Liu Lingpeng, Che Ben, Zhang Wenming, Du Dongnian, Zhang Dandan, Li Jiajuan, Chen Zehao, Yu Xuzhe, Ye Miao, Wang Wei, Li Zijing, Xie Fei, Wang Qing, Chen Leifeng, Shao Jianghua
Department of General Surgery, Second Affiliated Hospital of Nanchang University, Nanchang, China.
Jiangxi Province Key Laboratory of Molecular Medicine, Second Affiliated Hospital of Nanchang University, Nanchang, China.
Cell Death Dis. 2025 May 15;16(1):385. doi: 10.1038/s41419-025-07715-9.
Acute pancreatitis (AP) is characterised by inflammation and cell death in pancreatic tissue, with ferroptosis playing a critical role in its pathophysiology by mediating cellular damage and exacerbating inflammation. This study investigated the role of human leukocyte antigen (HLA)-F adjacent transcript 10 (FAT10) in AP, specifically its involvement in ferroptosis within pancreatic acinar cells. We observed that FAT10 expression was significantly elevated in AP tissues, which correlated with increased ferroptosis. Overexpression of FAT10 in pancreatic acinar cells enhances ferroptosis, whereas its knockdown reduced levels of ferroptosis markers. Furthermore, we confirmed that FAT10 enhanced ferroptosis in pancreatic acinar cells primarily by upregulating nuclear receptor coactivator 4 (NCOA4) expression. Mechanistic investigations revealed that FAT10 regulates NCOA4 expression to promote ferroptosis in a complex manner. FAT10 inhibits NCOA4 ubiquitination by reducing ubiquitin-NCOA4 complexes. Meanwhile, NCOA4 expression increased alongside the increase in FAT10-NCOA4 complexes, which are resistant to proteasomal degradation. Notably, we identified silibinin, a natural compound, as an effective inhibitor of the FAT10-NCOA4 axis, leading to reduced ferroptosis and alleviation of pancreatic damage in vivo. Silibinin treatment decreased the levels of ferroptosis-related proteins and inflammatory markers in both cell and animal models. Our findings highlight the FAT10-NCOA4 axis as a crucial regulator of ferroptosis in pancreatic acinar cells and suggest that targeting this pathway could offer a therapeutic strategy for mitigating AP. This study provides new insights into the regulatory mechanisms of ferroptosis in pancreatic acinar cells, identifying FAT10 as a potential therapeutic target for AP management.
急性胰腺炎(AP)的特征是胰腺组织发生炎症和细胞死亡,铁死亡在其病理生理学中起着关键作用,通过介导细胞损伤和加剧炎症。本研究调查了人类白细胞抗原(HLA)-F相邻转录本10(FAT10)在AP中的作用,特别是其在胰腺腺泡细胞铁死亡中的参与情况。我们观察到,FAT10在AP组织中的表达显著升高,这与铁死亡增加相关。在胰腺腺泡细胞中过表达FAT10可增强铁死亡,而敲低其表达则降低了铁死亡标志物的水平。此外,我们证实FAT10主要通过上调核受体辅激活因子4(NCOA4)的表达来增强胰腺腺泡细胞中的铁死亡。机制研究表明,FAT10以复杂的方式调节NCOA4的表达以促进铁死亡。FAT10通过减少泛素-NCOA4复合物来抑制NCOA4的泛素化。同时,NCOA4的表达随着FAT10-NCOA4复合物的增加而增加,而这些复合物对蛋白酶体降解具有抗性。值得注意的是,我们鉴定出天然化合物水飞蓟宾是FAT10-NCOA4轴的有效抑制剂,可导致体内铁死亡减少和胰腺损伤减轻。水飞蓟宾治疗降低了细胞和动物模型中与铁死亡相关的蛋白质水平和炎症标志物。我们的研究结果突出了FAT10-NCOA4轴作为胰腺腺泡细胞铁死亡的关键调节因子,并表明靶向该途径可能为减轻AP提供一种治疗策略。本研究为胰腺腺泡细胞中铁死亡的调节机制提供了新的见解,将FAT10确定为AP管理的潜在治疗靶点。