TGR5 controls bile acid composition and gallbladder function to protect the liver from bile acid overload.

ALP, alkaline phosphatase ALT, alanine aminotransferase BA, bile acid BDL, bile duct ligation Bile acids CA, cholic acid CC, cholecystectomy CT, cholestyramine CYP, cytochrome P450 EH, extended hepatectomy GB, gallbladder GM, gut microbiota GPBAR1 GPBAR1, G protein-coupled bile acid receptor 1 Gallbladder HI, hydrophobicity index Hepatoprotection KO, knockout ND, normal diet OA, oleanolic acid PH, partial hepatectomy TBA, total BA TGR5 TGR5, Takeda G protein coupled receptor UDCA, ursodeoxycholic acid WT, wild-type

Journal

JHEP reports : innovation in hepatology
ISSN: 2589-5559
Titre abrégé: JHEP Rep
Pays: Netherlands
ID NLM: 101761237

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 20 05 2020
revised: 29 10 2020
accepted: 30 10 2020
entrez: 19 2 2021
pubmed: 20 2 2021
medline: 20 2 2021
Statut: epublish

Résumé

As the composition of the bile acid (BA) pool has a major impact on liver pathophysiology, we studied its regulation by the BA receptor Takeda G protein coupled receptor (TGR5), which promotes hepatoprotection against BA overload. Wild-type, total and hepatocyte-specific TGR5-knockout, and TGR5-overexpressing mice were used in: partial (66%) and 89% extended hepatectomies (EHs) upon normal, ursodeoxycholic acid (UDCA)- or cholestyramine (CT)-enriched diet, bile duct ligation (BDL), cholic acid (CA)-enriched diet, and TGR5 agonist (RO) treatments. We thereby studied the impact of TGR5 on: BA composition, liver injury, regeneration and survival. We also performed analyses on the gut microbiota (GM) and gallbladder (GB). Liver BA composition was analysed in patients undergoing major hepatectomy. The TGR5-KO hyperhydrophobic BA composition was not directly related to altered BA synthesis, nor to TGR5-KO GM dysbiosis, as supported by hepatocyte-specific KO mice and co-housing experiments, respectively. The TGR5-dependent control of GB dilatation was crucial for BA composition, as determined by experiments including RO treatment and/or cholecystectomy. The poor TGR5-KO post-EH survival rate, related to exacerbated peribiliary necrosis and BA overload, was improved by shifting BAs toward a less toxic composition (CT treatment). After either BDL or a CA-enriched diet with or without cholecystectomy, we found that GB dilatation had strong TGR5-dependent hepatoprotective properties. In patients, a more hydrophobic liver BA composition was correlated with an unfavourable outcome after hepatectomy. BA composition is crucial for hepatoprotection in mice and humans. We indicate TGR5 as a key regulator of BA profile and thereby as a potential hepatoprotective target under BA overload conditions. Through multiple

Sections du résumé

BACKGROUND & AIMS OBJECTIVE
As the composition of the bile acid (BA) pool has a major impact on liver pathophysiology, we studied its regulation by the BA receptor Takeda G protein coupled receptor (TGR5), which promotes hepatoprotection against BA overload.
METHODS METHODS
Wild-type, total and hepatocyte-specific TGR5-knockout, and TGR5-overexpressing mice were used in: partial (66%) and 89% extended hepatectomies (EHs) upon normal, ursodeoxycholic acid (UDCA)- or cholestyramine (CT)-enriched diet, bile duct ligation (BDL), cholic acid (CA)-enriched diet, and TGR5 agonist (RO) treatments. We thereby studied the impact of TGR5 on: BA composition, liver injury, regeneration and survival. We also performed analyses on the gut microbiota (GM) and gallbladder (GB). Liver BA composition was analysed in patients undergoing major hepatectomy.
RESULTS RESULTS
The TGR5-KO hyperhydrophobic BA composition was not directly related to altered BA synthesis, nor to TGR5-KO GM dysbiosis, as supported by hepatocyte-specific KO mice and co-housing experiments, respectively. The TGR5-dependent control of GB dilatation was crucial for BA composition, as determined by experiments including RO treatment and/or cholecystectomy. The poor TGR5-KO post-EH survival rate, related to exacerbated peribiliary necrosis and BA overload, was improved by shifting BAs toward a less toxic composition (CT treatment). After either BDL or a CA-enriched diet with or without cholecystectomy, we found that GB dilatation had strong TGR5-dependent hepatoprotective properties. In patients, a more hydrophobic liver BA composition was correlated with an unfavourable outcome after hepatectomy.
CONCLUSIONS CONCLUSIONS
BA composition is crucial for hepatoprotection in mice and humans. We indicate TGR5 as a key regulator of BA profile and thereby as a potential hepatoprotective target under BA overload conditions.
LAY SUMMARY BACKGROUND
Through multiple

Identifiants

pubmed: 33604531
doi: 10.1016/j.jhepr.2020.100214
pii: S2589-5559(20)30148-8
pmc: PMC7872982
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100214

Informations de copyright

© 2020 The Authors.

Déclaration de conflit d'intérêts

The authors declare no conflicts of interest that pertain to this work.

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Auteurs

Valeska Bidault-Jourdainne (V)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Grégory Merlen (G)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Mathilde Glénisson (M)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Isabelle Doignon (I)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Isabelle Garcin (I)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Noémie Péan (N)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Raphael Boisgard (R)

Plateforme d'Imagerie du Petit Animal, SHFJ, 91405, Orsay, France.

José Ursic-Bedoya (J)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Matteo Serino (M)

IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039, 31024, Toulouse, France.

Christoph Ullmer (C)

Roche Innovation Center Basel CH-4070 Basel, Switzerland.

Lydie Humbert (L)

Sorbonne Université, Centre de Recherche Saint Antoine, CRSA, INSERM U 1057, 75571, Paris Cedex 12, France.

Ahmed Abdelrafee (A)

Centre Hépato-Biliaire, Hôpital Paul Brousse, Université Paris-Saclay, 94800, Villejuif, France.

Nicolas Golse (N)

Centre Hépato-Biliaire, Hôpital Paul Brousse, Université Paris-Saclay, 94800, Villejuif, France.

Eric Vibert (E)

Centre Hépato-Biliaire, Hôpital Paul Brousse, Université Paris-Saclay, 94800, Villejuif, France.

Jean-Charles Duclos-Vallée (JC)

Centre Hépato-Biliaire, Hôpital Paul Brousse, Université Paris-Saclay, 94800, Villejuif, France.

Dominique Rainteau (D)

Sorbonne Université, Centre de Recherche Saint Antoine, CRSA, INSERM U 1057, 75571, Paris Cedex 12, France.

Thierry Tordjmann (T)

Université Paris Saclay, Faculté des Sciences d'Orsay, INSERM U.1193, bât. 443, 91405, Orsay, France.

Classifications MeSH