The small and large intestine contain related mesenchymal subsets that derive from embryonic Gli1+ precursors

Simone Isling Pærregaard, Line Wulff, Sophie Schussek, Kristoffer Niss, Urs Mörbe, Johan Jendholm, Kerstin Wendland, Anna T. Andrusaite, Kevin F. Brulois, Robert J. B. Nibbs, Katarzyna Sitnik, Allan McI Mowat, Eugene C. Butcher, Søren Brunak and William W. Agace ()
Additional contact information
Simone Isling Pærregaard: Technical University of Denmark, Kemitorvet
Line Wulff: Technical University of Denmark, Kemitorvet
Sophie Schussek: Technical University of Denmark, Kemitorvet
Kristoffer Niss: University of Copenhagen
Urs Mörbe: Technical University of Denmark, Kemitorvet
Johan Jendholm: Technical University of Denmark, Kemitorvet
Kerstin Wendland: Lund University
Anna T. Andrusaite: University of Glasgow
Kevin F. Brulois: Stanford University
Robert J. B. Nibbs: University of Glasgow
Katarzyna Sitnik: Technical University of Denmark, Kemitorvet
Allan McI Mowat: University of Glasgow
Eugene C. Butcher: Stanford University
Søren Brunak: University of Copenhagen
William W. Agace: Technical University of Denmark, Kemitorvet

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract The intestinal lamina propria contains a diverse network of fibroblasts that provide key support functions to cells within their local environment. Despite this, our understanding of the diversity, location and ontogeny of fibroblasts within and along the length of the intestine remains incomplete. Here we show that the small and large intestinal lamina propria contain similar fibroblast subsets that locate in specific anatomical niches. Nevertheless, we find that the transcriptional profile of similar fibroblast subsets differs markedly between the small intestine and colon suggesting region specific functions. We perform in vivo transplantation and lineage-tracing experiments to demonstrate that adult intestinal fibroblast subsets, smooth muscle cells and pericytes derive from Gli1-expressing precursors present in embryonic day 12.5 intestine. Trajectory analysis of single cell RNA-seq datasets of E12.5 and adult mesenchymal cells suggest that adult smooth muscle cells and fibroblasts derive from distinct embryonic intermediates and that adult fibroblast subsets develop in a linear trajectory from CD81+ fibroblasts. Finally, we provide evidence that colonic subepithelial PDGFRαhi fibroblasts comprise several functionally distinct populations that originate from an Fgfr2-expressing fibroblast intermediate. Our results provide insights into intestinal stromal cell diversity, location, function, and ontogeny, with implications for intestinal development and homeostasis.

Date: 2023
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DOI: 10.1038/s41467-023-37952-5

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