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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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h, One-way analysis of variance with Holm–Sidak’s multiple-comparisons test.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We examined pseudotime trajectories of tissue-resident clusters with TCR repertoire clonal sharing (TRM(1), TRM(2), IL7R and CCL4 effectors) to infer putative differentiation pathways (Fig. 5a,b,e).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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The pseudotime trajectory showed two branches, formed predominantly of TRM(1) cells in branch 1 and TRM(2) cells in branch 2, developing from IL7R and CCL4 populations (Fig. 5a).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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While branch 1 cells were seen in both controls and CD, strikingly, branch 2 was almost totally restricted to ACD and TCD (Fig. 5b).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We examined cytokine, chemokine and TF expression by CD8 T cell subsets.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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The predominant CD8 sources of IFNG were CD8 TRM(2) and cycling clusters (Fig. 5c,d and Extended Data Fig. 5g–i).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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These populations also expressed the chemokine CCL5, CD70 and FASLG.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Natural IELs (reduced in ACD), produced CCL2, CXCL2, CXCL3, IL12, IL18 and type I interferon.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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TRM(1) and TRM(2) CD8 subsets showed distinct TF and regulon profiles; TRM(2) cells were associated with the TF regulons BACH1, CEBPZ, CREM, IRF4 and NR3C1 and TF expression of RORA, PRDM and FOXO1 (Extended Data Fig. 5j–l).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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CD8 T cell-induced epithelial damage is thought to be mediated via TCR-independent mechanisms.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We hypothesized that CD8 T cell TCR repertoires would be similar in health and disease.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Single-cell TCR sequences were examined, which showed expected clonal overlap between tissue-resident populations (Fig. 5e and Extended Data Fig. 6a).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Cluster TRBV gene usage was examined between health and CD.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Several high-frequency TRBV segments (>1% total clones) were overrepresented in CD (Fig. 5f and Extended Data Fig. 6b).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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However, statistical power was limited due to low clonotype numbers.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Consequently, we sorted intraepithelial CD8 T cells from 12 adults with and without CD (dataset 3) and performed bulk RNA-seq.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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This showed significant enrichment of one TRBV segment, TRBV28, enriched in ACD and TCD, but not controls (Fig. 5g).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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TRBV28 was the high-frequency V segment with the highest fold change for enrichment in CD within the TRM(2) population (Fig. 5f).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We validated this by performing bulk TCR repertoire sequencing on 1,068,814 mucosal CD8 T cells from 20 donors with and without CD (dataset 4).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Again, TRBV28 was highly upregulated in CD, forming 10% of unique CDR3 sequences in ACD and TCD, versus 2% in controls (Fig. 5h).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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TRBV28 was also enriched within the top 100 most expanded clonotypes.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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No association with TRAV usage was seen.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Clonotypes containing TRBV28 in CD paired with multiple TRBJ segments, and showed altered CDR3 amino acid usage, with enrichment of germline-encoded and non-germline-encoded leucine residues (Extended Data Fig. 6c–e).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We examined bulk TCR repertoires of intestinal CD8 T cells of colonic and small intestinal biopsy samples from three separate studies examining non-CD inflammatory gastrointestinal conditions.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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There was no signal for enrichment of TRBV28 gene usage in these disease settings (Extended Data Fig. 6f–h).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We hypothesized that differences in mucosal CD8 TCR repertoire/phenotype may be mirrored within gut-homing CD8 T cells in the circulation, as seen following gluten challenge.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We examined TRBV28 usage by circulating CD8 T cells using flow cytometry (dataset 9).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Using TCR sequencing (TCR-seq), we validated the specificity of the TRBV28-specific antibody clone (JOVI.3; Extended Data Fig. 7a–c).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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As expected, there was no difference in the fraction of TRBV28 cells in total peripheral CD3 or CD8 T cell compartments in participants with and without CD.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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However, within CD8 T cell populations expressing gut-specific chemokines (CCR9) or integrins (CD103/β-integrin), the fraction of TRBV28 cells was increased in ACD and TCD (Extended Data Fig. 7d–h).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Intraepithelial duodenal γδ T cells are increased in CD, although their role is unclear.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We analyzed a further dataset of 5,552 sorted intestinal CD8 αβ and γδ T cells (dataset 8; Extended Data Fig. 8).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Clustering of cell transcriptional states recapitulated the key populations described above (Extended Data Fig. 8a,b).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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As previously, the TRM(2) population (in this case split into IFNG and IKZF2 subpopulations) was increased in ACD, along with cycling T cells (Extended Data Fig. 8c).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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γδ T cells showed overlapping transcriptional profiles with mucosal CD8 αβ T cells, albeit with enrichment within specific clusters (Extended Data Fig. 8d,e).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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γδ T cells were most enriched within a natural IEL phenotype cluster and the GZMK/FGFBP2 effector populations, and were also present in the CCL4 effector and IKZF2 TRM(2) population.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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γδ T cells were uncommon within IFNG TRM(2) and cycling clusters.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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TRDV1 and TRDV3 expression was higher in the CCL4, IKZF2 TRM(2) and natural IEL populations, with TRDV3 in particular enriched in the natural IEL cluster (Extended Data Fig. 8f).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We analyzed the TCR repertoire of CD8 T cells in this dataset.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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The TRM and IL7R clusters showed greatest clonal expansion (Extended Data Fig. 8g).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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In all participants with CD, TRBV28-containing clonotypes were more clonally expanded than their non-TRBV28 counterparts.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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TRBV28 clonotypes were enriched in the top quintile of expanded clones, which were almost exclusively found within the TRM(2) and cycling clusters (Extended Data Fig. 8h,i).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We validated these findings through bulk RNA-seq of sorted intestinal αβ CD8 and γδ T cells from participants with and without CD (dataset 6).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Gene-set enrichment analysis of CD8 T cell gene expression in ACD showed upregulation of TCR activation gene sets, and enrichment of cluster marker gene sets from TRM(2) and cycling populations (Supplementary Fig. 3a–c), with upregulation of CXCR6, ENTPD1 and MKI67 (Supplementary Fig. 3d).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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CD8 T cells showed upregulation of IFNG and IL26 (Supplementary Fig. 3e).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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There was a shift from KLRC1 (NKG2A) to KLRC2 (NKG2C) expression, but KLRK1 (NKG2D) expression was not increased.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Inhibitory KIRs were upregulated in this dataset, consistent with recent findings.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Gene expression between health and CD was different in γδ and αβ CD8 T cells (Supplementary Fig. 3f,g).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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IFNG and MKI67 expression were not increased to the same extent in γδ T cells, nor were TRM(2) IFNG cluster markers like ENTPD1.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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There were also differences in NK cell receptor changes, KIRs, PDCD1 and TYROBP, a natural IEL marker (Supplementary Fig. 3h).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Bulk γδ TCR repertoire sequencing (dataset 7) revealed a skewed TRGV repertoire, with reduced TRGV4 and increased TRGV3 use in ACD (Supplementary Fig. 4a,b), which persisted after treatment, as previously described.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Most TRD CDR3 sequences were private; however, increased sequence sharing was noted between ACD repertoires (Supplementary Fig. 4c), with longer shared CDR3 sequences in ACD (Supplementary Fig. 4d).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Previously reported CD-associated TRDV CDR3 motifs, were increased in ACD; however, we were unable to replicate the previously described association between the TRDV H-J1 motif and CD (Supplementary Fig. 4e–i).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Samples from adults with TCD (GFD with good symptomatic, serological and histological response) were included in scRNA-seq, bulk RNA-seq and TCR-seq experiments (Supplementary Table 1).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We hypothesized that cell-type and transcriptional changes would normalize with treatment.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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However, many biological changes persisted.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Specifically, EC changes including increased TA cell proportions and cycling cells (Extended Data Fig. 1b–e) and the shift toward progenitor states (Fig. 2f) persisted despite treatment.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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EEC changes also persisted.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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However, absorptive function gene expression within mature enterocytes had predominantly normalized, aside from the ongoing reduction in fructose metabolism and lipid catabolism (Extended Data Fig. 1g).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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While TFH-like CD4 T cells and Treg cells returned toward control levels on treatment, the CD8 compartment remained perturbed, with reduced natural IELs and increases in TRM(2) CD8 T cells.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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However, the TRM(2) population showed reduced activation in TCD (lower IFNG, IL32 and pro-inflammatory markers).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Intestinal CD8 TCR repertoire changes remained (specifically TRBV28 enrichment), as did increased circulating TRBV28 gut-homing CD8 T cells.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We next analyzed duodenal stromal and endothelial populations in CD (dataset 3; Supplementary Fig. 5a–d).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Annotation of stromal populations based on previous descriptions showed S1, S2 and S3 fibroblasts, as well as myofibroblasts, with S1 fibroblasts most common in the duodenum.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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The pro-inflammatory S4 phenotype seen in colonic inflammatory bowel disease was not seen.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Differential gene expression and gene-set enrichment analysis showed upregulation of interferon-induced genes including STAT1, the major histocompatibility complex class II invariant chain (CD74), and SLIT2, encoding a secreted protein involved in intestinal homeostasis (Supplementary Fig. 5e,f).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Analysis of endothelial cells revealed arterial, capillary, venous and lymphatic populations, with upregulation of interferon-stimulated genes in CD (Supplementary Fig. 5g–i).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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We next performed spatial transcriptomics on duodenal biopsy samples (dataset 4; Fig. 6).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Spatial transcriptomics showed 13 transcriptionally distinct regions within the mucosa, representing compartments of the crypt–villus axis (stem cell niche, lower-crypt and mid-crypt regions and villus zones), stromal cell-rich regions, several lamina propria regions with immune cell infiltrates dominated by plasma cell signatures and lymphoid aggregates (LAs; Fig. 6a,b).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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In health, the epithelial villus compartments dominated; these were reduced in ACD (Fig. 6c–e).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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These villus regions expressed absorptive function genes, predominantly in the most mature villus compartment (Fig. 6b and Supplementary Fig. 6b).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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In contrast, immune-rich regions and LAs were greatly expanded in ACD (Fig. 6d,e).
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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These regions were themselves spatially organized, with LAs closely associated with lower-crypt and immune-rich regions, and telocyte-rich regions with villus structures (Fig. 6g).Fig.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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6Spatial transcriptomics of the intestinal mucosa reveals localized patterns of immune cell distribution.a, UMAP overlay of all spatial transcriptomics tissue-covered spots with transcriptome-driven clustering analysis, colored by region.
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PMC12133578
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Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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b, Bubble plot showing the expression of selected genes defining spatial regions.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
Scaled gene expression indicated by color; proportion of cells expressing the gene indicated by bubble size.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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c, Visualization of transcriptionally distinct spatial regions overlaid on representative HC tissue section.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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d, Proportion of intestinal mucosa formed in different regions in HCs (above) and ACD (below).
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Immune-rich and LA regions are highlighted.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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e, Local neighborhood enrichment of intestinal mucosal regions in ACD versus HCs.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Color indicates enrichment (log fold change) of cells in ACD versus HCs in that UMAP neighborhood.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
f, Volcano plot of differential gene expression between HCs and ACD within villus tip spatial regions.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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g, The spatial relationships between different regions in ACD can be visualized using a network plot.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
Regions that are more likely to be adjacent to another region are connected by arrows colored by the percentage of adjacent spots.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Region size is indicated by size and color of the region circle.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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h, Integrating scRNA-seq reference data localizes single-cell transcriptomes to spatial regions.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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These data are used to generate network plots visualizing colocalization of cell types together in ACD.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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Cell-type nodes close together and linked by connecting lines are more often located in the same spots.
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
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In ACD, mature enterocytes colocalize with TRM(2) CD8 T cells (lower red box), while TFH-like CD4 T cells localize with B cells, Treg cells and plasma cells (upper red box).
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PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
a, UMAP overlay of all spatial transcriptomics tissue-covered spots with transcriptome-driven clustering analysis, colored by region.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
b, Bubble plot showing the expression of selected genes defining spatial regions.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
Scaled gene expression indicated by color; proportion of cells expressing the gene indicated by bubble size.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
c, Visualization of transcriptionally distinct spatial regions overlaid on representative HC tissue section.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
d, Proportion of intestinal mucosa formed in different regions in HCs (above) and ACD (below).
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
Immune-rich and LA regions are highlighted.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
e, Local neighborhood enrichment of intestinal mucosal regions in ACD versus HCs.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
Color indicates enrichment (log fold change) of cells in ACD versus HCs in that UMAP neighborhood.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
f, Volcano plot of differential gene expression between HCs and ACD within villus tip spatial regions.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
g, The spatial relationships between different regions in ACD can be visualized using a network plot.
|
PMC12133578
|
Immune-epithelial-stromal networks define the cellular ecosystem of the small intestine in celiac disease.
|
Regions that are more likely to be adjacent to another region are connected by arrows colored by the percentage of adjacent spots.
|
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