(Pro)renin Receptor Knockdown Attenuates Liver Fibrosis Through Inactivation of ERK/TGF-β1/SMAD3 Pathway.


Journal

Cellular and molecular gastroenterology and hepatology
ISSN: 2352-345X
Titre abrégé: Cell Mol Gastroenterol Hepatol
Pays: United States
ID NLM: 101648302

Informations de publication

Date de publication:
2021
Historique:
received: 17 12 2020
revised: 25 05 2021
accepted: 25 05 2021
pubmed: 5 6 2021
medline: 23 3 2022
entrez: 4 6 2021
Statut: ppublish

Résumé

Activation of the (pro)renin receptor (PRR) up-regulates the expression of profibrotic genes in the kidney and heart. We aimed to investigate the role of PRR in hepatic fibrogenesis. Human hepatic PRR levels were measured in patients with or without liver fibrosis. PRR expression was analyzed in primary mouse hepatic stellate cells (HSCs). Experimental fibrosis was studied in thioacetamide (TAA)-treated or methionine choline-deficient (MCD) diet-fed C57BL/6 mice. Lentivirus-mediated PRR short hairpin RNA was used to knockdown hepatic PRR expression. Lentiviral vectors expressing PRR short hairpin RNA or complementary DNA from the α-smooth muscle actin promoter were used for myofibroblast-specific gene knockdown or overexpression. PRR is up-regulated in human and mouse fibrotic livers, and in activated HSCs. Hepatic PRR knockdown reduced liver fibrosis by suppressing the activation of HSCs and expression of profibrotic genes in TAA or MCD diet-injured mice without significant changes in hepatic inflammation. Renin and prorenin increased the expression of PRR and production of TGF-β1 in human activated HSC Lieming Xu-2 cells, and knockdown of PRR inactivated Lieming Xu-2 cells with decreased production of transforming growth factor (TGF)-β1 and Mothers against decapentaplegic homolog 3 (Smad3) phosphorylation. Myofibroblast-specific PRR knockdown also attenuated liver fibrosis in TAA or MCD diet-injured mice. Mice with both myofibroblast-specific and whole-liver PRR knockdown showed down-regulation of the hepatic extracellular signal-regulated kinase (ERK)/TGF-β1/Smad3 pathway. Myofibroblast-specific PRR overexpression worsened TAA-induced liver fibrosis by up-regulating the ERK/TGF-β1/Smad3 pathway. PRR contributes to liver fibrosis and HSC activation, and its down-regulation attenuates liver fibrosis through inactivation of the ERK/TGF-β1/Smad3 pathway. Therefore, PRR is a promising therapeutic target for liver fibrosis.

Sections du résumé

BACKGROUND & AIMS
Activation of the (pro)renin receptor (PRR) up-regulates the expression of profibrotic genes in the kidney and heart. We aimed to investigate the role of PRR in hepatic fibrogenesis.
METHODS
Human hepatic PRR levels were measured in patients with or without liver fibrosis. PRR expression was analyzed in primary mouse hepatic stellate cells (HSCs). Experimental fibrosis was studied in thioacetamide (TAA)-treated or methionine choline-deficient (MCD) diet-fed C57BL/6 mice. Lentivirus-mediated PRR short hairpin RNA was used to knockdown hepatic PRR expression. Lentiviral vectors expressing PRR short hairpin RNA or complementary DNA from the α-smooth muscle actin promoter were used for myofibroblast-specific gene knockdown or overexpression.
RESULTS
PRR is up-regulated in human and mouse fibrotic livers, and in activated HSCs. Hepatic PRR knockdown reduced liver fibrosis by suppressing the activation of HSCs and expression of profibrotic genes in TAA or MCD diet-injured mice without significant changes in hepatic inflammation. Renin and prorenin increased the expression of PRR and production of TGF-β1 in human activated HSC Lieming Xu-2 cells, and knockdown of PRR inactivated Lieming Xu-2 cells with decreased production of transforming growth factor (TGF)-β1 and Mothers against decapentaplegic homolog 3 (Smad3) phosphorylation. Myofibroblast-specific PRR knockdown also attenuated liver fibrosis in TAA or MCD diet-injured mice. Mice with both myofibroblast-specific and whole-liver PRR knockdown showed down-regulation of the hepatic extracellular signal-regulated kinase (ERK)/TGF-β1/Smad3 pathway. Myofibroblast-specific PRR overexpression worsened TAA-induced liver fibrosis by up-regulating the ERK/TGF-β1/Smad3 pathway.
CONCLUSIONS
PRR contributes to liver fibrosis and HSC activation, and its down-regulation attenuates liver fibrosis through inactivation of the ERK/TGF-β1/Smad3 pathway. Therefore, PRR is a promising therapeutic target for liver fibrosis.

Identifiants

pubmed: 34087453
pii: S2352-345X(21)00111-9
doi: 10.1016/j.jcmgh.2021.05.017
pmc: PMC8340309
pii:
doi:

Substances chimiques

Biomarkers 0
Receptors, Cell Surface 0
Smad3 Protein 0
Transforming Growth Factor beta1 0
Extracellular Signal-Regulated MAP Kinases EC 2.7.11.24
Prorenin Receptor 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

813-838

Subventions

Organisme : NIDDK NIH HHS
ID : P30 DK120515
Pays : United States

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Yun-Cheng Hsieh (YC)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan; Institute of Pharmacology, National Yang-Ming University School of Medicine, Taipei, Taiwan.

Kuei-Chuan Lee (KC)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan. Electronic address: kclee2@vghtpe.gov.tw.

Hao-Jan Lei (HJ)

Department of Medicine, Taipei, Taiwan; Division of General Surgery, Department of Surgery, Taipei Veterans General Hospital, Taipei, Taiwan.

Keng-Hsin Lan (KH)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan; Institute of Pharmacology, National Yang-Ming University School of Medicine, Taipei, Taiwan.

Teh-Ia Huo (TI)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan; Institute of Pharmacology, National Yang-Ming University School of Medicine, Taipei, Taiwan.

Yi-Tsung Lin (YT)

Department of Medicine, Taipei, Taiwan; Division of Infectious Disease, Department of Medicine, Taipei, Taiwan.

Che-Chang Chan (CC)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan.

Bernd Schnabl (B)

Department of Medicine, VA San Diego Healthcare System, San Diego, California.

Yi-Hsiang Huang (YH)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan.

Ming-Chih Hou (MC)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan.

Han-Chieh Lin (HC)

Division of Gastroenterology and Hepatology, Department of Medicine, Taipei, Taiwan; Department of Medicine, Taipei, Taiwan.

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Classifications MeSH