Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota

Abstract Background Endometriosis, affecting 10% of women in their reproductive years, remains poorly understood. Both individual and environmental unexplained factors are implicated in this heterogenous condition. This study aims to examine the influence of a Western diet on endometriosis lesion de...

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Main Authors: Guillaume Parpex, Benoît Chassaing, Mathilde Bourdon, Pietro Santulli, Ludivine Doridot, Marine Thomas, Frédéric Batteux, Sandrine Chouzenoux, Charles Chapron, Carole Nicco, Louis Marcellin
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Medicine
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Online Access:https://doi.org/10.1186/s12916-024-03738-9
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author Guillaume Parpex
Benoît Chassaing
Mathilde Bourdon
Pietro Santulli
Ludivine Doridot
Marine Thomas
Frédéric Batteux
Sandrine Chouzenoux
Charles Chapron
Carole Nicco
Louis Marcellin
author_facet Guillaume Parpex
Benoît Chassaing
Mathilde Bourdon
Pietro Santulli
Ludivine Doridot
Marine Thomas
Frédéric Batteux
Sandrine Chouzenoux
Charles Chapron
Carole Nicco
Louis Marcellin
author_sort Guillaume Parpex
collection DOAJ
description Abstract Background Endometriosis, affecting 10% of women in their reproductive years, remains poorly understood. Both individual and environmental unexplained factors are implicated in this heterogenous condition. This study aims to examine the influence of a Western diet on endometriosis lesion development in mice and to uncover the mechanisms involved. Methods Mice were fed either a control diet or a Western diet (high in fatty acids and low in fiber) for 4 weeks. Endometriosis was then surgically induced, and lesion development was monitored by ultrasound. After 7 weeks, the mice were sacrificed for analysis of lesion characteristics through RT-qPCR, immunohistochemistry, and flow cytometry. Additionally, the intestinal microbiota was assessed using 16S rRNA gene sequencing. Results Mice on the Western diet developed lesions that were significantly twice as large compared to those on the control diet. These lesions exhibited greater fibrosis and proliferation, alongside enhanced macrophage activity and leptin pathway expression. Changes in the intestinal microbiota were significantly noted after endometriosis induction, regardless of diet. Notably, mice on the Western diet with the most substantial lesions showed a loss of Akkermansia Muciniphila in their intestinal microbiota. Conclusions A Western diet significantly exacerbates lesion size in a mouse model of endometriosis, accompanied by metabolic and immune alterations. The onset of endometriosis also leads to substantial shifts in intestinal microbiota, suggesting a potential link between diet, intestinal health, and endometriosis development. Graphical Abstract
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spelling doaj-art-bd81e121f7724bde9565f376dc2b8db02025-08-20T02:13:39ZengBMCBMC Medicine1741-70152024-11-0122111510.1186/s12916-024-03738-9Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiotaGuillaume Parpex0Benoît Chassaing1Mathilde Bourdon2Pietro Santulli3Ludivine Doridot4Marine Thomas5Frédéric Batteux6Sandrine Chouzenoux7Charles Chapron8Carole Nicco9Louis Marcellin10Department of Gynecology Obstetrics II and Reproductive Medicine (Professor Chapron), Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpital Universitaire Paris Centre (HUPC), Centre Hospitalier Universitaire (CHU) CochinInstitut Pasteur, Université Paris Cité, Microbiome-Host Interaction GroupDepartment of Gynecology Obstetrics II and Reproductive Medicine (Professor Chapron), Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpital Universitaire Paris Centre (HUPC), Centre Hospitalier Universitaire (CHU) CochinDepartment of Gynecology Obstetrics II and Reproductive Medicine (Professor Chapron), Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpital Universitaire Paris Centre (HUPC), Centre Hospitalier Universitaire (CHU) CochinUniversité Paris Cité, CNRS, Institut CochinUniversité Paris Cité, CNRS, Institut CochinUniversité Paris Cité, CNRS, Institut CochinUniversité Paris Cité, CNRS, Institut CochinDepartment of Gynecology Obstetrics II and Reproductive Medicine (Professor Chapron), Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpital Universitaire Paris Centre (HUPC), Centre Hospitalier Universitaire (CHU) CochinUniversité Paris Cité, CNRS, Institut CochinDepartment of Gynecology Obstetrics II and Reproductive Medicine (Professor Chapron), Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpital Universitaire Paris Centre (HUPC), Centre Hospitalier Universitaire (CHU) CochinAbstract Background Endometriosis, affecting 10% of women in their reproductive years, remains poorly understood. Both individual and environmental unexplained factors are implicated in this heterogenous condition. This study aims to examine the influence of a Western diet on endometriosis lesion development in mice and to uncover the mechanisms involved. Methods Mice were fed either a control diet or a Western diet (high in fatty acids and low in fiber) for 4 weeks. Endometriosis was then surgically induced, and lesion development was monitored by ultrasound. After 7 weeks, the mice were sacrificed for analysis of lesion characteristics through RT-qPCR, immunohistochemistry, and flow cytometry. Additionally, the intestinal microbiota was assessed using 16S rRNA gene sequencing. Results Mice on the Western diet developed lesions that were significantly twice as large compared to those on the control diet. These lesions exhibited greater fibrosis and proliferation, alongside enhanced macrophage activity and leptin pathway expression. Changes in the intestinal microbiota were significantly noted after endometriosis induction, regardless of diet. Notably, mice on the Western diet with the most substantial lesions showed a loss of Akkermansia Muciniphila in their intestinal microbiota. Conclusions A Western diet significantly exacerbates lesion size in a mouse model of endometriosis, accompanied by metabolic and immune alterations. The onset of endometriosis also leads to substantial shifts in intestinal microbiota, suggesting a potential link between diet, intestinal health, and endometriosis development. Graphical Abstracthttps://doi.org/10.1186/s12916-024-03738-9EndometriosisDietIntestinal MicrobiotaAkkermansia muciniphila
spellingShingle Guillaume Parpex
Benoît Chassaing
Mathilde Bourdon
Pietro Santulli
Ludivine Doridot
Marine Thomas
Frédéric Batteux
Sandrine Chouzenoux
Charles Chapron
Carole Nicco
Louis Marcellin
Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota
BMC Medicine
Endometriosis
Diet
Intestinal Microbiota
Akkermansia muciniphila
title Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota
title_full Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota
title_fullStr Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota
title_full_unstemmed Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota
title_short Western diet promotes endometriotic lesion growth in mice and induces depletion of Akkermansia muciniphila in intestinal microbiota
title_sort western diet promotes endometriotic lesion growth in mice and induces depletion of akkermansia muciniphila in intestinal microbiota
topic Endometriosis
Diet
Intestinal Microbiota
Akkermansia muciniphila
url https://doi.org/10.1186/s12916-024-03738-9
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