Background and Aims
Characterising how the epithelial barrier interacts with its surrounding microenvironment is essential for understanding intestinal remodelling in celiac disease (CeD). We previously used low resolution spatial transcriptomics (ST) to localise disease processes within the intestinal mucosa, describing changes in epithelial gene expression and identifying lymphoid aggregates as potential sites of gluten-specific immune interactions (1). We sought to perform sub-cellular resolution mapping of the CeD duodenum, focusing on how immune and stromal cells influence epithelial function.
Materials and Methods
We performed sub-cellular resolution imaging-based ST (Xenium, 10x Genomics) on 40 duodenal biopsy sections (active CeD (ACD), n=16; treated CeD (TCD), n=10; potential CeD (PCD), n=3; non-celiac controls (NCC), n=11) with a panel of 5101 genes.
Results
Our dataset of 170 million transcripts across more than 800,000 cells allowed detailed mapping of CeD-associated changes to the digestive and protective functions of the epithelium along the crypt-villus axis, including zonated changes to immune response and absorption pathways and localised shifts toward a gastric phenotype. We linked these changes with phenotypic shifts in surrounding stromal cells and matrix metalloproteinase (MMP)-expressing macrophages which may contribute to remodelling through persistent inflammation, wound-healing responses, and changes in extracellular matrix organisation. We identified further lymphoid aggregates in both ACD and TCD, in some cases exhibiting follicle-like structure with separate T- and B-cell areas, dendritic cells, MMP-expressing macrophages, and a specialised epithelium with antigen-presenting capacity (M cells) as well as pro-inflammatory stromal populations associated with lymphoid follicle formation in other autoimmune conditions (2).
Conclusions
Using ST, we have characterised crosstalk with stromal and immune cells as a driver of epithelial reprogramming and tissue remodelling and identified lymphoid aggregates as specialised sites of adaptive immune activity in CeD.