OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis

Abstract Stressed hepatocytes promote liver fibrosis through communications with hepatic stellate cells (HSCs) during chronic liver injury. However, intra‐hepatocyte players that facilitate such cell‐to‐cell communications are largely undefined. It is previously reported that hepatocyte E4BP4 is pot...

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Main Authors: Sujuan Wang, Jiashi Gao, Meichan Yang, Gary Zhang, Lei Yin, Xin Tong
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202405678
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author Sujuan Wang
Jiashi Gao
Meichan Yang
Gary Zhang
Lei Yin
Xin Tong
author_facet Sujuan Wang
Jiashi Gao
Meichan Yang
Gary Zhang
Lei Yin
Xin Tong
author_sort Sujuan Wang
collection DOAJ
description Abstract Stressed hepatocytes promote liver fibrosis through communications with hepatic stellate cells (HSCs) during chronic liver injury. However, intra‐hepatocyte players that facilitate such cell‐to‐cell communications are largely undefined. It is previously reported that hepatocyte E4BP4 is potently induced by ER stress and hepatocyte deletion of E4bp4 protects mice from high‐fat diet‐induced liver steatosis. Here how hepatocyte E4bp4 deficiency impacts the activation of HSCs and the progression toward MASH‐associated liver fibrosis is examined. Hepatic E4BP4 is increased in mouse models of NASH diet‐ or CCl4‐induced liver fibrosis. Hepatocyte‐specific E4bp4 deletion protected mice against NASH diet‐induced liver injury, inflammation, and fibrosis without impacting liver steatosis. Hepatocyte E4BP4 overexpression activated HSCs in a medium transfer experiment, whereas hepatocyte E4bp4 depletion did the opposite. RNA‐Seq analysis identified the pro‐fibrogenic factor OPN as a critical target of E4BP4 within hepatocytes. Antibody neutralization or shRNA depletion of Opn abrogated hepatocyte E4BP4‐induced HSC activation. E4BP4 interacted with and stabilized YAP, an established activator of OPN. Loss of hepatic Yap blocked OPN induction in the liver of Ad‐E4bp4‐injected mice. Hepatocyte E4BP4 induces OPN via YAP to activate HSCs and promote liver fibrosis during diet‐induced MASH. Inhibition of the hepatocyte E4BP4‐OPN pathway could offer a novel therapeutic avenue for treating MASLD/MASH.
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spelling doaj-art-56570a7fb4dc4d5d83f3e1109b841b112025-08-20T01:58:42ZengWileyAdvanced Science2198-38442024-12-011147n/an/a10.1002/advs.202405678OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver FibrosisSujuan Wang0Jiashi Gao1Meichan Yang2Gary Zhang3Lei Yin4Xin Tong5Department of Infectious Diseases The Second Xiangya Hospital Central South University 139 Renmin Middle Rd, Furong District Changsha Hunan 410011 P. R. ChinaDepartment of Infectious Diseases The Second Xiangya Hospital Central South University 139 Renmin Middle Rd, Furong District Changsha Hunan 410011 P. R. ChinaDepartment of Radiology Guangdong Provincial People's Hospital (Guangdong Academy of Medical Sciences) Southern Medical University 106 Zhongshan 2nd Road Guangzhou Guangdong 51008 P. R. ChinaDepartment of Molecular & Integrative Physiology University of Michigan Medical School NCRC 20–3843, 2800 Plymouth Road Ann Arbor MI 48105 USADepartment of Molecular & Integrative Physiology University of Michigan Medical School NCRC 20–3843, 2800 Plymouth Road Ann Arbor MI 48105 USADepartment of Molecular & Integrative Physiology University of Michigan Medical School NCRC 20–3843, 2800 Plymouth Road Ann Arbor MI 48105 USAAbstract Stressed hepatocytes promote liver fibrosis through communications with hepatic stellate cells (HSCs) during chronic liver injury. However, intra‐hepatocyte players that facilitate such cell‐to‐cell communications are largely undefined. It is previously reported that hepatocyte E4BP4 is potently induced by ER stress and hepatocyte deletion of E4bp4 protects mice from high‐fat diet‐induced liver steatosis. Here how hepatocyte E4bp4 deficiency impacts the activation of HSCs and the progression toward MASH‐associated liver fibrosis is examined. Hepatic E4BP4 is increased in mouse models of NASH diet‐ or CCl4‐induced liver fibrosis. Hepatocyte‐specific E4bp4 deletion protected mice against NASH diet‐induced liver injury, inflammation, and fibrosis without impacting liver steatosis. Hepatocyte E4BP4 overexpression activated HSCs in a medium transfer experiment, whereas hepatocyte E4bp4 depletion did the opposite. RNA‐Seq analysis identified the pro‐fibrogenic factor OPN as a critical target of E4BP4 within hepatocytes. Antibody neutralization or shRNA depletion of Opn abrogated hepatocyte E4BP4‐induced HSC activation. E4BP4 interacted with and stabilized YAP, an established activator of OPN. Loss of hepatic Yap blocked OPN induction in the liver of Ad‐E4bp4‐injected mice. Hepatocyte E4BP4 induces OPN via YAP to activate HSCs and promote liver fibrosis during diet‐induced MASH. Inhibition of the hepatocyte E4BP4‐OPN pathway could offer a novel therapeutic avenue for treating MASLD/MASH.https://doi.org/10.1002/advs.202405678E4BP4hepatic stellate cellsliver fibrosisMASHOPN
spellingShingle Sujuan Wang
Jiashi Gao
Meichan Yang
Gary Zhang
Lei Yin
Xin Tong
OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis
Advanced Science
E4BP4
hepatic stellate cells
liver fibrosis
MASH
OPN
title OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis
title_full OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis
title_fullStr OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis
title_full_unstemmed OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis
title_short OPN‐Mediated Crosstalk Between Hepatocyte E4BP4 and Hepatic Stellate Cells Promotes MASH‐Associated Liver Fibrosis
title_sort opn mediated crosstalk between hepatocyte e4bp4 and hepatic stellate cells promotes mash associated liver fibrosis
topic E4BP4
hepatic stellate cells
liver fibrosis
MASH
OPN
url https://doi.org/10.1002/advs.202405678
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