Fang Qi, Yan Qi, Liu Xingyun, Zhang Xiaolu, Zha Lixia, Zhang Ruixin, Gao Zhixin, Du Jian, Chen Lijian
Department of Anesthesiology, The First Affiliated Hospital of Anhui Medical University, Hefei 230032, China.
Department of Biochemistry and Molecular Biology, Research Center for Infectious Diseases, School of Basic Medical Sciences, Anhui Medical University, Hefei 230032, China.
Int J Biol Sci. 2025 Jan 20;21(3):1294-1307. doi: 10.7150/ijbs.103789. eCollection 2025.
Hepatic ischemia-reperfusion (I/R) injury can cause poor prognosis of liver transplantation and hepatectomy, especially in patients with alcohol-associated liver disease (ALD). Apoptosis is closely related to different stages of liver injury, and the death of hepatocytes caused by endoplasmic reticulum (ER) and mitochondria homeostasis perturbation may be key to liver injury. The receptor tyrosine kinases AXL encoded by the gene axl, is a member of the TAM (TYRO3, AXL, and MERTK) family, which participates in various biological processes by binding to the ligand of growth arrest-specific protein 6 (Gas6). However, whether AXL is involved in apoptosis pathways, and the detailed mechanism in hepatic I/R injury remains unknown. In the present study, we found that total AXL is up-regulated while phosphorylated AXL (p-AXL, the active form of AXL) was down-regulated after I/R in human liver tissues from liver transplantation. Consistently, total AXL was found up-regulated while p-AXL was down-regulated during hepatic I/R injury in mice. Pretreatment with Gas6 increased p-AXL expression, reduced ER stress-associated cell apoptosis, alleviated liver damage, and restored ER and mitochondria ultrastructure during hepatic I/R in mice. Furthermore, the ALD model was established by chronic-plus-binge ethanol feeding to explore the role of AXL in I/R liver injury with ethanol-associated steatosis. We found that ALD mice had a lower p-AXL level and were more susceptible to hepatic I/R injury. Importantly, activated AXL ameliorated liver injury by inhibiting IRE1 and PERK pathway to reduce ER stress-associated apoptosis. In conclusion, activated AXL protects alcohol-associated steatotic liver against I/R injury by inhibiting ER stress and mitochondria-associated apoptosis, suggesting that targeting AXL serves as a potential strategy for liver I/R injury, particularly for marginal liver donors with alcohol-associated steatosis.
肝缺血再灌注(I/R)损伤会导致肝移植和肝切除术后预后不良,尤其是在酒精性肝病(ALD)患者中。细胞凋亡与肝损伤的不同阶段密切相关,内质网(ER)和线粒体稳态紊乱导致的肝细胞死亡可能是肝损伤的关键。由axl基因编码的受体酪氨酸激酶AXL是TAM(TYRO3、AXL和MERTK)家族的成员,它通过与生长停滞特异性蛋白6(Gas6)的配体结合参与各种生物学过程。然而,AXL是否参与凋亡途径以及在肝I/R损伤中的详细机制仍不清楚。在本研究中,我们发现肝移植患者的人肝组织在I/R后总AXL上调而磷酸化AXL(p-AXL,AXL的活性形式)下调。同样,在小鼠肝I/R损伤过程中也发现总AXL上调而p-AXL下调。Gas6预处理可增加p-AXL表达,减少ER应激相关的细胞凋亡,减轻肝损伤,并在小鼠肝I/R期间恢复ER和线粒体超微结构。此外,通过慢性加暴饮乙醇喂养建立ALD模型,以探讨AXL在伴有乙醇性脂肪变性的I/R肝损伤中的作用。我们发现ALD小鼠的p-AXL水平较低,更容易受到肝I/R损伤。重要的是,激活的AXL通过抑制IRE1和PERK途径减轻肝损伤,以减少ER应激相关的细胞凋亡。总之,激活的AXL通过抑制ER应激和线粒体相关的细胞凋亡来保护酒精性脂肪变性肝脏免受I/R损伤,这表明靶向AXL是肝I/R损伤的一种潜在策略,特别是对于伴有酒精性脂肪变性的边缘性肝供体。