---
title: "Decoding regulatory and conventional CD4+ T cells in the human term decidua"
id: "frontiers-in-immunology-14-defining-nature-responses-and-drivers-of-regulatory-and-conventional-cd4-t"
canonical_url: "https://medichelpline.com/clinical-feed/frontiers-in-immunology-14-defining-nature-responses-and-drivers-of-regulatory-and-conventional-cd4-t"
content_type: "clinical_feed_article"
specialty: "Infectious Disease"
source_name: "Frontiers in Immunology"
source_url: "https://www.frontiersin.org/articles/10.3389/fimmu.2026.1865340"
published_at: "2026-08-04T00:00:00.000Z"
evidence_level: "Journal Feed"
license: "CC-BY-NC-4.0 / Informational Use"
---
# Decoding regulatory and conventional CD4+ T cells in the human term decidua
## Provenance & Clinical Metadata
- **Canonical URL:** https://medichelpline.com/clinical-feed/frontiers-in-immunology-14-defining-nature-responses-and-drivers-of-regulatory-and-conventional-cd4-t
- **Specialty:** [Infectious Disease](https://medichelpline.com/clinical-feed/infectious-disease.md)
- **Primary Source:** Frontiers in Immunology
- **Source URL:** [Original Journal Publication](https://www.frontiersin.org/articles/10.3389/fimmu.2026.1865340)
- **Published At:** 2026-08-04T00:00:00.000Z
- **Evidence Rating:** Journal Feed
## Executive GIST (TL;DR)
- The study characterizes maternal **decidual CD4+ regulatory T cells (Tregs)** and conventional CD4+ T cells (Tconvs) at term pregnancy using single-cell transcriptomics and paired TCR sequencing from decidua basalis, decidua parietalis, maternal peripheral blood and cord blood from Caesarean deliveries. - Donors had healthy term pregnancies delivered by C-section prior to labor; tissue handling included enzymatic digestion, density centrifugation and magnetic or flow sorting for CD4+ subsets. Matched peripheral and cord blood were processed by Ficoll. - Flow cytometry and Opt-SNE analyses revealed increased effector-memory phenotypes in decidual CD4+ T cells with tissue-specific expression differences in FOXP3, CD25, CTLA-4 and PD-1. - scRNA-seq and scTCR-seq identified both shared and distinct transcriptomic features of decidual Tregs and Tconvs, including evidence of local antigen recognition, activation, clonal expansion and effector differentiation. - The large majority of decidual Tregs at term were classified as thymus-derived (**tTregs**) based on enrichment of a tTreg core signature and largely non-overlapping TCR repertoires with Tconvs. - Decidual Tregs expanded locally more than Tconvs and acquired a non-lymphoid tissue (NLT) resident effector phenotype with multiple suppressive functions; TNF receptor-2 (**TNFR2**) costimulation was identified as a key driver of this differentiation. - Additional shared drivers of effector differentiation for both Tregs and Tconvs included **IFNs**, interleukins and prolactin as detected or inferred from transcriptomic signatures. - Effector Tconvs developed proinflammatory and cytotoxic lineage-defining features, yet were constrained by intrinsic inhibitory receptors and extrinsic suppression by Tregs; both cell types shared glycolytic and **antigen-presenting** transcriptional programs. - Subpopulations of both Tregs and Tconvs showed markers consistent with exhaustion, supporting a model of chronic antigenic stimulation and ongoing T-cell priming and turnover in the decidua across pregnancy. - The molecular definitions provided can support mRNA- and protein-level diagnostics and improve mechanistic understanding of maternal–fetal tolerance by delineating lineage origins, activation states, drivers and functional specializations of decidual CD4+ T cells.
## Clinical Analysis & Structured Key Points
Frontiers | Defining nature, responses and drivers of regulatory- and conventional CD4+ T cells in the human term decidua ORIGINAL RESEARCH article Front. Immunol. , 04 August 2026 Sec. Immunological Tolerance and Regulation Volume 17 - 2026 | https://doi.org/10.3389/fimmu.2026.1865340 Published in Frontiers in Immunology Immunological Tolerance and Regulation 7 impact factor 11.3 citescore Editor & Reviewers Edited by A R Abdel Rahim A Hamad Reviewed by Y S Yohei Sato N I Nadia Ikumi Outline Figures and Tables Figure 1 View in article Figure 2 View in article Figure 3 View in article Figure 4 View in article Figure 5 View in article Figure 6 View in article Figure 7 View in article Table 1 Characteristics of patients included in the study. View in article ORIGINAL RESEARCH article Front. Immunol. , 04 August 2026 Sec. Immunological Tolerance and Regulation Volume 17 - 2026 | https://doi.org/10.3389/fimmu.2026.1865340 Defining nature, responses and drivers of regulatory- and conventional CD4 + T cells in the human term decidua L J Lotte J. Verleng 1,2 J B Julia Busselaar 1,2 M M Mark Mensink 1,2 E S Ellen Schrama 1,2 H K Hanneke Kapsenberg 1 C V Carin van der Keur 1 X L Xin Lei 1,2 M E Michael Eikmans 1 Y X Yanling Xiao 1,2 S D Sander de Kivit 1,2 † * +2 more J B Jannie Borst 1,2 † * 1. Department of Immunology, Leiden University Medical Center, Leiden, Netherlands 2. Oncode Institute, Leiden University Medical Center, Leiden, Netherlands Article metrics View details Abstract Background: During mammalian pregnancy, a maternal immunoregulatory network develops in the decidua that fosters fetal development, maintains tolerance to fetal antigens and protects against infection. Herein, decidual regulatory T cells (Tregs) are crucial for pregnancy success. Aim and methodology: To understand the nature and response of maternal CD4 + Tregs and CD4 + conventional T-cells (Tconv) in healthy human pregnancy, we analyzed these cells in decidua and blood at term, caesarean delivery by single-cell transcriptomics and TCR sequencing. Results: Data mining revealed novel discerning, as well as shared features and functionalities of decidual CD4 + Tregs and Tconvs. Both cell types showed evidence of antigen recognition and activation in the decidua, followed by local clonal expansion and effector differentiation. Tregs were largely of the thymus-derived (t)Treg lineage that has a self-antigen reactive T cell receptor (TCR) repertoire. Tregs locally expanded, more so than Tconvs, and differentiated into typical non-lymphoid tissue (NLT)-resident effector cells with discerning cell surface markers and multiple suppressive functions, driven by TNF receptor-2 costimulation. Additional factors, including IFNs, interleukins and prolactin emerged as shared drivers of decidual Treg and Tconv effector differentiation. Effector Tconvs had cell lineage-discerning proinflammatory and cytotoxic capacities, restrained by cell-intrinsic and -extrinsic mechanisms, while sharing glycolytic and antigen-presenting features with Tregs. Treg and Tconv subpopulations showed signs of exhaustion, suggesting chronic antigenic stimulation. Overall, the observed features argue for ongoing de novo T-cell priming and dynamic T-cell turnover in the decidua throughout pregnancy. Conclusion: Our findings suggest that non-self-reactive CD4 + Tconvs and self-reactive tTregs are continuously primed in lymphoid organs during pregnancy, reactivated by antigen in the decidua and dynamically turned over. In the decidua, CD4 + Tconvs and Tregs expand and differentiate under influence of specific cytokines into tissue-resident effector cells with opposing and restrained pro- and anti-inflammatory functions, as well as shared antigen-presenting capacity. Significance: These molecular definitions of decidual CD4 + Tregs and Tconvs can be used to aid diagnostics at mRNA and protein level. Moreover, they facilitate mechanistic understanding of maternal-fetal tolerance, based on extrapolation of known T-cell lineage characteristics and tissue adaptations in health and disease. 1 Introduction During mammalian pregnancy, the blastocyst implants into the uterine endometrium and develops into both fetus and placenta. The uterine endometrium transforms into decidual tissue, which supports fetal and placental development. Fetal cytotrophoblasts (CTBs) form placental villi covered by further differentiated syncytiotrophoblasts (STBs), while the inner CTB layer anchors the placenta to the decidua through invasion ( 1 ). CTBs also differentiate into extravillous trophoblasts (EVTs), which remodel maternal blood vessels to enable direct maternal-fetal contact and efficient exchange of nutrients, gases and waste products ( 2 ). The decidua basalis (DB) constitutes the placental interface, while the decidua parietalis (DP) lines the distal uterine wall. This type of placentation occurs in mammals with a hemochorial placenta, including humans and mice ( 3 ), and establishes the structural context for maternal-fetal immune interactions ( 4 , 5 ). The immune cell composition of the endometrium dynamically changes upon decidualization during the menstrual cycle and pregnancy, in response to seminal fluid and fetal signals. The decidua is populated with maternal macrophages, dendritic cells (DCs) and lymphoid cells, but direct recognition of the semi-allogeneic fetal trophoblasts by T cells is limited because STBs do not express any major histocompatibility complex (MHC) molecules and EVTs only express HLA-C. Furthermore, EVTs attenuate natural killer (NK) cell activity via non-polymorphic HLA-E and -G ( 6 , 7 ) and T-cell activation via PD-1 ligands, which is critical for successful pregnancy ( 8 ). Indirect recognition of the allogenic fetus by T cells is possible, however, also on basis of MHC-II, because macrophages and DCs of the mother will be able to phagocytose fetal cell debris and present antigens. Responses of CD4 + and CD8 + Tconvs may be required in case of fetal infection and therefore Tconv responses must be carefully controlled. Accordingly, Tregs are required for fetal tolerance from the first trimester onwards, as shown by Treg depletion studies in mice ( 9 – 13 ) and human data linking low Treg number or impaired Treg function in decidua and peripheral blood to pregnancy failure ( 14 , 15 ). Tregs are required for allogeneic but not syngeneic pregnancy success ( 9 ), indicating that decidual Tregs restrain Tconv responses to paternal alloantigens. Indeed, mouse studies showed that pregnancy induces maternal T-cell tolerance to paternal (MHC) molecules, allowing acceptance of the fetus as well as implanted tumors of the same MHC type ( 16 ). Paternal antigen presentation to maternal CD4 + and CD8 + Tconvs relies on maternal antigen presenting cells ( 17 ), which may include conventional (c)DCs ( 18 ). Trafficking of cDCs to draining lymph nodes (dLNs) typically initiates T-cell priming ( 19 ), but upon decidualization, DCs appear physically trapped ( 20 ), and lymphatic vessels disappear ( 21 ), suggesting an additional mechanism preventing anti-fetal T-cell priming. Nevertheless, Tconv responses to paternal antigens have been demonstrated in mouse models and in humans ( 17 , 22 – 25 ). During murine pregnancy, Tregs were shown to expand in uterine dLNs and systemically, with more overt responses in the allogeneic setting ( 12 ). In human pregnancy, Treg frequencies among decidual T cells also increase ( 12 , 26 ), particularly upon HLA-C mismatch ( 27 ). Although these data suggest that the responding Tregs are activated by paternal allo-antigens, this has not been proven ( 28 ). Alternatively, Tregs may be maternal self-antigen specific and expand in response to IL-2 produced by activated (alloreactive) Tconvs ( 29 ). A key question has been whether decidual Tregs are thymus-derived (t)Tregs, peripherally-induced (p)Tregs or both. While tTregs are generated as a separate cell lineage in the thymus, pTregs arise during an ongoing immune response from CD4 + Tconvs ( 30 , 31 ). Genetic evidence from a mouse study has argued in favor of pTregs being at least in part responsible for pregnancy success ( 32 ). In the studies cited above, Tregs were mostly defined on a CD4 + CD25 high phenotype rather than expression of Forkhead Box P3 (FOXP3), which has been used later to define decidual Tregs ( 33 – 35 ). The core transcriptomic signature of tTregs includes FOXP3 , IKZF2/4 , CTLA4 , IL2RA/RB , TNFRSF4, -9 and -18 ( 36 – 40 ). FOXP3 installs part of this signature ( 36 ), while chromatin remodeling and transcription factors such as IKAROS Family Zinc Finger 2 (IKZF2; HELIOS) and IKZF4 (EOS) further stabilize tTreg identity ( 29 , 41 ). It is important to classify Tregs as tTregs or pTregs because tTregs have a primarily self-reactive TCR repertoire and stably express FOXP3 ( 42 ), while pTregs recognize non-self antigens and may lose FOXP3 expression. Loss of the Foxp3 gene in established Tregs results in loss of their in vivo suppressive function and a gained ability to produce IL-2 and pro-inflammatory cytokines ( 43 ). Because tTregs cannot produce IL-2, they depend on Tconv-derived IL-2 for clonal expansion and survival ( 42 ). Importantly, they retain their suppressive identity in pro-inflammatory environments by differentially processing cytokine signals compared to Tconvs ( 44 ). Tregs populate non-lymphoid tissues (NLT) both in health and disease, where they display a unique, tissue-resident phenotype and gene expression profile ( 45 – 47 ). The relationship of NLT-resident effector (e)Tregs to naive tTregs has long been unclear, but we recently demonstrated that naive tTregs from human blood can differentiate into cells with the NLT-resident gene expression profile upon TCR-mediated activation and costimulation via TNF receptor (TNFR)2 ( 48 ). Accumulating evidence indicates that, both in the first trimester and at term, the human decidua is primarily populated by Tregs with unique TCR repertoires compared to decidual Tconvs, suggesting their divergent origins ( 34 , 35 ). In addition, decidual Tregs display an effector phenotype resembling Tregs in other peripheral tissues, including tumors ( 33 , 35 ). Importantly, a CCR8 + decidual Treg population has been implicated in promoting pregnancy success in mice ( 35 ), highlighting a critical role for specialized Treg subsets at the maternal-fetal interface ( 47 ). With these insights in mind, we defined discerning and common features of human decidual CD4 + Tregs and Tconvs, as isolated from the placenta at term delivery by scRNA- and TCRseq analysis. CD4 + Tregs and Tconvs from matched maternal peripheral blood and cord blood were also included in the analysis. The donors underwent healthy pregnancies with delivery by caesarean (C-)section, excluding immune regulatory effects of labor. We resolved the clonal relationships among and between Tregs and Tconvs, their activation states and functional properties, revealing a dynamic immune landscape in which maternal CD4 + T cells undergo continuous priming and reactivation in the decidua, followed by local expansion and effector differentiation. Our findings indicate that decidual Tregs are primarily tTregs, based on non-overlapping TCR repertoires compared to Tconvs and enrichment of the stable tTreg core signature ( 44 ). These tTregs adopt an NLT-resident gene expression profile within the decidua, under influence of TNFR2 driver signals. Effector Tconvs and Tregs shared capacity for antigen presentation on MHC-I and II, while CD4 + Tconvs become vigilant cytotoxic and pro-inflammatory cells, apparently restrained intrinsically by inhibitory receptors and extrinsically by Tregs. Our findings suggest a dynamic local immune regulatory network in the decidua, that maintains maternal-fetal tolerance whilst being alert to combat infection. This study classifies the great majority of decidual Tregs at term pregnancy as tTregs, provides important phenotypic distinctions between decidual CD4 + Tregs and Tconvs and clarifies their response to the fetus in terms of clonal expansion, acquisition of distinct functional states and turnover. 2 Materials and methods 2.1 Isolation of lymphocytes from human blood and placenta Donors were recruited at Leiden University Medical Center and clinical parameters are listed in Table 1 . Maternal (m)PB was collected 1 h prior to C-section and umbilical cord blood (UCB) was collected directly after, in heparin anticoagulation blood tubes. Mononuclear cells were isolated from mPB and UCB by Ficoll-Paque (GE Healthcare) density gradient centrifugation (820x g , no brake, room temperature, 20 min). Mononuclear cells were isolated from DP and DB as described ( 49 ), with adaptations as follows: DP and DB were macroscopically dissected and tissues were washed in PBS, minced, and resuspended in RPMI 1640 (Life Technologies) with 0.2 mg/ml Collagenase IV (MilliporeSigma) and 0.01 mg/ml DNAse I (Sigma) at a ratio of 10 ml digestion mix per 5 g tissue. Tissue was homogenized with a GentleMACS tissue dissociator (Miltenyi Biotec), using program m-tumor 02 (37 seconds at 235 rpr) for DP and program m-heart 02.01 (17 seconds at 668 rpr) for DB and incubated for 30 min at 37°C. Next, cell suspensions were sequentially passed through a 250-μm- and a 70-μm filter and washed in RPMI 1640 with 5% FCS. They were mixed with 20 ml of 1.023 g/ml Percoll (GE Healthcare) and separated by density gradient centrifugation (820 g , no brake, room temperature, 30 min) on a Percoll gradient (10 ml of 1.080 g/ml, 15 ml of 1.053 g/ml, pH = 7.4). Mononuclear cells were isolated from the 1.080–1.053 g/ml interface. Subsequently, samples were washed twice in RPMI. Cells were processed for flow cytometric analysis directly after isolation, or cryopreserved and stored in liquid nitrogen until processing for scRNAseq. Decidual and mPB cells were by definition from females, while UCB was from males or females as indicated in Table 1 . Table 1 Donor # 1 Maternal age BMI 2 Gravidity 3 Parity 4 Gestational age Gender baby 5 C-section indication Analysis 1 32 y 25.6 3 1 39 w F Previous C-section scRNA/TCRseq 6 2 31 y 29.0 2 1 39 w + 1 d M Previous C-section scRNA/TCRseq 6 3 31 y 22.0 2 1 40 w + 5 d F Previous C-section scRNA/TCRseq 6 4 33 y 24.7 1 0 39 w + 1 d M Caput in fundo FC 7 5 30 y 30.6 1 0 39 w + 4 d M Caput in fundo FC 7 6 41 y 30.1 1 0 37 w + 6 d F Placenta praevia FC 7 7 29 y 27.0 4 1 39 w + 2 d F Previous C-section FC 8 8 33 y 32.4 3 2 38 w F Previous C-section FC 8 9 34 y 25.4 2 1 38 w + 2 d F No C-section FC 8 10 40 y 18.6 5 2 35 w + 5 d F Previous C-section; PE FC 8 Characteristics of patients included in the study. 1 Donor 1–5, 7 and 8: spontaneous conception, Donor 6 and 10: intracytoplasmic sperm injection, Donor 9: IVF. Donor 8 had diabetes gravidarum; 2 BMI, body mass index (prior to pregnancy); 3 Total number of pregnancies, prior to this study; 4 Total number of pregnancies that reached viable gestational age, prior to this study. Donor 1 had one miscarriage and donors 7 and 10 had two miscarriages in the past; 5 F, female, M, male; 6 see Figures 3 – 7 , and Supplementary Figures 1 – 3 and 5 – 7 ; 7 see Figure 1 and Supplementary Figure 1 FC, flow cytometry; 8 see Supplementary Figure 4 and Mensink et al., 2024 ( 48 ). (PE, preeclampsia). 2.2 Phenotypic analysis by flow cytometry Donors used for the scRNAseq (n=3, pooled) and the flow cytometry analyses shown in Figure 1 and Supplementary Figure 1 (n=3) had healthy term pregnancies and underwent C-section prior to labor commencement ( Table 1 ), while donors (n=4) used for the flow cytometry analysis shown in Supplementary Figure 4 had a more variable clinical history ( Table 1 ). CD4 + T cells were isolated from decidua, mPB and UCB by magnetic purification from mononuclear cells by MACS cell separation (Miltenyi Biotec) using CD4 MicroBeads (Miltenyi Biotec, cat. #130-045-101). The CD4 + cell fraction was washed in PBS/1% FCS and incubated on ice with human Fc-Block (BioLegend) for 5 min and next stained for 30 min with the mAbs listed in Supplementary Table 1 . Cell viability was assessed using LIVE/DEAD blue dye (ThermoFisher Scientific). For intracellular staining, cells were fixed and permeabilized using the eBioscience™ FOXP3 transcription factor staining buffer set (Invitrogen), according to the manufacturer’s instructions. Cells were stained for 45 min on ice in permeabilization buffer with the following mAbs: FOXP3-APC (Invitrogen), Helios-PE-Cy7, EOS-PE (both Biolegend) and CTLA-4-BB700 (BD Biosciences). After washing, flow cytometry analysis was performed on a 5-laser Cytek Aurora with SpectroFlo software (Cytek Biosciences). Flow cytometry data were analyzed with the OMIQ platform (Dotmatics) or FlowJo software. In OMIQ analyses, the Flow AI algorithm ( 50 ) was used for anomaly detection and exclusion, followed by data scaling and compensation when necessary. Cells of interest were gated as visualized in Supplementary Figure 1 . Dimension reduction was performed using Opt-SNE ( 51 ) using all markers except Live-dead, CD3, CD4 and CD8. Mean expression data were exported for quantification. Figure 1 Flow cytometric analysis of CD4+ T cells from decidua and blood. (A) Methodology used for isolation CD4 + T cells from DB, DP, mPB and UCB prior to analysis by spectral flow cytometry. Created in BioRender ( https://BioRender.com/6gve59e ). (B, C) Opt-SNE cluster analysis of concatenated flow cytometric data from all CD4 + T-cell samples, indicating relative signal density in the different tissues (B) and relative expression of indicated markers (C) . (D) Representative dot plots (left) and quantification (right) of CD45RO + effector Treg and Tconv frequencies in the four tissues. One-way ANOVA with Tukey’s post hoc test was used for statistical analysis. (E–H) Representative histograms (upper panels) and quantification (lower panels) of mean fluorescence intensity (MFI) of FOXP3 (E) , CD25 (F) , CTLA-4 (G) and PD-1 (H) measurements on CD4 + T cells from the indicated tissues. Two-way repeated measures ANOVA with Tukey’s post hoc test was used for statistical analysis (* p < 0.05, ** p < 0.01, *** p < 0.001). (A–H) Data represent samples obtained from n = 3 individual donors ( Table 1 ). (D–H) Data are presented as mean ± SEM. 2.3 Sample and library preparation for scRNAseq and coupled scTCRseq Mononuclear cells were isolated by density centrifugation from DP, DB, mPB and UCB (n=3, see Table 1 ) and cryopreserved as described above. A small fraction was analyzed by flow cytometry to check frequencies of decidual Tregs which were comparable between donors. Before flow cytometric sorting, cells were quickly thawed in a 37 °C water bath and washed in IMDM with 8% FCS (ThermoFisher Scientific) with 0.01 mg/ml DNAse I (Sigma). Samples were pooled in equal representation of each of the three donors per tissue and stained with CD4-BB700, CD25-PE (BD BioSciences), CD8-PE-Cy7, CD127-BV421 and CD26-APC (BioLegend) mAbs for flow cytometric sorting ( Supplementary Figure 1D ). Cell viability was assessed using LIVE/DEAD blue dye (Invitrogen) for placenta samples and 4-6-diamidino-2-phenylindole (DAPI) stain (Sigma) for blood samples. Tregs (CD25 hi CD26 low in decidua and CD25 hi CD127 low in blood) and Tconvs cells (CD25 low/int in decidua and CD25 low CD127 + in blood) were sorted using a BD FACSAria II sorter with FACSDiva Software (version 9.0.1, BD Biosciences). Samples were kept at 4 °C throughout the procedure and collected on ice. After cell sorting, Tregs and Tconvs from each tissue were transferred to a 96-well U-bottom plate (Corning) in a 1:1 ratio to ensure equal representation of both cell types in the scRNAseq data. To discern cells from the different tissues, they were each labeled with a distinct 5’ hashtag oligonucleotide (HTO)-conjugated antibody (TotalSeq™-C0251 - C0254, BioLegend). Cell v
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