An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery

Summary: Although high-fat diet (HFD)-induced gut microbiota dysbiosis is known to affect atherosclerosis, the underlying mechanisms remain to be fully explored. Here, we show that the progression of atherosclerosis depends on a gut microbiota shaped by an HFD but not a high-cholesterol (HC) diet an...

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Main Authors: Ludivine Laurans, Nirmala Mouttoulingam, Mouna Chajadine, Aonghus Lavelle, Marc Diedisheim, Emilie Bacquer, Laura Creusot, Nadine Suffee, Bruno Esposito, Nada Joe Melhem, Wilfried Le Goff, Yacine Haddad, Jean-Louis Paul, Dominique Rainteau, Alain Tedgui, Hafid Ait-Oufella, Laurence Zitvogel, Harry Sokol, Soraya Taleb
Format: Article
Language:English
Published: Elsevier 2023-11-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723013621
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author Ludivine Laurans
Nirmala Mouttoulingam
Mouna Chajadine
Aonghus Lavelle
Marc Diedisheim
Emilie Bacquer
Laura Creusot
Nadine Suffee
Bruno Esposito
Nada Joe Melhem
Wilfried Le Goff
Yacine Haddad
Jean-Louis Paul
Dominique Rainteau
Alain Tedgui
Hafid Ait-Oufella
Laurence Zitvogel
Harry Sokol
Soraya Taleb
author_facet Ludivine Laurans
Nirmala Mouttoulingam
Mouna Chajadine
Aonghus Lavelle
Marc Diedisheim
Emilie Bacquer
Laura Creusot
Nadine Suffee
Bruno Esposito
Nada Joe Melhem
Wilfried Le Goff
Yacine Haddad
Jean-Louis Paul
Dominique Rainteau
Alain Tedgui
Hafid Ait-Oufella
Laurence Zitvogel
Harry Sokol
Soraya Taleb
author_sort Ludivine Laurans
collection DOAJ
description Summary: Although high-fat diet (HFD)-induced gut microbiota dysbiosis is known to affect atherosclerosis, the underlying mechanisms remain to be fully explored. Here, we show that the progression of atherosclerosis depends on a gut microbiota shaped by an HFD but not a high-cholesterol (HC) diet and, more particularly, on low fiber (LF) intake. Mechanistically, gut lymphoid cells impacted by HFD- or LF-induced microbiota dysbiosis highly proliferate in mesenteric lymph nodes (MLNs) and migrate from MLNs to the periphery, which fuels T cell accumulation within atherosclerotic plaques. This is associated with the induction of mucosal addressin cell adhesion molecule 1 (MAdCAM-1) within plaques and the presence of enterotropic lymphocytes expressing β7 integrin. MLN resection or lymphocyte deficiency abrogates the pro-atherogenic effects of a microbiota shaped by LF. Our study shows a pathological link between a diet-shaped microbiota, gut immune cells, and atherosclerosis, suggesting that a diet-modulated microbiome might be a suitable therapeutic target to prevent atherosclerosis.
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spelling doaj.art-dc302500baab428b8478bd6724febd132023-11-30T05:06:53ZengElsevierCell Reports2211-12472023-11-014211113350An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the peripheryLudivine Laurans0Nirmala Mouttoulingam1Mouna Chajadine2Aonghus Lavelle3Marc Diedisheim4Emilie Bacquer5Laura Creusot6Nadine Suffee7Bruno Esposito8Nada Joe Melhem9Wilfried Le Goff10Yacine Haddad11Jean-Louis Paul12Dominique Rainteau13Alain Tedgui14Hafid Ait-Oufella15Laurence Zitvogel16Harry Sokol17Soraya Taleb18Université Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceSorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Saint Antoine Hospital, Gastroenterology Department, 75012 Paris, France; Paris Centre for Microbiome Medicine (PaCeMM) FHU, Paris, FranceClinique Saint Gatien Alliance (NCT+), 37540 Saint-Cyr-sur-Loire, France; Institut Necker-Enfants Malades (INEM), Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, 75015 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceSorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Saint Antoine Hospital, Gastroenterology Department, 75012 Paris, France; Paris Centre for Microbiome Medicine (PaCeMM) FHU, Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, France; INSERM UMRS1166, ICAN-Institute of Cardiometabolism and Nutrition, Sorbonne University, 75013 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceINSERM UMRS1166, ICAN-Institute of Cardiometabolism and Nutrition, Sorbonne University, 75013 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, France; Gustave Roussy, Villejuif, France; Institut National de la Santé et de la Recherche Médicale, Gustave Roussy, UMR1015, Villejuif, FranceUniversité Paris-Sud, Equipe d’Accueil 4529, UFR de Pharmacie, Chatenay-Malabry, France and Assistance Publique Hôpitaux de Paris, Hôpital Européen Georges Pompidou, Paris, FranceParis Centre for Microbiome Medicine (PaCeMM) FHU, Paris, France; Sorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Saint Antoine Hospital, Clinical Metabolomics Department, 75012 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, FranceGustave Roussy, Villejuif, France; Institut National de la Santé et de la Recherche Médicale, Gustave Roussy, UMR1015, Villejuif, France; Université Paris-Saclay, Faculté de Médecine, Le Kremlin Bicêtre, France; Center of Clinical Investigations BIOTHERIS, INSERM CIC1428, Gustave Roussy, Villejuif, FranceSorbonne Université, INSERM, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Saint Antoine Hospital, Gastroenterology Department, 75012 Paris, France; Paris Centre for Microbiome Medicine (PaCeMM) FHU, Paris, France; INRAe, Micalis & AgroParisTech, Jouy en Josas, FranceUniversité Paris Cité, INSERM, Paris Cardiovascular Research Center, 75015 Paris, France; Corresponding authorSummary: Although high-fat diet (HFD)-induced gut microbiota dysbiosis is known to affect atherosclerosis, the underlying mechanisms remain to be fully explored. Here, we show that the progression of atherosclerosis depends on a gut microbiota shaped by an HFD but not a high-cholesterol (HC) diet and, more particularly, on low fiber (LF) intake. Mechanistically, gut lymphoid cells impacted by HFD- or LF-induced microbiota dysbiosis highly proliferate in mesenteric lymph nodes (MLNs) and migrate from MLNs to the periphery, which fuels T cell accumulation within atherosclerotic plaques. This is associated with the induction of mucosal addressin cell adhesion molecule 1 (MAdCAM-1) within plaques and the presence of enterotropic lymphocytes expressing β7 integrin. MLN resection or lymphocyte deficiency abrogates the pro-atherogenic effects of a microbiota shaped by LF. Our study shows a pathological link between a diet-shaped microbiota, gut immune cells, and atherosclerosis, suggesting that a diet-modulated microbiome might be a suitable therapeutic target to prevent atherosclerosis.http://www.sciencedirect.com/science/article/pii/S2211124723013621CP: MetabolismCP: Immunology
spellingShingle Ludivine Laurans
Nirmala Mouttoulingam
Mouna Chajadine
Aonghus Lavelle
Marc Diedisheim
Emilie Bacquer
Laura Creusot
Nadine Suffee
Bruno Esposito
Nada Joe Melhem
Wilfried Le Goff
Yacine Haddad
Jean-Louis Paul
Dominique Rainteau
Alain Tedgui
Hafid Ait-Oufella
Laurence Zitvogel
Harry Sokol
Soraya Taleb
An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery
Cell Reports
CP: Metabolism
CP: Immunology
title An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery
title_full An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery
title_fullStr An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery
title_full_unstemmed An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery
title_short An obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis-induced gut lymphocyte trafficking into the periphery
title_sort obesogenic diet increases atherosclerosis through promoting microbiota dysbiosis induced gut lymphocyte trafficking into the periphery
topic CP: Metabolism
CP: Immunology
url http://www.sciencedirect.com/science/article/pii/S2211124723013621
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