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Structural Mechanism Underpinning Cross-reactivity of a CD8+ T-cell Clone That Recognizes a Peptide Derived from Human Telomerase Reverse Transcriptase.

Cole DK, van den Berg HA, Lloyd A, Crowther MD, Beck K, Ekeruche-Makinde J, Miles JJ, Bulek AM, Dolton G, Schauenburg AJ, Wall A, Fuller A, Clement M, Laugel B, Rizkallah PJ, Wooldridge L, Sewell AK
J Biol Chem 292 802-813 (2017)
Related entries: 5meo, 5mep, 5meq, 5mer

Cited: 18 times
EuropePMC logo PMID: 27903649

Abstract

T-cell cross-reactivity is essential for effective immune surveillance but has also been implicated as a pathway to autoimmunity. Previous studies have demonstrated that T-cell receptors (TCRs) that focus on a minimal motif within the peptide are able to facilitate a high level of T-cell cross-reactivity. However, the structural database shows that most TCRs exhibit less focused antigen binding involving contact with more peptide residues. To further explore the structural features that allow the clonally expressed TCR to functionally engage with multiple peptide-major histocompatibility complexes (pMHCs), we examined the ILA1 CD8+ T-cell clone that responds to a peptide sequence derived from human telomerase reverse transcriptase. The ILA1 TCR contacted its pMHC with a broad peptide binding footprint encompassing spatially distant peptide residues. Despite the lack of focused TCR-peptide binding, the ILA1 T-cell clone was still cross-reactive. Overall, the TCR-peptide contacts apparent in the structure correlated well with the level of degeneracy at different peptide positions. Thus, the ILA1 TCR was less tolerant of changes at peptide residues that were at, or adjacent to, key contact sites. This study provides new insights into the molecular mechanisms that control T-cell cross-reactivity with important implications for pathogen surveillance, autoimmunity, and transplant rejection.

Reviews - 5men mentioned but not cited (1)

  1. 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)

Articles - 5men mentioned but not cited (4)

  1. 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)
  2. Structural Mechanism Underpinning Cross-reactivity of a CD8+ T-cell Clone That Recognizes a Peptide Derived from Human Telomerase Reverse Transcriptase. Cole DK, van den Berg HA, Lloyd A, Crowther MD, Beck K, Ekeruche-Makinde J, Miles JJ, Bulek AM, Dolton G, Schauenburg AJ, Wall A, Fuller A, Clement M, Laugel B, Rizkallah PJ, Wooldridge L, Sewell AK. J Biol Chem 292 802-813 (2017)
  3. Molecular Rules Underpinning Enhanced Affinity Binding of Human T Cell Receptors Engineered for Immunotherapy. Crean RM, MacLachlan BJ, Madura F, Whalley T, Rizkallah PJ, Holland CJ, McMurran C, Harper S, Godkin A, Sewell AK, Pudney CR, van der Kamp MW, Cole DK. Mol Ther Oncolytics 18 443-456 (2020)
  4. Thermal Stability of Heterotrimeric pMHC Proteins as Determined by Circular Dichroism Spectroscopy. Fuller A, Wall A, Crowther MD, Lloyd A, Zhurov A, Sewell AK, Cole DK, Beck K. Bio Protoc 7 e2366 (2017)


Reviews citing this publication (3)

  1. T-cell-receptor cross-recognition and strategies to select safe T-cell receptors for clinical translation. Bentzen AK, Hadrup SR. Immunooncol Technol 2 1-10 (2019)
  2. Engineering soluble T-cell receptors for therapy. Robinson RA, McMurran C, McCully ML, Cole DK. FEBS J 288 6159-6173 (2021)
  3. Conserved Binding Regions Provide the Clue for Peptide-Based Vaccine Development: A Chemical Perspective. Curtidor H, Reyes C, Bermúdez A, Vanegas M, Varela Y, Patarroyo ME. Molecules 22 E2199 (2017)

Articles citing this publication (10)

  1. Optimized Peptide-MHC Multimer Protocols for Detection and Isolation of Autoimmune T-Cells. Dolton G, Zervoudi E, Rius C, Wall A, Thomas HL, Fuller A, Yeo L, Legut M, Wheeler S, Attaf M, Chudakov DM, Choy E, Peakman M, Sewell AK. Front Immunol 9 1378 (2018)
  2. Specificity of bispecific T cell receptors and antibodies targeting peptide-HLA. Holland CJ, Crean RM, Pentier JM, de Wet B, Lloyd A, Srikannathasan V, Lissin N, Lloyd KA, Blicher TH, Conroy PJ, Hock M, Pengelly RJ, Spinner TE, Cameron B, Potter EA, Jeyanthan A, Molloy PE, Sami M, Aleksic M, Liddy N, Robinson RA, Harper S, Lepore M, Pudney CR, van der Kamp MW, Rizkallah PJ, Jakobsen BK, Vuidepot A, Cole DK. J Clin Invest 130 2673-2688 (2020)
  3. Affinity-enhanced T-cell receptors for adoptive T-cell therapy targeting MAGE-A10: strategy for selection of an optimal candidate. Border EC, Sanderson JP, Weissensteiner T, Gerry AB, Pumphrey NJ. Oncoimmunology 8 e1532759 (2019)
  4. In Silico and Structural Analyses Demonstrate That Intrinsic Protein Motions Guide T Cell Receptor Complementarity Determining Region Loop Flexibility. Holland CJ, MacLachlan BJ, Bianchi V, Hesketh SJ, Morgan R, Vickery O, Bulek AM, Fuller A, Godkin A, Sewell AK, Rizkallah PJ, Wells S, Cole DK. Front Immunol 9 674 (2018)
  5. TCR-induced alteration of primary MHC peptide anchor residue. Madura F, Rizkallah PJ, Legut M, Holland CJ, Fuller A, Bulek A, Schauenburg AJ, Trimby A, Hopkins JR, Wells SA, Godkin A, Miles JJ, Sami M, Li Y, Liddy N, Jakobsen BK, Loveridge EJ, Cole DK, Sewell AK. Eur J Immunol 49 1052-1066 (2019)
  6. T cell receptor interactions with human leukocyte antigen govern indirect peptide selectivity for the cancer testis antigen MAGE-A4. Coles CH, McMurran C, Lloyd A, Hock M, Hibbert L, Raman MCC, Hayes C, Lupardus P, Cole DK, Harper S. J Biol Chem 295 11486-11494 (2020)
  7. T cells targeted to TdT kill leukemic lymphoblasts while sparing normal lymphocytes. Ali M, Giannakopoulou E, Li Y, Lehander M, Virding Culleton S, Yang W, Knetter C, Odabasi MC, Bollineni RC, Yang X, Foldvari Z, Böschen ML, Taraldsrud E, Strønen E, Toebes M, Hillen A, Mazzi S, de Ru AH, Janssen GMC, Kolstad A, Tjønnfjord GE, Lie BA, Griffioen M, Lehmann S, Osnes LT, Buechner J, Garcia KC, Schumacher TN, van Veelen PA, Leisegang M, Jacobsen SEW, Woll P, Olweus J. Nat Biotechnol 40 488-498 (2022)
  8. CD8 coreceptor-mediated focusing can reorder the agonist hierarchy of peptide ligands recognized via the T cell receptor. Clement M, Knezevic L, Dockree T, McLaren JE, Ladell K, Miners KL, Llewellyn-Lacey S, Rubina A, Francis O, Cole DK, Sewell AK, Bridgeman JS, Price DA, van den Berg HA, Wooldridge L. Proc Natl Acad Sci U S A 118 e2019639118 (2021)
  9. Peptide cargo tunes a network of correlated motions in human leucocyte antigens. Hopkins JR, Crean RM, Catici DAM, Sewell AK, Arcus VL, Van der Kamp MW, Cole DK, Pudney CR. FEBS J 287 3777-3793 (2020)
  10. Structural insights into engineering a T-cell receptor targeting MAGE-A10 with higher affinity and specificity for cancer immunotherapy. Simister PC, Border EC, Vieira JF, Pumphrey NJ. J Immunother Cancer 10 e004600 (2022)


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