RIPK3-mediated dysregulated arachidonic acid metabolism in necroptosis contributes to sepsis-associated intestinal injury by driving epithelial cell ferroptosis and mitochondrial fission

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Authors: Liting Deng, Huan Yang, Yue Chao, 邱明杰, Peiyang Wang, Haiyang Jiang, Zexing Lin, Xufei Zhang, Chujun Ni, Xuanheng Li, Peizhao Liu, Luyao Wang
+8 more Xinya Fu, Jianghao Zou, Rui Ma, Jie Liu, Yeting Zhu, Yuanzhang Zhao, Jianan Ren, Xiuwen Wu
Cited by: 1
References: 46

Abstract

Here, we identify a necroptosis-lipid mediator-receptor axis that links epithelial danger signaling in sepsis to crosstalk among regulated cell-death pathways. Integrated in vivo and in vitro transcriptomic analyses together with targeted arachidonic acid metabolomics revealed that necroptotic intestinal epithelial cells (IECs) upregulate PTGS2 and PTGES, synthesize prostaglandin E 2 (PGE 2 ), and release it in a RIPK3- and PTGS2-dependent manner. Mechanistically, RIPK3 interacted with STAT1 and promoted its phosphorylation and nuclear translocation, thereby enhancing PTGS2/PTGES transcription. Conditioned media from necroptotic IECs induced cell death in lipopolysaccharide (LPS)-primed recipient IECs across species and organoid models, and this effect was prevented by the ferroptosis inhibitor ferrostatin-1, accompanied by suppression of mitochondrial fission and preservation of mitochondrial membrane potential. Pharmacological inhibition of E-prostanoid receptor 1 (EP1) reduced cell death in LPS-activated IECs, preserved mitochondrial morphology, and improved organoid integrity. In septic mice, both genetic Ripk3 deficiency and pharmacological EP1 blockade improved survival, reduced plasma alanine aminotransferase (ALT) and creatine kinase (CK), lowered intestinal injury markers D-lactate and intestinal fatty acid–binding protein (I-FABP), and alleviated villus and crypt damage. In a clinical cohort, circulating PGE 2 levels were significantly elevated in patients with sepsis and were positively correlated with I-FABP and D-lactate, supporting a link between PGE 2 and intestinal injury in human sepsis. Collectively, these findings define a necroptosis-PGE 2 -ferroptosis program in which necroptotic epithelia generate pathogenic PGE 2 through a RIPK3-STAT1-PTGS2/PTGES pathway, whereas EP1-dependent ferroptotic signaling converts this lipid cue into mitochondrial dysfunction and intestinal barrier injury. These results identify selective EP1 blockade as a potential therapeutic strategy for sepsis-associated intestinal injury.

Fields of Study & Subjects

Ferroptosis and cancer prognosis Cell death mechanisms and regulation Autophagy in Disease and Therapy

Publication details

Journal / source
Genes & Diseases
Publisher
Elsevier BV
Pages
102307–102307
Publication date
1 June 2026
Language
EN