Tubular-Cell-Derived Extracellular Vesicle miR-491-3p Aggravates Renal Ischemia-Reperfusion Injury by Inhibiting Macrophage SIRT1-Mediated Notch Intracellular Domain Deacetylation-Driven Ubiquitin-Proteasome Degradation

肾小管细胞来源的细胞外囊泡 miR-491-3p 通过抑制巨噬细胞 SIRT1 介导的 Notch 胞内结构域去乙酰化驱动的泛素-蛋白酶体降解加重肾脏缺血再灌注损伤

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Abstract

Renal ischemia-reperfusion injury triggers substantial inflammatory reactions, with renal tubular epithelial cells (TECs) and macrophages playing crucial roles. Extracellular vesicles (EVs) are key mediators of intercellular signaling. However, the precise roles and mechanisms by which TEC-derived EVs influence macrophage functions remain unclear. This study investigated how miR-491-3p within EVs from TECs modulates macrophage polarization, thus worsening renal inflammation and damage. In models that are in vitro and in vivo, EVs enriched with miR-491-3p from TECs subjected to hypoxia/reoxygenation were shown to promote M1 polarization in macrophages, enhancing inflammatory responses and inducing TEC apoptosis. Mechanistically, miR-491-3p directly targets sirtuin 1 (SIRT1) in macrophages, inhibiting SIRT1-mediated Notch intracellular domain (NICD) deacetylation, thereby regulating NICD stability. This regulation blocks F-box and WD repeat domain-containing 7 (FBXW7)-NICD binding, reduces NICD ubiquitination, and activates the Notch/nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) pathway. Furthermore, Rab27a knockout, which limits EVs' release, substantially reduces M1 macrophage polarization and renal tissue damage. These findings indicate that miR-491-3p from TEC-derived EVs targets SIRT1, inhibiting the deacetylation of NICD mediated by SIRT1, which subsequently prevents ubiquitin-mediated NICD degradation. This mechanism modulates the inflammatory phenotype of macrophages and promotes the inflammatory response, thereby worsening renal injury induced by ischemia-reperfusion injury and highlighting a potential therapeutic target.

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