National & Local Joint Engineering Research Center of High throughput Drug Screening Technology, Hubei Province Key Laboratory of Biotechnology of Chinese Traditional Medicine, College of Health Science and Engineering, Hubei University, Wuhan 430062, China.
Int J Mol Sci. 2024 Jul 19;25(14):7897. doi: 10.3390/ijms25147897.
Non-alcoholic fatty liver disease (NAFLD) has emerged as the leading cause of chronic liver disease worldwide. Caspase 8 and FADD-like apoptosis regulator (CFLAR) has been identified as a potent factor in mitigating non-alcoholic steatohepatitis (NASH) by inhibiting the N-terminal dimerization of apoptosis signal-regulating kinase 1 (ASK1). While arginine methyltransferase 1 (PRMT1) was previously reported to be associated with increased hepatic glucose production, its involvement in hepatic lipid metabolism remains largely unexplored. The interaction between PRMT1 and CFLAR and the methylation of CFLAR were verified by Co-IP and immunoblotting assays. Recombinant adenoviruses were generated for overexpression or knockdown of PRMT1 in hepatocytes. The role of PRMT1 in NAFLD was investigated in normal and high-fat diet-induced obese mice. In this study, we found a significant upregulation of PRMT1 and downregulation of CFLAR after 48h of fasting, while the latter significantly rebounded after 12h of refeeding. The expression of PRMT1 increased in the livers of mice fed a methionine choline-deficient (MCD) diet and in hepatocytes challenged with oleic acid (OA)/palmitic acid (PA). Overexpression of PRMT1 not only inhibited the expression of genes involved in fatty acid oxidation (FAO) and promoted the expression of genes involved in fatty acid synthesis (FAS), resulting in increased triglyceride accumulation in primary hepatocytes, but also enhanced the gluconeogenesis of primary hepatocytes. Conversely, knockdown of hepatic PRMT1 significantly alleviated MCD diet-induced hepatic lipid metabolism abnormalities and liver injury in vivo, possibly through the upregulation of CFLAR protein levels. Knockdown of PRMT1 suppressed the expression of genes related to FAS and enhanced the expression of genes involved in FAO, causing decreased triglyceride accumulation in OA/PA-treated primary hepatocytes in vitro. Although short-term overexpression of PRMT1 had no significant effect on hepatic triglyceride levels under physiological conditions, it resulted in increased serum triglyceride and fasting blood glucose levels in normal C57BL/6J mice. More importantly, PRMT1 was observed to interact with and methylate CFLAR, ultimately leading to its ubiquitination-mediated protein degradation. This process subsequently triggered the activation of c-Jun N-terminal kinase 1 (JNK1) and lipid deposition in primary hepatocytes. Together, these results suggested that PRMT1-mediated methylation of CFLAR plays a critical role in hepatic lipid metabolism. Targeting PRMT1 for drug design may represent a promising strategy for the treatment of NAFLD.
非酒精性脂肪性肝病(NAFLD)已成为全球慢性肝病的主要病因。半胱天冬酶 8 和 FADD 样凋亡调节剂(CFLAR)已被确定为通过抑制凋亡信号调节激酶 1(ASK1)的 N 端二聚化来减轻非酒精性脂肪性肝炎(NASH)的有效因素。虽然先前已有报道称精氨酸甲基转移酶 1(PRMT1)与肝葡萄糖产生增加有关,但它在肝脂代谢中的作用在很大程度上仍未得到探索。通过 Co-IP 和免疫印迹实验验证了 PRMT1 和 CFLAR 之间的相互作用以及 CFLAR 的甲基化。生成重组腺病毒以在肝细胞中过表达或敲低 PRMT1。在正常和高脂肪饮食诱导肥胖的小鼠中研究了 PRMT1 在 NAFLD 中的作用。在这项研究中,我们发现禁食 48 小时后 PRMT1 的表达显著上调,而 CFLAR 的表达显著下调,而在重新喂食 12 小时后后者显著反弹。在给予蛋氨酸胆碱缺乏(MCD)饮食的小鼠肝脏和油酸(OA)/棕榈酸(PA)处理的肝细胞中,PRMT1 的表达增加。PRMT1 的过表达不仅抑制了脂肪酸氧化(FAO)相关基因的表达,促进了脂肪酸合成(FAS)相关基因的表达,导致原代肝细胞中甘油三酯积累增加,而且增强了原代肝细胞的糖异生。相反,肝 PRMT1 的敲低显著缓解了体内 MCD 饮食诱导的肝脂质代谢异常和肝损伤,可能是通过上调 CFLAR 蛋白水平。敲低 PRMT1 抑制了 OA/PA 处理的原代肝细胞中与 FAS 相关的基因的表达,增强了与 FAO 相关的基因的表达,导致甘油三酯积累减少。虽然 PRMT1 的短期过表达在生理条件下对肝甘油三酯水平没有显著影响,但它导致正常 C57BL/6J 小鼠的血清甘油三酯和空腹血糖水平升高。更重要的是,观察到 PRMT1 与 CFLAR 相互作用并使其甲基化,最终导致其泛素化介导的蛋白降解。这一过程随后触发了原代肝细胞中 c-Jun N 端激酶 1(JNK1)的激活和脂质沉积。总之,这些结果表明 PRMT1 介导的 CFLAR 甲基化在肝脂代谢中起关键作用。针对 PRMT1 进行药物设计可能是治疗 NAFLD 的一种有前途的策略。