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Immune–epithelial–stromal networks define the cellular ecosystem of the small intestine in celiac disease

Abstract:

The immune–epithelial–stromal interactions underpinning intestinal damage in celiac disease (CD) are incompletely understood. To address this, we performed single-cell transcriptomics (RNA sequencing; 86,442 immune, parenchymal and epithelial cells; 35 participants) and spatial transcriptomics (20 participants) on CD intestinal biopsy samples. Here we show that in CD, epithelial populations shifted toward a progenitor state, with interferon-driven transcriptional responses, and perturbation of secretory and enteroendocrine populations. Mucosal T cells showed numeric and functional changes in regulatory and follicular helper-like CD4+ T cells, intraepithelial lymphocytes, CD8+ and γδ T cell subsets, with skewed T cell antigen receptor repertoires. Mucosal changes remained detectable despite treatment, representing a persistent immune–epithelial ‘scar’. Spatial transcriptomics defined transcriptional niches beyond those captured in conventional histological scores, including CD-specific lymphoid aggregates containing T cell–B cell interactions. Receptor–ligand spatial analyses integrated with disease susceptibility gene expression defined networks of altered chemokine and morphogen signaling, and provide potential therapeutic targets for CD prevention and treatment.

Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s41590-025-02146-2

Authors


More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDM
Sub department:
NDM Experimental Medicine
Oxford college:
Trinity College
Role:
Author
ORCID:
0000-0003-2365-2012
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Inst of Molecular Medicine
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDM
Sub department:
Centre for Human Genetics
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Inst of Molecular Medicine
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDM
Sub department:
Centre for Human Genetics
Role:
Author


More from this funder
Funder identifier:
https://ror.org/00c489v88
Grant:
SGL025\1066


Publisher:
Springer Nature
Journal:
Nature Immunology More from this journal
Volume:
26
Issue:
6
Pages:
947-962
Publication date:
2025-05-06
Acceptance date:
2025-03-25
DOI:
EISSN:
1529-2916
ISSN:
1529-2908


Language:
English
Keywords:
Pubs id:
2100687
Local pid:
pubs:2100687
Deposit date:
2025-03-27

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