A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus

Thymus-committed regulatory T cells (Tregs) are essential for immune homeostasis. Recent findings stress their heterogeneity, suggesting possible alternate routes for thymic Treg development with unique features in humans, namely the clear evidence of Treg commitment at the double-positive (DP) stag...

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Main Authors: Beatriz Moleirinho, Margarida Paulo-Pedro, Nicole C. Martins, Emily Jelagat, Eller Conti, Tiago R. Velho, Miguel Abecasis, Rui Anjos, Afonso R. M. Almeida, Ana E. Sousa
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1553535/full
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author Beatriz Moleirinho
Beatriz Moleirinho
Margarida Paulo-Pedro
Margarida Paulo-Pedro
Nicole C. Martins
Nicole C. Martins
Emily Jelagat
Emily Jelagat
Eller Conti
Eller Conti
Tiago R. Velho
Tiago R. Velho
Miguel Abecasis
Rui Anjos
Afonso R. M. Almeida
Afonso R. M. Almeida
Ana E. Sousa
Ana E. Sousa
author_facet Beatriz Moleirinho
Beatriz Moleirinho
Margarida Paulo-Pedro
Margarida Paulo-Pedro
Nicole C. Martins
Nicole C. Martins
Emily Jelagat
Emily Jelagat
Eller Conti
Eller Conti
Tiago R. Velho
Tiago R. Velho
Miguel Abecasis
Rui Anjos
Afonso R. M. Almeida
Afonso R. M. Almeida
Ana E. Sousa
Ana E. Sousa
author_sort Beatriz Moleirinho
collection DOAJ
description Thymus-committed regulatory T cells (Tregs) are essential for immune homeostasis. Recent findings stress their heterogeneity, suggesting possible alternate routes for thymic Treg development with unique features in humans, namely the clear evidence of Treg commitment at the double-positive (DP) stage and the presence of a significant population of CD8 single-positive (SP) FOXP3pos Tregs. Here, we present a dedicated analysis strategy to a spectral flow cytometry-based study of thymus from children and aged adults (≥ 74-years-old), to further elucidate Treg development and heterogeneity in the human thymus. We applied an unsupervised analysis pipeline to data generated from 6 high-dimensional panels, taking advantage of a common backbone of 11 markers, and we were able to map thymocytes along T cell maturation stages. Generating UMAP and FlowSOM cluster coordinates from the backbone, we projected all other markers onto these, characterizing clusters with the information of all markers. Focusing this analysis on events inside a putative total Treg gate, we could portray rarer subsets of human thymic Tregs and investigate their trajectories using pseudotime analysis. We uncover clusters within human DP thymocytes uniquely expressing FOXP3 or CD25, a DP-branching trajectory towards a CD103posCD8SP Tregs endpoint, and define trajectories towards CD4SP Tregs, including towards a cluster of CXCR3posCD4SP Tregs, that may consist of thymic resident or recirculating Tregs, and do not expand in the elderly. Our flow cytometry approach separates Treg populations with likely distinct functions and facilitates the design of future studies to unravel the complexity of human regulatory T cells.
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spelling doaj-art-c6bf933b08bd45bda273732bcce2977d2025-08-20T02:00:47ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-03-011610.3389/fimmu.2025.15535351553535A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymusBeatriz Moleirinho0Beatriz Moleirinho1Margarida Paulo-Pedro2Margarida Paulo-Pedro3Nicole C. Martins4Nicole C. Martins5Emily Jelagat6Emily Jelagat7Eller Conti8Eller Conti9Tiago R. Velho10Tiago R. Velho11Miguel Abecasis12Rui Anjos13Afonso R. M. Almeida14Afonso R. M. Almeida15Ana E. Sousa16Ana E. Sousa17GIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalGIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalGIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalGIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalGIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalCardiothoracic Surgery Research Unit, Centro Cardiovascular da Universidade de Lisboa, Faculdade de Medicina da Universidade de Lisboa, Lisbon, PortugalDepartment of Cardiothoracic Surgery, Hospital de Santa Maria, Unidade Local de Saúde de Santa Maria, Lisbon, PortugalHospital de Santa Cruz, Unidade Local de Saúde de Lisboa Ocidental, Carnaxide, PortugalHospital de Santa Cruz, Unidade Local de Saúde de Lisboa Ocidental, Carnaxide, PortugalGIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalGIMM- Gulbenkian Institute for Molecular Medicine, Lisbon, PortugalFaculdade de Medicina, Universidade de Lisboa, Lisbon, PortugalThymus-committed regulatory T cells (Tregs) are essential for immune homeostasis. Recent findings stress their heterogeneity, suggesting possible alternate routes for thymic Treg development with unique features in humans, namely the clear evidence of Treg commitment at the double-positive (DP) stage and the presence of a significant population of CD8 single-positive (SP) FOXP3pos Tregs. Here, we present a dedicated analysis strategy to a spectral flow cytometry-based study of thymus from children and aged adults (≥ 74-years-old), to further elucidate Treg development and heterogeneity in the human thymus. We applied an unsupervised analysis pipeline to data generated from 6 high-dimensional panels, taking advantage of a common backbone of 11 markers, and we were able to map thymocytes along T cell maturation stages. Generating UMAP and FlowSOM cluster coordinates from the backbone, we projected all other markers onto these, characterizing clusters with the information of all markers. Focusing this analysis on events inside a putative total Treg gate, we could portray rarer subsets of human thymic Tregs and investigate their trajectories using pseudotime analysis. We uncover clusters within human DP thymocytes uniquely expressing FOXP3 or CD25, a DP-branching trajectory towards a CD103posCD8SP Tregs endpoint, and define trajectories towards CD4SP Tregs, including towards a cluster of CXCR3posCD4SP Tregs, that may consist of thymic resident or recirculating Tregs, and do not expand in the elderly. Our flow cytometry approach separates Treg populations with likely distinct functions and facilitates the design of future studies to unravel the complexity of human regulatory T cells.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1553535/fullthymushuman immunologyregulatory T cellsT cell developmentspectral flow cytometry
spellingShingle Beatriz Moleirinho
Beatriz Moleirinho
Margarida Paulo-Pedro
Margarida Paulo-Pedro
Nicole C. Martins
Nicole C. Martins
Emily Jelagat
Emily Jelagat
Eller Conti
Eller Conti
Tiago R. Velho
Tiago R. Velho
Miguel Abecasis
Rui Anjos
Afonso R. M. Almeida
Afonso R. M. Almeida
Ana E. Sousa
Ana E. Sousa
A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus
Frontiers in Immunology
thymus
human immunology
regulatory T cells
T cell development
spectral flow cytometry
title A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus
title_full A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus
title_fullStr A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus
title_full_unstemmed A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus
title_short A backbone-based flow cytometry approach to decipher regulatory T cell trajectories in the human thymus
title_sort backbone based flow cytometry approach to decipher regulatory t cell trajectories in the human thymus
topic thymus
human immunology
regulatory T cells
T cell development
spectral flow cytometry
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1553535/full
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