illing PT, Bhati M, Kostenko L, Bharadwaj M, Meehan B, Hansen TH, Godfrey DI, Rossjohn J, McCluskey J. J Exp Med 209 761-774 (2012)
  5. Contribution of naïve and memory T-cell populations to the human alloimmune response. Macedo C, Orkis EA, Popescu I, Elinoff BD, Zeevi A, Shapiro R, Lakkis FG, Metes D. Am J Transplant 9 2057-2066 (2009)
  6. A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells. Wun KS, Cameron G, Patel O, Pang SS, Pellicci DG, Sullivan LC, Keshipeddy S, Young MH, Uldrich AP, Thakur MS, Richardson SK, Howell AR, Illarionov PA, Brooks AG, Besra GS, McCluskey J, Gapin L, Porcelli SA, Godfrey DI, Rossjohn J. Immunity 34 327-339 (2011)
  7. Oxypurinol directly and immediately activates the drug-specific T cells via the preferential use of HLA-B*58:01. Yun J, Marcaida MJ, Eriksson KK, Jamin H, Fontana S, Pichler WJ, Yerly D. J Immunol 192 2984-2993 (2014)
  8. Common viruses associated with lower pediatric multiple sclerosis risk. Waubant E, Mowry EM, Krupp L, Chitnis T, Yeh EA, Kuntz N, Ness J, Chabas D, Strober J, McDonald J, Belman A, Milazzo M, Gorman M, Weinstock-Guttman B, Rodriguez M, Oksenberg JR, James JA, US Pediatric MS Network. Neurology 76 1989-1995 (2011)
  9. 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)
  10. Peptide length determines the outcome of TCR/peptide-MHCI engagement. Ekeruche-Makinde J, Miles JJ, van den Berg HA, Skowera A, Cole DK, Dolton G, Schauenburg AJ, Tan MP, Pentier JM, Llewellyn-Lacey S, Miles KM, Bulek AM, Clement M, Williams T, Trimby A, Bailey M, Rizkallah P, Rossjohn J, Peakman M, Price DA, Burrows SR, Sewell AK, Wooldridge L. Blood 121 1112-1123 (2013)
  11. Allelic polymorphism in the T cell receptor and its impact on immune responses. Gras S, Chen Z, Miles JJ, Liu YC, Bell MJ, Sullivan LC, Kjer-Nielsen L, Brennan RM, Burrows JM, Neller MA, Khanna R, Purcell AW, Brooks AG, McCluskey J, Rossjohn J, Burrows SR. J Exp Med 207 1555-1567 (2010)
  12. HLA-B*57 Micropolymorphism shapes HLA allele-specific epitope immunogenicity, selection pressure, and HIV immune control. Kloverpris HN, Stryhn A, Harndahl M, van der Stok M, Payne RP, Matthews PC, Chen F, Riddell L, Walker BD, Ndung'u T, Buus S, Goulder P. J Virol 86 919-929 (2012)
  13. Structure of a TCR with high affinity for self-antigen reveals basis for escape from negative selection. Yin Y, Li Y, Kerzic MC, Martin R, Mariuzza RA. EMBO J 30 1137-1148 (2011)
  14. Cross-recognition of HLA DR4 alloantigen by virus-specific CD8+ T cells: a new paradigm for self-/nonself-recognition. Rist M, Smith C, Bell MJ, Burrows SR, Khanna R. Blood 114 2244-2253 (2009)
  15. 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 188 311-321 (2012)
  16. HIV control through a single nucleotide on the HLA-B locus. Kløverpris HN, Harndahl M, Leslie AJ, Carlson JM, Ismail N, van der Stok M, Huang KH, Chen F, Riddell L, Steyn D, Goedhals D, van Vuuren C, Frater J, Walker BD, Carrington M, Ndung'u T, Buus S, Goulder P. J Virol 86 11493-11500 (2012)
  17. A structural basis for antigen presentation by the MHC class Ib molecule, Qa-1b. Zeng L, Sullivan LC, Vivian JP, Walpole NG, Harpur CM, Rossjohn J, Clements CS, Brooks AG. J Immunol 188 302-310 (2012)
  18. Loss of anti-viral immunity by infection with a virus encoding a cross-reactive pathogenic epitope. Chen AT, Cornberg M, Gras S, Guillonneau C, Rossjohn J, Trees A, Emonet S, de la Torre JC, Welsh RM, Selin LK. PLoS Pathog 8 e1002633 (2012)
  19. Position 156 influences the peptide repertoire and tapasin dependency of human leukocyte antigen B*44 allotypes. Badrinath S, Saunders P, Huyton T, Aufderbeck S, Hiller O, Blasczyk R, Bade-Doeding C. Haematologica 97 98-106 (2012)
  20. Specific roles of each TCR hemichain in generating functional chain-centric TCR. Nakatsugawa M, Yamashita Y, Ochi T, Tanaka S, Chamoto K, Guo T, Butler MO, Hirano N. J Immunol 194 3487-3500 (2015)
  21. Alloreactivity is limited by the endogenous peptide repertoire. Morris GP, Ni PP, Allen PM. Proc Natl Acad Sci U S A 108 3695-3700 (2011)
  22. CD8+ TCR repertoire formation is guided primarily by the peptide component of the antigenic complex. Koning D, Costa AI, Hoof I, Miles JJ, Nanlohy NM, Ladell K, Matthews KK, Venturi V, Schellens IM, Borghans JA, Kesmir C, Price DA, van Baarle D. J Immunol 190 931-939 (2013)
  23. Structural and Biochemical Analyses of Swine Major Histocompatibility Complex Class I Complexes and Prediction of the Epitope Map of Important Influenza A Virus Strains. Fan S, Wu Y, Wang S, Wang Z, Jiang B, Liu Y, Liang R, Zhou W, Zhang N, Xia C. J Virol 90 6625-6641 (2016)
  24. 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)
  25. A comprehensive analysis of peptides presented by HLA-A1. Giam K, Ayala-Perez R, Illing PT, Schittenhelm RB, Croft NP, Purcell AW, Dudek NL. Tissue Antigens 85 492-496 (2015)
  26. 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)
  27. High frequency of herpesvirus-specific clonotypes in the human T cell repertoire can remain stable over decades with minimal turnover. Neller MA, Burrows JM, Rist MJ, Miles JJ, Burrows SR. J Virol 87 697-700 (2013)
  28. Structural features underlying T-cell receptor sensitivity to concealed MHC class I micropolymorphisms. Stewart-Jones GB, Simpson P, van der Merwe PA, Easterbrook P, McMichael AJ, Rowland-Jones SL, Jones EY, Gillespie GM. Proc Natl Acad Sci U S A 109 E3483-92 (2012)
  29. 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)
  30. The molecular basis for peptide repertoire selection in the human leucocyte antigen (HLA) C*06:02 molecule. Mobbs JI, Illing PT, Dudek NL, Brooks AG, Baker DG, Purcell AW, Rossjohn J, Vivian JP. J Biol Chem 292 17203-17215 (2017)
  31. The molecular basis of how buried human leukocyte antigen polymorphism modulates natural killer cell function. Saunders PM, MacLachlan BJ, Pymm P, Illing PT, Deng Y, Wong SC, Oates CVL, Purcell AW, Rossjohn J, Vivian JP, Brooks AG. Proc Natl Acad Sci U S A 117 11636-11647 (2020)
  32. The structure and stability of the monomorphic HLA-G are influenced by the nature of the bound peptide. Walpole NG, Kjer-Nielsen L, Kostenko L, McCluskey J, Brooks AG, Rossjohn J, Clements CS. J Mol Biol 397 467-480 (2010)
  33. Insights into the structure of the LC13 TCR/HLA-B8-EBV peptide complex with molecular dynamics simulations. Stavrakoudis A. Cell Biochem Biophys 60 283-295 (2011)
  34. Molecular imprint of exposure to naturally occurring genetic variants of human cytomegalovirus on the T cell repertoire. Smith C, Gras S, Brennan RM, Bird NL, Valkenburg SA, Twist KA, Burrows JM, Miles JJ, Chambers D, Bell S, Campbell S, Kedzierska K, Burrows SR, Rossjohn J, Khanna R. Sci Rep 4 3993 (2014)
  35. Characterization of conserved CDR3 sequence of TCR alpha- and beta-chain genes in peripheral blood T-cells from patients with diffuse large B-cell lymphoma. Yin Q, Tan H, Chen S, Yang L, Ye J, Li Y. Hematology 15 48-57 (2010)
  36. Impact of HLA-B*35 subtype differences on HIV disease outcome in Mexico. Juarez-Molina CI, Valenzuela-Ponce H, Avila-Rios S, Garrido-Rodriguez D, Garcia-Tellez T, Soto-Nava M, Garcia-Morales C, Goulder P, Reyes-Teran G. AIDS 28 1687-1690 (2014)
  37. Structural and functional correlates of enhanced antiviral immunity generated by heteroclitic CD8 T cell epitopes. Trujillo JA, Gras S, Twist KA, Croft NP, Channappanavar R, Rossjohn J, Purcell AW, Perlman S. J Immunol 192 5245-5256 (2014)
  38. Structure of Staphylococcal Enterotoxin E in Complex with TCR Defines the Role of TCR Loop Positioning in Superantigen Recognition. Rödström KE, Regenthal P, Lindkvist-Petersson K. PLoS One 10 e0131988 (2015)
  39. Novel HLA class I associations with HIV-1 control in a unique genetically admixed population. Valenzuela-Ponce H, Alva-Hernández S, Garrido-Rodríguez D, Soto-Nava M, García-Téllez T, Escamilla-Gómez T, García-Morales C, Quiroz-Morales VS, Tapia-Trejo D, Del Arenal-Sánchez S, Prado-Galbarro FJ, Hernández-Juan R, Rodríguez-Aguirre E, Murakami-Ogasawara A, Mejía-Villatoro C, Escobar-Urias IY, Pinzón-Meza R, Pascale JM, Zaldivar Y, Porras-Cortés G, Quant-Durán C, Lorenzana I, Meza RI, Palou EY, Manzanero M, Cedillos RA, Aláez C, Brockman MA, Harrigan PR, Brumme CJ, Brumme ZL, Ávila-Ríos S, Reyes-Terán G, Mesoamerican HIV Project Group. Sci Rep 8 6111 (2018)
  40. Understanding TR binding to pMHC complexes: how does a TR scan many pMHC complexes yet preferentially bind to one. Khan JM, Ranganathan S. PLoS One 6 e17194 (2011)
  41. A high-resolution HLA reference panel capturing global population diversity enables multi-ancestry fine-mapping in HIV host response. Luo Y, Kanai M, Choi W, Li X, Sakaue S, Yamamoto K, Ogawa K, Gutierrez-Arcelus M, Gregersen PK, Stuart PE, Elder JT, Forer L, Schönherr S, Fuchsberger C, Smith AV, Fellay J, Carrington M, Haas DW, Guo X, Palmer ND, Chen YI, Rotter JI, Taylor KD, Rich SS, Correa A, Wilson JG, Kathiresan S, Cho MH, Metspalu A, Esko T, Okada Y, Han B, NHLBI Trans-Omics for Precision Medicine (TOPMed) Consortium, McLaren PJ, Raychaudhuri S. Nat Genet 53 1504-1516 (2021)
  42. Cis-trans isomerization of the Epstein-Barr virus determinant peptide EENLLDFVRF after the DM1 TCR recognition of the HLA-B*4405/peptide complex. Stavrakoudis A. FEBS Lett 585 485-491 (2011)
  43. T-cell epitopes predicted from the Nucleocapsid protein of Sin Nombre virus restricted to 30 HLA alleles common to the North American population. Sankar S, Ramamurthy M, Nandagopal B, Sridharan G. Bioinformation 13 94-100 (2017)
  44. The same major histocompatibility complex polymorphism involved in control of HIV influences peptide binding in the mouse H-2Ld system. Narayanan S, Kranz DM. J Biol Chem 288 31784-31794 (2013)
  45. The Dynamics of the Human Leukocyte Antigen Head Domain Modulates Its Recognition by the T-Cell Receptor. García-Guerrero E, Pérez-Simón JA, Sánchez-Abarca LI, Díaz-Moreno I, De la Rosa MA, Díaz-Quintana A. PLoS One 11 e0154219 (2016)


Quick links