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CD1d protects against hepatocyte apoptosis in non-alcoholic steatohepatitis.
Lei, Zhigang; Yu, Jiaojiao; Wu, Yu; Shen, Junyao; Lin, Shibo; Xue, Weijie; Mao, Chenxu; Tang, Rui; Sun, Haoran; Qi, Xin; Wang, Xiaohong; Xu, Lei; Wei, Chuan; Wang, Xiaowei; Chen, Hongbing; Hao, Ping; Yin, Wen; Zhu, Jifeng; Li, Yalin; Wu, Yi; Liu, Shouguo; Liang, Hui; Chen, Xiaojun; Su, Chuan; Zhou, Sha.
Afiliación
  • Lei Z; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Yu J; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Wu Y; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Shen J; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Lin S; Department of General Surgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu, China.
  • Xue W; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Mao C; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Tang R; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Sun H; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Qi X; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Wang X; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Xu L; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Wei C; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Wang X; Department of Blood Transfusion, Children's Hospital of Nanjing Medical University, Nanjing, Jiangsu, China.
  • Chen H; Department of Clinical Laboratory, Children's Hospital of Nanjing Medical University, Nanjing, Jiangsu, China.
  • Hao P; MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu, China.
  • Yin W; MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu, China.
  • Zhu J; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Li Y; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China.
  • Wu Y; MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu, China.
  • Liu S; Center for Rehabilitation Medicine, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu, China.
  • Liang H; Department of General Surgery, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu, China.
  • Chen X; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China. Electronic address: chenxiaojun@njmu.edu.cn.
  • Su C; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China. Electronic address: chuansu@njmu.edu.cn.
  • Zhou S; Jiangsu Key Laboratory of Pathogen Biology, Department of Pathogen Biology and Immunology, State Key Lab of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu, China. Electronic address: shazhou@njmu.edu.cn.
J Hepatol ; 80(2): 194-208, 2024 02.
Article en En | MEDLINE | ID: mdl-38438948
ABSTRACT
BACKGROUND &

AIMS:

Hepatocyte apoptosis, a well-defined form of cell death in non-alcoholic steatohepatitis (NASH), is considered the primary cause of liver inflammation and fibrosis. However, the mechanisms underlying the regulation of hepatocyte apoptosis in NASH remain largely unclear. We explored the anti-apoptotic effect of hepatocyte CD1d in NASH.

METHODS:

Hepatocyte CD1d expression was analyzed in patients with NASH and mouse models. Hepatocyte-specific gene overexpression or knockdown and anti-CD1d crosslinking were used to investigate the anti-apoptotic effect of hepatocyte CD1d on lipotoxicity-, Fas-, and concanavalin (ConA)-mediated liver injuries. A high-fat diet, a methionine-choline-deficient diet, a Fas agonist, and ConA were used to induce lipotoxic and/or apoptotic liver injuries. Palmitic acid was used to mimic lipotoxicity-induced apoptosis in vitro.

RESULTS:

We identified a dramatic decrease in CD1d expression in hepatocytes of patients with NASH and mouse models. Hepatocyte-specific CD1d overexpression and knockdown experiments collectively demonstrated that hepatocyte CD1d protected against hepatocyte apoptosis and alleviated hepatic inflammation and injuries in NASH mice. Furthermore, decreased JAK2-STAT3 signaling was observed in NASH patient livers. Mechanistically, anti-CD1d crosslinking on hepatocytes induced tyrosine phosphorylation of the CD1d cytoplasmic tail, leading to the recruitment and phosphorylation of JAK2. Phosphorylated JAK2 activated STAT3 and subsequently reduced apoptosis in hepatocytes, which was associated with an increase in anti-apoptotic effectors (Bcl-xL and Mcl-1) and a decrease in pro-apoptotic effectors (cleaved-caspase 3/7). Moreover, anti-CD1d crosslinking effectively protected against Fas- or ConA-mediated hepatocyte apoptosis and liver injury in mice.

CONCLUSIONS:

Our study uncovered a previously unrecognized anti-apoptotic CD1d-JAK2-STAT3 axis in hepatocytes that conferred hepatoprotection and highlighted the potential of hepatocyte CD1d-directed therapy for liver injury and fibrosis in NASH, as well as in other liver diseases associated with hepatocyte apoptosis. IMPACT AND IMPLICATIONS Excessive and/or sustained hepatocyte apoptosis is critical in driving liver inflammation and injury. The mechanisms underlying the regulation of hepatocyte apoptosis in non-alcoholic steatohepatitis (NASH) remain largely unclear. Here, we found that CD1d expression in hepatocytes substantially decreases and negatively correlates with the severity of liver injury in patients with NASH. We further revealed a previously unrecognized anti-apoptotic CD1d-JAK2-STAT3 signaling axis in hepatocytes, which confers significant protection against liver injury in NASH and acute liver diseases. Thus, hepatocyte CD1d-targeted therapy could be a promising strategy to manipulate liver injury in both NASH and other hepatocyte apoptosis-related liver diseases.
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Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Enfermedad del Hígado Graso no Alcohólico Límite: Animals / Humans Idioma: En Revista: J Hepatol Asunto de la revista: GASTROENTEROLOGIA Año: 2024 Tipo del documento: Article País de afiliación: China Pais de publicación: Países Bajos

Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Enfermedad del Hígado Graso no Alcohólico Límite: Animals / Humans Idioma: En Revista: J Hepatol Asunto de la revista: GASTROENTEROLOGIA Año: 2024 Tipo del documento: Article País de afiliación: China Pais de publicación: Países Bajos