PRIP/PLCL deficiency activates PI3K-AKT-YAP signaling and promotes organ fibrosis

PRIP/PLCL 缺乏激活 PI3K-AKT-YAP 信号通路并促进器官纤维化

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Abstract

BACKGROUND: Fibrosis, a hallmark of multiple chronic diseases, is regulated by transforming growth factor beta (TGF-β)-mediated PI3K-AKT signaling. Phospholipase C-related catalytically inactive protein (PRIP), also known as phospholipase C-like protein (PLCL) in humans, acts as a negative regulator of PI3K-AKT signaling. However, the role of PRIP/PLCL in fibrotic remodeling and its underlying molecular mechanisms remain unclear. Therefore, we investigated the involvement of PRIP/PLCL in fibrogenesis. METHODS: Bioinformatics analyses were performed to determine the relationship between PRIP/PLCL and fibrosis, as well as its involvement in fibrotic signaling pathways. For in vivo experiments, we developed a mouse fibrosis model using male wild-type (WT) and Prip- knockout (KO) mice treated with angiotensin II (Ang II) to evaluate fibrogenesis in the kidney and heart. For in vitro experiments, we treated mouse embryonic fibroblasts (MEFs) from WT and Prip-KO mice with TGF-β1 (5 ng/ml) to verify PRIP/PLCL-modulated signaling in fibrosis using qPCR and western blotting. RESULTS: Bioinformatics analyses revealed that PRIP/PLCL expression was significantly downregulated in fibrotic tissues and negatively correlated with the severity of renal fibrosis. Prip-KO mice exhibited accelerated fibrogenesis in the kidneys and heart following Ang II treatment. Consistently, PRIP deficiency exacerbated TGF-β1-induced fibroblast activation in MEFs. Gene set enrichment analysis of genes ranked by their correlation with PLCL expression revealed significant negative enrichment of the PI3K-AKT and Hippo signaling pathways. Accordingly, loss of PRIP enhanced AKT activation, promoted MST2 phosphorylation at Thr117, and facilitated the nuclear translocation of yes-associated protein (YAP), a core effector of the Hippo pathway and driver of fibrogenesis, leading to increased YAP-dependent profibrotic activity in TGF-β1-stimulated Prip-knockout MEFs. CONCLUSION: PRIP/PLCL deficiency mediates YAP activation via the PI3K-AKT-MST2 axis, thereby accelerating fibroblast activation and organ fibrotic remodeling. Collectively, PRIP/PLCL acts as a novel anti-fibrotic factor, and restoring its activity could be an effective therapeutic approach for treating fibrotic diseases.

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