Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis

Abstract The dynamic interplay between parenchymal hepatocytes and non‐parenchymal cells (NPCs), such as macrophages, is an important mechanism for liver metabolic homeostasis. Although numerous endeavors have been made to identify the mediators of metabolic dysfunction associated steatohepatitis (M...

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Main Authors: Tian Su, Yue He, Min Wang, Haiyan Zhou, Yan Huang, Mingsheng Ye, Qi Guo, Ye Xiao, Guangping Cai, Mingyang Zhao, Jianping Wang, Xianghang Luo
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202406500
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author Tian Su
Yue He
Min Wang
Haiyan Zhou
Yan Huang
Mingsheng Ye
Qi Guo
Ye Xiao
Guangping Cai
Mingyang Zhao
Jianping Wang
Xianghang Luo
author_facet Tian Su
Yue He
Min Wang
Haiyan Zhou
Yan Huang
Mingsheng Ye
Qi Guo
Ye Xiao
Guangping Cai
Mingyang Zhao
Jianping Wang
Xianghang Luo
author_sort Tian Su
collection DOAJ
description Abstract The dynamic interplay between parenchymal hepatocytes and non‐parenchymal cells (NPCs), such as macrophages, is an important mechanism for liver metabolic homeostasis. Although numerous endeavors have been made to identify the mediators of metabolic dysfunction associated steatohepatitis (MASH), the molecular underpinnings of MASH progression remain poorly understood, and therapies to arrest MASH progression remain elusive. Herein, it is revealed that the expression of grancalcin (GCA) is upregulated in the macrophages of patients and rodents with MASH and correlates with MASH progression. Notably, the administration of recombinant GCA aggravates the development of MASH, whereas, Gca deletion in myeloid cells blunts liver steatosis and inflammation in multiple MASH murine models. Mechanistically, GCA activates macrophages via TLR9‐NF‐κB signaling, and the activated macrophages promote hepatocyte lipid accumulation and apoptosis via secretion of Interleukin‐6(IL‐6), Tumor Necrosis Factor α (TNFα), and Interleukin‐1β(IL‐1β), thereby leading to hepatic steatosis and inflammation. Finally, the therapeutic administration of antibody blocking GCA effectively halts the progression of MASH. Collectively, these findings implicate GCA as a crucial mediator of MASH and clarify a new metabolic signaling axis between the hepatocytes and macrophages, implying that GCA can emerge as a particularly interesting putative therapeutic target for reversing MASH progression.
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spelling doaj-art-9c8e0869ffba4652bde06b7a04717fa82025-08-20T01:51:14ZengWileyAdvanced Science2198-38442024-11-011142n/an/a10.1002/advs.202406500Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated SteatohepatitisTian Su0Yue He1Min Wang2Haiyan Zhou3Yan Huang4Mingsheng Ye5Qi Guo6Ye Xiao7Guangping Cai8Mingyang Zhao9Jianping Wang10Xianghang Luo11Department of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaDepartment of Endocrinology The Second Affiliated Hospital of University of South China Hengyang Hunan 421000 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital of Central South University Changsha Hunan 410008 ChinaAbstract The dynamic interplay between parenchymal hepatocytes and non‐parenchymal cells (NPCs), such as macrophages, is an important mechanism for liver metabolic homeostasis. Although numerous endeavors have been made to identify the mediators of metabolic dysfunction associated steatohepatitis (MASH), the molecular underpinnings of MASH progression remain poorly understood, and therapies to arrest MASH progression remain elusive. Herein, it is revealed that the expression of grancalcin (GCA) is upregulated in the macrophages of patients and rodents with MASH and correlates with MASH progression. Notably, the administration of recombinant GCA aggravates the development of MASH, whereas, Gca deletion in myeloid cells blunts liver steatosis and inflammation in multiple MASH murine models. Mechanistically, GCA activates macrophages via TLR9‐NF‐κB signaling, and the activated macrophages promote hepatocyte lipid accumulation and apoptosis via secretion of Interleukin‐6(IL‐6), Tumor Necrosis Factor α (TNFα), and Interleukin‐1β(IL‐1β), thereby leading to hepatic steatosis and inflammation. Finally, the therapeutic administration of antibody blocking GCA effectively halts the progression of MASH. Collectively, these findings implicate GCA as a crucial mediator of MASH and clarify a new metabolic signaling axis between the hepatocytes and macrophages, implying that GCA can emerge as a particularly interesting putative therapeutic target for reversing MASH progression.https://doi.org/10.1002/advs.202406500GCAmacrophage‐hepatocytemetabolic dysfunction associated steatohepatitis
spellingShingle Tian Su
Yue He
Min Wang
Haiyan Zhou
Yan Huang
Mingsheng Ye
Qi Guo
Ye Xiao
Guangping Cai
Mingyang Zhao
Jianping Wang
Xianghang Luo
Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis
Advanced Science
GCA
macrophage‐hepatocyte
metabolic dysfunction associated steatohepatitis
title Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis
title_full Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis
title_fullStr Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis
title_full_unstemmed Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis
title_short Macrophage‐Hepatocyte Circuits Mediated by Grancalcin Aggravate the Progression of Metabolic Dysfunction Associated Steatohepatitis
title_sort macrophage hepatocyte circuits mediated by grancalcin aggravate the progression of metabolic dysfunction associated steatohepatitis
topic GCA
macrophage‐hepatocyte
metabolic dysfunction associated steatohepatitis
url https://doi.org/10.1002/advs.202406500
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