Language

English

Publication Date

10-3-2024

Journal

Cell Stem Cell

DOI

10.1016/j.stem.2024.08.006

PMID

39232559

PMCID

PMC11963838

PubMedCentral® Posted Date

10-3-2025

PubMedCentral® Full Text Version

Author MSS

Abstract

It remains unknown whether, and how intestinal stem cells (ISC) adapt to inflammatory exposure, and if the adaptation leaves scars will affect their subsequent regeneration. We investigated the consequences of inflammation on Lgr5+ISCs in well-defined clinically relevant models of gastrointestinal acute graft-versus-host disease (GI GVHD). Utilizing single cell transcriptomics, organoid, metabolic, epigenomic and in vivo models we found that Lgr5+ISCs undergo metabolic changes that lead to accumulation of succinate, which reprograms its epigenome. These changes reduced the ability of ISCs to differentiate and regenerate ex vivo in serial organoid cultures and also in vivo following serial transplantation. Furthermore, ISCs demonstrated a reduced capacity for in vivo regeneration despite resolution of the initial inflammatory exposure demonstrating the persistence of the maladaptive impact induced by the inflammatory encounter. Thus, inflammation imprints the epigenome of ISCs that persists and affects their sensitivity to adapt to future stress or challenges.

Keywords

Animals, Inflammation, Epigenesis, Genetic, Stem Cells, Mice, Intestines, Genomic Imprinting, Mice, Inbred C57BL, Graft vs Host Disease, Regeneration, Cell Differentiation, Receptors, G-Protein-Coupled, Organoids

Published Open-Access

yes

nihms-2017912-f0001.jpg (232 kB)
Graphical Abstract

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