Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus

Here, we sequenced rearranged TCRβ and TCRα chain sequences in CD4+CD8+ double positive (DP), CD4+CD8- single positive (SP4) and CD4-CD8+ (SP8) thymocyte populations from the foetus and young adult mouse. We found that life-stage had a greater impact on TCRβ and TCRα gene segment usage than cell-typ...

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Main Authors: Jasmine Rowell, Ching-In Lau, Susan Ross, Diana C Yanez, Oscar A Peña, Benny Chain, Tessa Crompton
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/93493
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author Jasmine Rowell
Ching-In Lau
Susan Ross
Diana C Yanez
Oscar A Peña
Benny Chain
Tessa Crompton
author_facet Jasmine Rowell
Ching-In Lau
Susan Ross
Diana C Yanez
Oscar A Peña
Benny Chain
Tessa Crompton
author_sort Jasmine Rowell
collection DOAJ
description Here, we sequenced rearranged TCRβ and TCRα chain sequences in CD4+CD8+ double positive (DP), CD4+CD8- single positive (SP4) and CD4-CD8+ (SP8) thymocyte populations from the foetus and young adult mouse. We found that life-stage had a greater impact on TCRβ and TCRα gene segment usage than cell-type. Foetal repertoires showed bias towards 3’TRAV and 5’TRAJ rearrangements in all populations, whereas adult repertoires used more 5’TRAV gene segments, suggesting that progressive TCRα rearrangements occur less frequently in foetal DP cells. When we synchronised young adult DP thymocyte differentiation by hydrocortisone treatment the new recovering DP thymocyte population showed more foetal-like 3’TRAV and 5’TRAJ gene segment usage. In foetus we identified less influence of MHC-restriction on α-chain and β-chain combinatorial VxJ usage and CDR1xCDR2 (V region) usage in SP compared to adult, indicating weaker impact of MHC-restriction on the foetal TCR repertoire. The foetal TCRβ repertoire was less diverse, less evenly distributed, with fewer non-template insertions, and all foetal populations contained more clonotypic expansions than adult. The differences between the foetal and adult thymus TCR repertoires are consistent with the foetal thymus producing αβT-cells with properties and functions that are distinct from adult T-cells: their repertoire is less governed by MHC-restriction, with preference for particular gene segment usage, less diverse with more clonotypic expansions, and more closely encoded by genomic sequence.
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spelling doaj-art-cad8f80190414a5682a9e4cb024960d62024-12-05T14:24:22ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.93493Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymusJasmine Rowell0https://orcid.org/0000-0001-7040-8528Ching-In Lau1Susan Ross2Diana C Yanez3Oscar A Peña4https://orcid.org/0000-0002-2582-0238Benny Chain5https://orcid.org/0000-0002-7417-3970Tessa Crompton6https://orcid.org/0000-0002-8973-4021UCL Great Ormond Street Institute of Child Health, London, United KingdomUCL Great Ormond Street Institute of Child Health, London, United KingdomUCL Great Ormond Street Institute of Child Health, London, United KingdomUCL Great Ormond Street Institute of Child Health, London, United KingdomSchool of Biochemistry, University of Bristol, Bristol, United KingdomDivision of Infection and Immunity, University College London, London, United KingdomUCL Great Ormond Street Institute of Child Health, London, United KingdomHere, we sequenced rearranged TCRβ and TCRα chain sequences in CD4+CD8+ double positive (DP), CD4+CD8- single positive (SP4) and CD4-CD8+ (SP8) thymocyte populations from the foetus and young adult mouse. We found that life-stage had a greater impact on TCRβ and TCRα gene segment usage than cell-type. Foetal repertoires showed bias towards 3’TRAV and 5’TRAJ rearrangements in all populations, whereas adult repertoires used more 5’TRAV gene segments, suggesting that progressive TCRα rearrangements occur less frequently in foetal DP cells. When we synchronised young adult DP thymocyte differentiation by hydrocortisone treatment the new recovering DP thymocyte population showed more foetal-like 3’TRAV and 5’TRAJ gene segment usage. In foetus we identified less influence of MHC-restriction on α-chain and β-chain combinatorial VxJ usage and CDR1xCDR2 (V region) usage in SP compared to adult, indicating weaker impact of MHC-restriction on the foetal TCR repertoire. The foetal TCRβ repertoire was less diverse, less evenly distributed, with fewer non-template insertions, and all foetal populations contained more clonotypic expansions than adult. The differences between the foetal and adult thymus TCR repertoires are consistent with the foetal thymus producing αβT-cells with properties and functions that are distinct from adult T-cells: their repertoire is less governed by MHC-restriction, with preference for particular gene segment usage, less diverse with more clonotypic expansions, and more closely encoded by genomic sequence.https://elifesciences.org/articles/93493thymusTCR sequencingTCR repertoirerepertoire selectionMHC-restrictionT-cell development
spellingShingle Jasmine Rowell
Ching-In Lau
Susan Ross
Diana C Yanez
Oscar A Peña
Benny Chain
Tessa Crompton
Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus
eLife
thymus
TCR sequencing
TCR repertoire
repertoire selection
MHC-restriction
T-cell development
title Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus
title_full Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus
title_fullStr Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus
title_full_unstemmed Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus
title_short Distinct T-cell receptor (TCR) gene segment usage and MHC-restriction between foetal and adult thymus
title_sort distinct t cell receptor tcr gene segment usage and mhc restriction between foetal and adult thymus
topic thymus
TCR sequencing
TCR repertoire
repertoire selection
MHC-restriction
T-cell development
url https://elifesciences.org/articles/93493
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