Luo Xiaoying, Luo Xuan, Zhu Xintao, Wang Guozhen, Ning Zuowei, Li Yang, Ma Xiaoxin, Yang Renqiang, Jin Siyi, Huang Yun, Meng Ying, Li Xu
Guangdong Provincial Key Laboratory of Gastroenterology, Department of Gastroenterology, Nanfang Hospital, Southern Medical University, Guangzhou, China; State Key Laboratory of Organ Failure Research, Guangdong Provincial Key Laboratory of Viral Hepatitis Research, Department of Infectious Diseases, Nanfang Hospital, Southern Medical University, Guangzhou, China.
Guangdong Provincial Key Laboratory of Gastroenterology, Department of Gastroenterology, Nanfang Hospital, Southern Medical University, Guangzhou, China.
Redox Biol. 2017 Oct;13:508-521. doi: 10.1016/j.redox.2017.07.011. Epub 2017 Jul 13.
Aldosterone, with pro-oxidation and pro-autophagy capabilities, plays a key role in liver fibrosis. However, the mechanisms underlying aldosterone-promoted liver sinusoidal endothelial cells (LSECs) defenestration remain unknown. Caveolin 1 (Cav1) displays close links with autophagy and fenestration. Hence, we aim to investigate the role of Cav1-related autophagy in LSECs defenestration. We found the increase of aldosterone/MR (mineralocorticoid receptor) level, oxidation, autophagy, and defenestration in LSECs in the human fibrotic liver, BDL or hyperaldosteronism models; while antagonizing aldosterone or inhibiting autophagy relieved LSECs defenestration in BDL-induced fibrosis or hyperaldosteronism models. In vitro, fenestrae of primary LSECs gradually shrank, along with the down-regulation of the NO-dependent pathway and the augment of the AMPK-dependent autophagy; these effects were aggravated by rapamycin (an autophagy activator) or aldosterone treatment. Additionally, aldosterone increased oxidation mediated by Cav1, reduced ATP generation, and subsequently induced the AMPK-dependent autophagy, leading to the down-regulation of the NO-dependent pathway and LSECs defenestration. These effects were reversed by MR antagonist spironolactone, antioxidants or autophagy inhibitors. Besides, aldosterone enhanced the co-immunoprecipitation of Cav1 with p62 and ubiquitin, and induced Cav1 co-immunofluorescence staining with LC3, ubiquitin, and F-actin in the perinuclear area of LSECs. Furthermore, aldosterone treatment increased the membrane protein level of Cav1, whereas decrease the cytoplasmic protein level of Cav1, indicating that aldosterone induced Cav1-related selective autophagy and F-actin remodeling to promote defenestration. Consequently, Cav1-related selective autophagy initiated by aldosterone-induced oxidation promotes LSECs defenestration via activating the AMPK-ULK1 pathway and inhibiting the NO-dependent pathway.
醛固酮具有促氧化和促自噬能力,在肝纤维化中起关键作用。然而,醛固酮促进肝窦内皮细胞(LSECs)窗孔消失的潜在机制仍不清楚。小窝蛋白1(Cav1)与自噬和窗孔形成密切相关。因此,我们旨在研究Cav1相关自噬在LSECs窗孔消失中的作用。我们发现,在人类纤维化肝脏、胆管结扎(BDL)或醛固酮增多症模型中,LSECs中醛固酮/盐皮质激素受体(MR)水平、氧化、自噬和窗孔消失增加;而拮抗醛固酮或抑制自噬可缓解BDL诱导的纤维化或醛固酮增多症模型中的LSECs窗孔消失。在体外,原代LSECs的窗孔逐渐缩小,同时一氧化氮(NO)依赖性途径下调,AMPK依赖性自噬增强;雷帕霉素(一种自噬激活剂)或醛固酮处理会加剧这些效应。此外,醛固酮增加了由Cav1介导的氧化,减少了三磷酸腺苷(ATP)生成,随后诱导了AMPK依赖性自噬,导致NO依赖性途径下调和LSECs窗孔消失。盐皮质激素受体拮抗剂螺内酯、抗氧化剂或自噬抑制剂可逆转这些效应。此外,醛固酮增强了Cav1与p62和泛素的共免疫沉淀,并在LSECs的核周区域诱导了Cav1与微管相关蛋白1轻链3(LC3)、泛素和丝状肌动蛋白(F-actin)的共免疫荧光染色。此外,醛固酮处理增加了Cav1的膜蛋白水平,而降低了Cav1的细胞质蛋白水平,表明醛固酮诱导了Cav1相关的选择性自噬和F-actin重塑以促进窗孔消失。因此,醛固酮诱导的氧化引发的Cav1相关选择性自噬通过激活AMPK-UNC-51样激酶1(ULK1)途径和抑制NO依赖性途径促进LSECs窗孔消失。