Department of Gynaecology and Obstetrics, Xijing Hospital, Air Force Medical University, Xi'an, China.
Apoptosis. 2024 Aug;29(7-8):1232-1245. doi: 10.1007/s10495-024-01962-5. Epub 2024 Apr 13.
MARCH5 is a ring-finger E3 ubiquitin ligase located in the outer membrane of mitochondria. A previous study has reported that MARCH5 was up-regulated and contributed to the migration and invasion of OC cells by serving as a competing endogenous RNA. However, as a mitochondrial localized E3 ubiquitin ligase, the function of MARCH5 in mitochondrial-associated metabolism reprogramming in human cancers remains largely unexplored, including OC. We first assessed the glycolysis effect of MARCH5 in OC both in vitro and in vivo. Then we analyzed the effect of MARCH5 knockdown or overexpression on respiratory activity by evaluating oxygen consumption rate, activities of OXPHOS complexes and production of ATP in OC cells with MARCH5. Co-immunoprecipitation, western-blot, and in vitro and vivo experiments were performed to investigate the molecular mechanisms underlying MARCH5-enhanced aerobic glycolysis s in OC. In this study, we demonstrate that the abnormal upregulation of MARCH5 is accompanied by significantly increased aerobic glycolysis in OC. Mechanistically, MARCH5 promotes aerobic glycolysis via ubiquitinating and degrading mitochondrial pyruvate carrier 1 (MPC1), which mediates the transport of cytosolic pyruvate into mitochondria by localizing on mitochondria outer membrane. In line with this, MPC1 expression is significantly decreased and its downregulation is closely correlated with unfavorable survival. Furthermore, in vitro and in vivo assays revealed that MARCH5 upregulation-enhanced aerobic glycolysis played a critical role in the proliferation and metastasis of OC cells. Taken together, we identify a MARCH5-regulated aerobic glycolysis mechanism by degradation of MPC1, and provide a rationale for therapeutic targeting of aerobic glycolysis via MARCH5-MPC1 axis inhibition.
MARCH5 是一种位于线粒体外膜的指环指 E3 泛素连接酶。先前的研究报道,MARCH5 上调并通过作为竞争性内源性 RNA 促进 OC 细胞的迁移和侵袭。然而,作为一种定位于线粒体的 E3 泛素连接酶,MARCH5 在人类癌症中线粒体相关代谢重编程中的作用在很大程度上仍未得到探索,包括 OC。我们首先评估了 MARCH5 在 OC 中的体外和体内的糖酵解作用。然后,我们通过评估 OC 细胞中的耗氧量、OXPHOS 复合物的活性和 ATP 的产生,分析了 MARCH5 敲低或过表达对呼吸活性的影响。通过共免疫沉淀、Western blot 以及体内和体外实验,研究了 MARCH5 增强 OC 有氧糖酵解的分子机制。在这项研究中,我们证明了 MARCH5 的异常上调伴随着 OC 中明显增加的有氧糖酵解。从机制上讲,MARCH5 通过泛素化和降解线粒体丙酮酸载体 1(MPC1)来促进有氧糖酵解,MPC1 通过定位于线粒体外膜来介导细胞质丙酮酸向线粒体的转运。与此一致的是,MPC1 的表达显著降低,其下调与不良生存密切相关。此外,体外和体内实验表明,MARCH5 上调增强的有氧糖酵解在 OC 细胞的增殖和转移中发挥了关键作用。总之,我们通过 MPC1 的降解鉴定了一种由 MARCH5 调节的有氧糖酵解机制,并为通过 MARCH5-MPC1 轴抑制靶向有氧糖酵解提供了依据。