Differential effects of selective- and pan-PPAR agonists on experimental steatohepatitis and hepatic macrophages


Journal

Journal of hepatology
ISSN: 1600-0641
Titre abrégé: J Hepatol
Pays: Netherlands
ID NLM: 8503886

Informations de publication

Date de publication:
10 2020
Historique:
received: 11 09 2019
revised: 30 03 2020
accepted: 13 04 2020
pubmed: 4 5 2020
medline: 16 11 2021
entrez: 4 5 2020
Statut: ppublish

Résumé

Peroxisome proliferator-activated receptors (PPARs) are essential regulators of whole-body metabolism, but also modulate inflammation in immune cells, notably macrophages. We compared the effects of selective PPAR agonists to those of the pan-PPAR agonist lanifibranor in non-alcoholic fatty liver disease (NAFLD), and studied isoform-specific effects on hepatic macrophage biology. Lanifibranor or selective PPARα (fenofibrate), PPARγ (pioglitazone) and PPARδ (GW501516) agonists were therapeutically administered in choline-deficient, amino acid-defined high-fat diet (CDAA-HFD)- and Western diet (WD)-fed mouse models of NAFLD. Acute liver injury was induced by carbon tetrachloride (CCl Lanifibranor improved all histological features of steatohepatitis in CDAA-HFD-fed mice, including liver fibrosis, thereby combining and exceeding specific effects of the single PPAR agonists. Its potent anti-steatotic efficacy was confirmed in a 3D liver biochip model with primary cells. Infiltrating hepatic monocyte-derived macrophages were reduced following PPAR agonist administration, especially with lanifibranor, even after short-term treatment, paralleling improved steatosis and hepatitis. Lanifibranor similarly decreased steatosis, liver injury and monocyte infiltration in the WD model. In the acute CCl Pan-PPAR agonists combine the beneficial effects of selective PPAR agonists and may counteract inflammation and disease progression more potently. PPARδ agonism and lanifibranor directly modulate macrophage activation, but not infiltration, thereby synergizing with beneficial metabolic effects of PPARα/γ agonists. Peroxisome proliferated-activated receptors (PPARs) are essential regulators of metabolism and inflammation. We demonstrated that the pan-PPAR agonist lanifibranor ameliorated all aspects of non-alcoholic fatty liver disease in independent experimental mouse models. Non-alcoholic fatty liver disease and fatty acids induce a specific polarization status in macrophages, which was altered by lanifibranor to increase expression of lipid handling genes, thereby decreasing inflammation. PPAR isoforms have differential therapeutic effects on fat-laden hepatocytes, activated hepatic stellate cells and inflammatory macrophages, supporting the clinical development of pan-PPAR agonists.

Sections du résumé

BACKGROUND & AIMS
Peroxisome proliferator-activated receptors (PPARs) are essential regulators of whole-body metabolism, but also modulate inflammation in immune cells, notably macrophages. We compared the effects of selective PPAR agonists to those of the pan-PPAR agonist lanifibranor in non-alcoholic fatty liver disease (NAFLD), and studied isoform-specific effects on hepatic macrophage biology.
METHODS
Lanifibranor or selective PPARα (fenofibrate), PPARγ (pioglitazone) and PPARδ (GW501516) agonists were therapeutically administered in choline-deficient, amino acid-defined high-fat diet (CDAA-HFD)- and Western diet (WD)-fed mouse models of NAFLD. Acute liver injury was induced by carbon tetrachloride (CCl
RESULTS
Lanifibranor improved all histological features of steatohepatitis in CDAA-HFD-fed mice, including liver fibrosis, thereby combining and exceeding specific effects of the single PPAR agonists. Its potent anti-steatotic efficacy was confirmed in a 3D liver biochip model with primary cells. Infiltrating hepatic monocyte-derived macrophages were reduced following PPAR agonist administration, especially with lanifibranor, even after short-term treatment, paralleling improved steatosis and hepatitis. Lanifibranor similarly decreased steatosis, liver injury and monocyte infiltration in the WD model. In the acute CCl
CONCLUSION
Pan-PPAR agonists combine the beneficial effects of selective PPAR agonists and may counteract inflammation and disease progression more potently. PPARδ agonism and lanifibranor directly modulate macrophage activation, but not infiltration, thereby synergizing with beneficial metabolic effects of PPARα/γ agonists.
LAY SUMMARY
Peroxisome proliferated-activated receptors (PPARs) are essential regulators of metabolism and inflammation. We demonstrated that the pan-PPAR agonist lanifibranor ameliorated all aspects of non-alcoholic fatty liver disease in independent experimental mouse models. Non-alcoholic fatty liver disease and fatty acids induce a specific polarization status in macrophages, which was altered by lanifibranor to increase expression of lipid handling genes, thereby decreasing inflammation. PPAR isoforms have differential therapeutic effects on fat-laden hepatocytes, activated hepatic stellate cells and inflammatory macrophages, supporting the clinical development of pan-PPAR agonists.

Identifiants

pubmed: 32360434
pii: S0168-8278(20)30269-5
doi: 10.1016/j.jhep.2020.04.025
pii:
doi:

Substances chimiques

Fenofibrate U202363UOS
GW 501516 0
Hypolipidemic Agents 0
Peroxisome Proliferator-Activated Receptors 0
Thiazoles 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

757-770

Informations de copyright

Copyright © 2020 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest VA, ED, CE and GW are employees of Inventiva. Work in FT's laboratory has received funding by Allergan, Galapagos, Inventiva and Bristol Myers Squibb. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Sander Lefere (S)

Department of Gastroenterology and Hepatology, Hepatology Research Unit, Ghent University, Ghent, Belgium; Department of Medicine III, University Hospital Aachen, Aachen, Germany.

Tobias Puengel (T)

Department of Medicine III, University Hospital Aachen, Aachen, Germany; Department of Hepatology and Gastroenterology, Charité University Medicine Berlin, Berlin, Germany.

Jana Hundertmark (J)

Department of Medicine III, University Hospital Aachen, Aachen, Germany; Department of Hepatology and Gastroenterology, Charité University Medicine Berlin, Berlin, Germany.

Christian Penners (C)

Department of Medicine III, University Hospital Aachen, Aachen, Germany.

Anna Katharina Frank (AK)

Department of Medicine III, University Hospital Aachen, Aachen, Germany.

Adrien Guillot (A)

Department of Hepatology and Gastroenterology, Charité University Medicine Berlin, Berlin, Germany.

Kevin de Muynck (K)

Department of Basic and Applied Medical Sciences, Gut-Liver Immunopharmacology Unit, Ghent University, Ghent, Belgium.

Felix Heymann (F)

Department of Medicine III, University Hospital Aachen, Aachen, Germany; Department of Hepatology and Gastroenterology, Charité University Medicine Berlin, Berlin, Germany.

Vanessa Adarbes (V)

Inventiva, Daix, France.

Evelyne Defrêne (E)

Inventiva, Daix, France.

Céline Estivalet (C)

Inventiva, Daix, France.

Anja Geerts (A)

Department of Gastroenterology and Hepatology, Hepatology Research Unit, Ghent University, Ghent, Belgium.

Lindsey Devisscher (L)

Department of Basic and Applied Medical Sciences, Gut-Liver Immunopharmacology Unit, Ghent University, Ghent, Belgium.

Guillaume Wettstein (G)

Inventiva, Daix, France.

Frank Tacke (F)

Department of Medicine III, University Hospital Aachen, Aachen, Germany; Department of Hepatology and Gastroenterology, Charité University Medicine Berlin, Berlin, Germany. Electronic address: frank.tacke@charite.de.

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Classifications MeSH