Paneth cells promote angiogenesis and regulate portal hypertension in response to microbial signals.


Journal

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

Informations de publication

Date de publication:
09 2020
Historique:
received: 26 09 2019
revised: 27 02 2020
accepted: 13 03 2020
pubmed: 25 3 2020
medline: 9 11 2021
entrez: 25 3 2020
Statut: ppublish

Résumé

Paneth cells (PCs) synthesize and secrete antimicrobial peptides that are key mediators of host-microbe interactions, establishing a balance between intestinal microflora and enteric pathogens. We observed that their number increases in experimental portal hypertension and aimed to investigate the mechanisms by which these cells can contribute to the regulation of portal pressure. We first treated Math1 Portal hypertension was significantly attenuated in PC-depleted mice compared to control mice and was associated with a decrease in portosystemic shunts. Depletion of PCs also resulted in a significantly decreased density of blood vessels in the intestinal wall and mesentery. Furthermore, we observed reduced expression of intestinal genes regulating angiogenesis in Paneth cell depleted mice using arrays and next generation sequencing. Tube formation and wound healing responses were significantly decreased in ECs treated with conditioned media from PC-depleted intestinal organoids exposed to intestinal microbiota-derived products. Proteomic analysis of conditioned media in the presence of PCs revealed an increase in factors regulating angiogenesis and additional metabolic processes. In vivo endomicroscopy showed decreased vascular proliferation in the absence of PCs. These results suggest that in response to intestinal flora and microbiota-derived factors, PCs secrete not only antimicrobial peptides, but also pro-angiogenic signaling molecules, thereby promoting intestinal and mesenteric angiogenesis and regulating portal hypertension. Paneth cells are present in the lining of the small intestine. They prevent the passage of bacteria from the intestine into the blood circulation by secreting substances to fight bacteria. In this paper, we discovered that these substances not only act against bacteria, but also increase the quantity of blood vessels in the intestine and blood pressure in the portal vein. This is important, because high blood pressure in the portal vein may result in several complications which could be targeted with novel approaches.

Sections du résumé

BACKGROUND & AIMS
Paneth cells (PCs) synthesize and secrete antimicrobial peptides that are key mediators of host-microbe interactions, establishing a balance between intestinal microflora and enteric pathogens. We observed that their number increases in experimental portal hypertension and aimed to investigate the mechanisms by which these cells can contribute to the regulation of portal pressure.
METHODS
We first treated Math1
RESULTS
Portal hypertension was significantly attenuated in PC-depleted mice compared to control mice and was associated with a decrease in portosystemic shunts. Depletion of PCs also resulted in a significantly decreased density of blood vessels in the intestinal wall and mesentery. Furthermore, we observed reduced expression of intestinal genes regulating angiogenesis in Paneth cell depleted mice using arrays and next generation sequencing. Tube formation and wound healing responses were significantly decreased in ECs treated with conditioned media from PC-depleted intestinal organoids exposed to intestinal microbiota-derived products. Proteomic analysis of conditioned media in the presence of PCs revealed an increase in factors regulating angiogenesis and additional metabolic processes. In vivo endomicroscopy showed decreased vascular proliferation in the absence of PCs.
CONCLUSIONS
These results suggest that in response to intestinal flora and microbiota-derived factors, PCs secrete not only antimicrobial peptides, but also pro-angiogenic signaling molecules, thereby promoting intestinal and mesenteric angiogenesis and regulating portal hypertension.
LAY SUMMARY
Paneth cells are present in the lining of the small intestine. They prevent the passage of bacteria from the intestine into the blood circulation by secreting substances to fight bacteria. In this paper, we discovered that these substances not only act against bacteria, but also increase the quantity of blood vessels in the intestine and blood pressure in the portal vein. This is important, because high blood pressure in the portal vein may result in several complications which could be targeted with novel approaches.

Identifiants

pubmed: 32205193
pii: S0168-8278(20)30178-1
doi: 10.1016/j.jhep.2020.03.019
pii:
doi:

Substances chimiques

Culture Media, Conditioned 0
Pore Forming Cytotoxic Proteins 0
Proteome 0
Tamoxifen 094ZI81Y45

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

628-639

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK118904
Pays : United States

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 The authors declare no conflicts of interest that pertain to this work. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Mohsin Hassan (M)

Department for Biomedical Research, Hepatology, University of Bern, Switzerland.

Sheida Moghadamrad (S)

Department for Biomedical Research, Hepatology, University of Bern, Switzerland; Inselspital, Hepatology, University of Bern, Switzerland (Clinic of Visceral Surgery and Medicine, Inselspital, Berne, Switzerland).

Marcel Sorribas (M)

Department for Biomedical Research, Gastroenterology, University of Bern, Switzerland.

Sergi G Muntet (SG)

Department for Biomedical Research, Hepatology, University of Bern, Switzerland.

Philipp Kellmann (P)

Department for Biomedical Research, Hepatology, University of Bern, Switzerland.

Coralie Trentesaux (C)

INSERM, U106, Institut Cochin, F-75014 Paris, France; CNRS, UMR8104, F-75014 Paris, France; Université paris Descartes Sorbonne paris Cité, Paris, France.

Marie Fraudeau (M)

INSERM, U106, Institut Cochin, F-75014 Paris, France; CNRS, UMR8104, F-75014 Paris, France; Université paris Descartes Sorbonne paris Cité, Paris, France.

Paolo Nanni (P)

Functional Genomic Centre, Swiss Federal Institute of Technology, Zurich, Switzerland.

Witold Wolski (W)

Functional Genomic Centre, Swiss Federal Institute of Technology, Zurich, Switzerland.

Irene Keller (I)

Department for Biomedical Research and Swiss Institute of Bioinformatics, University of Bern, Switzerland.

Siegfried Hapfelmeier (S)

Institut of infectious diseases, University of Bern, Switzerland.

Noah F Shroyer (NF)

Gastroenterology and Hepatology, Baylor College of Medicine, Houston, Texas, USA.

Reiner Wiest (R)

Department for Biomedical Research, Gastroenterology, University of Bern, Switzerland; Inselspital, Hepatology, University of Bern, Switzerland (Clinic of Visceral Surgery and Medicine, Inselspital, Berne, Switzerland).

Beatrice Romagnolo (B)

INSERM, U106, Institut Cochin, F-75014 Paris, France; CNRS, UMR8104, F-75014 Paris, France; Université paris Descartes Sorbonne paris Cité, Paris, France.

Andrea De Gottardi (A)

Department for Biomedical Research, Hepatology, University of Bern, Switzerland; Inselspital, Hepatology, University of Bern, Switzerland (Clinic of Visceral Surgery and Medicine, Inselspital, Berne, Switzerland); Gastroenterology and Hepatology, Ente Ospedaliero Cantonale, Università della Svizzera Italiana, Lugano, Switzerland. Electronic address: andrea.degottardi@gmail.com.

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Classifications MeSH