Schonfeld Michael, Nataraj Kruti, Mah Samson, Weinman Steven, Tikhanovich Irina
Department of Internal Medicine, University of Kansas Medical Center, Kansas City, Kansas.
Department of Internal Medicine, University of Kansas Medical Center, Kansas City, Kansas; Kansas City VA Medical Center, Kansas City, Missouri.
Cell Mol Gastroenterol Hepatol. 2025 Apr 26;19(9):101525. doi: 10.1016/j.jcmgh.2025.101525.
BACKGROUND & AIMS: Abstinence is an important therapeutic intervention for patients with alcohol-associated liver disease (ALD). However, fibrosis improvement after cessation is not uniform and some patients do not improve.
Mice were fed high-fat diet with 20% alcohol in the drinking water for 20 weeks (ALD) followed by 4 weeks of chow diet with plain water (resolution). scATAC-seq dataset was analyzed using Signac R package. Cebpb floxed mice received AAV-TBG-Cre or AAV-control at the time of alcohol cessation. Hepatocyte-macrophage and endothelial cell-hepatocytes crosstalk was investigated using a Transwell coculture system. To test the role of angiopoietin mice were treated with recombinant angiopoietin-1, 1 week after alcohol cessation.
We analyzed differentially accessible regions in hepatocytes from control, ALD, or 4 weeks post alcohol cessation mice and identified transcription factors activated in ALD that remained activated after alcohol withdrawal. The top hit was CCAAT enhancer binding protein beta (C/EBPβ). We found that hepatocyte-specific Cebpb knockout at the time of alcohol cessation promoted fibrosis resolution. The resolution was mediated by altered hepatocyte-macrophage crosstalk. C/EBPβ suppressed the expression of CYP3A family of enzymes in hepatocytes and downstream macrophage collagen degradation ability. Cebpb knockout in hepatocytes promoted a proresolving phenotype in liver macrophages. We further identified upstream events leading to persistent C/EBPβ activation. C/EBPβ was induced by alcohol-mediated endothelial changes during ALD development and resolution. Restoring endothelial cell function with angiopoietin-1 supplementation reduced C/EBPβ and promoted fibrosis resolution.
Taken together, alcohol-induced C/EBPβ activation is a key driver of poor disease resolution in ALD and a promising target for patients who fail to recover after alcohol abstinence.
戒酒是酒精性肝病(ALD)患者的重要治疗干预措施。然而,戒酒之后纤维化的改善并不一致,部分患者并无改善。
给小鼠喂食高脂饮食,并在饮用水中添加20%的酒精,持续20周(ALD阶段),随后给予普通饮食和纯水,持续4周(恢复阶段)。使用Signac R软件包分析单细胞染色质转座酶可及性测序(scATAC-seq)数据集。在戒酒时,Cebpb基因敲除小鼠接受腺相关病毒-甲状腺激素结合球蛋白-cre(AAV-TBG-Cre)或腺相关病毒对照(AAV-control)。使用Transwell共培养系统研究肝细胞-巨噬细胞和内皮细胞-肝细胞之间的相互作用。为了测试血管生成素的作用,在戒酒1周后用重组血管生成素-1对小鼠进行治疗。
我们分析了对照、ALD或戒酒4周后小鼠肝细胞中差异可及区域,并确定了在ALD中被激活且在戒酒之后仍保持激活状态的转录因子。最显著的是CCAAT增强子结合蛋白β(C/EBPβ)。我们发现,在戒酒时肝细胞特异性敲除Cebpb可促进纤维化的消退。这种消退是由肝细胞-巨噬细胞相互作用的改变介导的。C/EBPβ抑制肝细胞中CYP3A家族酶以及下游巨噬细胞胶原降解能力的表达。肝细胞中Cebpb基因敲除促进肝巨噬细胞中促消退表型的形成。我们进一步确定了导致C/EBPβ持续激活的上游事件。在ALD发展和恢复过程中,C/EBPβ由酒精介导的内皮细胞变化诱导产生。补充血管生成素-1恢复内皮细胞功能可降低C/EBPβ并促进纤维化消退。
综上所述,酒精诱导的C/EBPβ激活是ALD疾病消退不佳的关键驱动因素,也是戒酒之后未能恢复的患者的一个有前景的治疗靶点。