Nutrient starvation activates ECM remodeling gene enhancers associated with inflammatory bowel disease risk in fibroblasts

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The paper studied how serum nutrient deprivation affects fibroblast transcription and chromatin regulation, using cultured fibroblasts exposed to starvation conditions that induce a quiescence cell-cycle arrest. Despite quiescence-associated transcriptional silencing and chromatin compaction, serum deprivation extensively activated transcription of extracellular matrix (ECM) remodeling genes, accompanied by large-scale histone acetylation at putative distal enhancers rather than promoters. The starvation-activated enhancers were enriched for inflammatory bowel disease (IBD) non-coding risk variants, and the authors found that the ECM-related gene PLAU and its IBD-linked enhancer were upregulated and gained chromatin accessibility in inflammatory fibroblasts from intestinal tissue of IBD patients. The paper is limited to fibroblast models and tissue correlations rather than direct demonstration of nutrient deprivation as a causal driver in vivo. Relevance to endometriosis: the work does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

ABSTRACT Nutrient deprivation induces a reversible cell cycle arrest state termed quiescence, which often accompanies transcriptional silencing and chromatin compaction. Paradoxically, nutrient deprivation is associated with activated fibroblast states in pathological microenvironments in which fibroblasts drive extracellular matrix (ECM) remodeling to alter tissue environments. The relationship between nutrient deprivation and fibroblast activation remains unclear. Here, we report that serum deprivation extensively activates transcription of ECM remodeling genes in cultured fibroblasts, despite the induction of quiescence. Starvation-induced transcriptional activation accompanied large-scale histone acetylation of putative distal enhancers, but not promoters. The starvation-activated putative enhancers were enriched for non-coding genetic risk variants associated with inflammatory bowel disease (IBD), suggesting that the starvation-activated gene regulatory network may contribute to fibroblast activation in IBD. Indeed, the starvation-activated gene PLAU , encoding uPA serine protease for plasminogen and ECM, was upregulated in inflammatory fibroblasts in the intestines of IBD patients. Furthermore, the starvation-activated putative enhancer at PLAU , which harbors an IBD risk variant, gained chromatin accessibility in IBD patient fibroblasts. This study implicates nutrient deprivation in transcriptional activation of ECM remodeling genes in fibroblasts and suggests nutrient deprivation as a potential mechanism for pathological fibroblast activation in IBD. HIGHLIGHTS - Serum starvation transcriptionally activates ECM remodeling genes in fibroblasts. - Fibroblast starvation activates putative distal enhancers associated with ECM remodeling genes. - Starvation-activated putative enhancers are enriched for inflammatory bowel disease (IBD) risk variants. - PLAU enhancer and expression are activated in IBD intestinal fibroblasts, as in starved fibroblasts.
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ABSTRACT Nutrient deprivation induces a reversible cell cycle arrest state termed quiescence, which often accompanies transcriptional silencing and chromatin compaction. Paradoxically, nutrient deprivation is associated with activated fibroblast states in pathological microenvironments in which fibroblasts drive extracellular matrix (ECM) remodeling to alter tissue environments. The relationship between nutrient deprivation and fibroblast activation remains unclear. Here, we report that serum deprivation extensively activates transcription of ECM remodeling genes in cultured fibroblasts, despite the induction of quiescence. Starvation-induced transcriptional activation accompanied large-scale histone acetylation of putative distal enhancers, but not promoters. The starvation-activated putative enhancers were enriched for non-coding genetic risk variants associated with inflammatory bowel disease (IBD), suggesting that the starvation-activated gene regulatory network may contribute to fibroblast activation in IBD. Indeed, the starvation-activated gene PLAU, encoding uPA serine protease for plasminogen and ECM, was upregulated in inflammatory fibroblasts in the intestines of IBD patients. Furthermore, the starvation-activated putative enhancer at PLAU, which harbors an IBD risk variant, gained chromatin accessibility in IBD patient fibroblasts. This study implicates nutrient deprivation in transcriptional activation of ECM remodeling genes in fibroblasts and suggests nutrient deprivation as a potential mechanism for pathological fibroblast activation in IBD. HIGHLIGHTS - Serum starvation transcriptionally activates ECM remodeling genes in fibroblasts. - Fibroblast starvation activates putative distal enhancers associated with ECM remodeling genes. - Starvation-activated putative enhancers are enriched for inflammatory bowel disease (IBD) risk variants. - PLAU enhancer and expression are activated in IBD intestinal fibroblasts, as in starved fibroblasts. Competing Interest Statement The authors have declared no competing interest.

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License: CC-BY-NC-ND-4.0