Li Chunming, Fang Lei, Su Xingxing, Zhang Jie, Xiong Haojun, Yu Hongqiang, Zhu Zhu, Lin Xiaotong, Min Ke, Wu Di, Chen Zhiyu, Gong Jianping, Xie Chuan-Ming
Key Laboratory of Hepatobiliary and Pancreatic Surgery, Institute of Hepatobiliary Surgery, Southwest Hospital, Third Military Medical University (Army Medical University), Chongqing, China.
Department of Hepatobiliary Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing, China.
Cell Death Dis. 2025 Apr 19;16(1):315. doi: 10.1038/s41419-025-07574-4.
Macrophages hold a critical position in maintenance of hepatic homeostasis and in injury and repair processes in acute and chronic liver diseases. TIM3 is a promising protector in MCD-induced steatohepatitis in acute liver injury. However, we recently find TIM3 as a driver of fibrosis in MCD/HFD-induced chronic liver injury. This study aims to explore how macrophage TIM3 drivers NAFLD-associated chronic liver injury as well as identify a subtype of fibrotic patients suitable for anti-TIM3 immunotherapy. Here, we found that TIM3 was highly expressed in liver macrophages in a long-term MCD- or HFD-fed mice with fibrotic NASH. Elevated β-TrCP in macrophages promoted TIM3 polyubiquitination and membrane translocation. The ubiquitinated TIM3 then bound with PI3K and followed by inhibition of mTOR and activation of macrophage M2 polarization and TGF-β release, leading to HSC activation and liver fibrosis. Furthermore, elevated TIM3 was attributed to the transcriptional TBP upregulation and miR-4524a-5p downregulation. Targeting of TIM3 significantly attenuated liver fibrosis in mice. In clinical NASH patients, elevated macrophage TIM3 is positively correlated with TBP expression and negatively associated with miR-4524a-5p. Decreased miR-4524a-5p in plasma was a biomarker for the NASH fibrosis patients suitable for anti-TIM3 therapy. In conclusion, this study reveals that miR-4524a-5p/TBP promotes β-TrCP/TIM3 complex activation in macrophages and aggravates chronic NASH fibrosis, providing miR-4524a-5p as an effective blood biomarker for a subtype of chronic NASH patients with fibrosis suitable for anti-TIM3 treatment.
巨噬细胞在维持肝脏内环境稳态以及急性和慢性肝病的损伤与修复过程中发挥着关键作用。TIM3是急性肝损伤中蛋氨酸胆碱缺乏(MCD)诱导的脂肪性肝炎的一种有前景的保护因子。然而,我们最近发现TIM3是MCD/高脂饮食(HFD)诱导的慢性肝损伤中纤维化的驱动因素。本研究旨在探讨巨噬细胞TIM3如何驱动非酒精性脂肪性肝病(NAFLD)相关的慢性肝损伤,并确定适合抗TIM3免疫治疗的纤维化患者亚型。在此,我们发现TIM3在长期喂食MCD或HFD的纤维化非酒精性脂肪性肝炎(NASH)小鼠的肝脏巨噬细胞中高表达。巨噬细胞中β - 转导素重复序列包含蛋白(β-TrCP)升高促进TIM3多聚泛素化和膜易位。泛素化的TIM3随后与磷脂酰肌醇-3-激酶(PI3K)结合,继而抑制雷帕霉素靶蛋白(mTOR)并激活巨噬细胞M2极化和转化生长因子-β(TGF-β)释放,导致肝星状细胞(HSC)激活和肝纤维化。此外,TIM3升高归因于转录因子TATA结合蛋白(TBP)上调和微小RNA-4524a-5p(miR-4524a-5p)下调。靶向TIM3可显著减轻小鼠肝纤维化。在临床NASH患者中,巨噬细胞TIM3升高与TBP表达呈正相关,与miR-4524a-5p呈负相关。血浆中miR-4524a-5p降低是适合抗TIM3治疗的NASH纤维化患者的生物标志物。总之,本研究揭示miR-4524a-5p/TBP促进巨噬细胞中β-TrCP/TIM3复合物激活并加重慢性NASH纤维化,为适合抗TIM3治疗的慢性NASH纤维化患者亚型提供了有效的血液生物标志物miR-4524a-5p。