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Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries

Obesity induced by a high-fat diet (HFD) leads to the excessive consumption of primordial follicles (PFs) in the ovaries. There is systemic chronic inflammation under HFD conditions, but no previous studies have explored whether there is a certain causal relationship between HFD-induced chronic infl...

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Autores principales: Fan, Zhihao, Zhang, Xiaoqian, Shang, Yanxing, Zou, Maosheng, Zhou, Meng, E, Qiukai, Fei, Shujia, Chen, Wei, Li, Jing, Zhang, Xuesen, Liu, Xiaoqiu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9100959/
https://www.ncbi.nlm.nih.gov/pubmed/35563189
http://dx.doi.org/10.3390/ijms23094797
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author Fan, Zhihao
Zhang, Xiaoqian
Shang, Yanxing
Zou, Maosheng
Zhou, Meng
E, Qiukai
Fei, Shujia
Chen, Wei
Li, Jing
Zhang, Xuesen
Liu, Xiaoqiu
author_facet Fan, Zhihao
Zhang, Xiaoqian
Shang, Yanxing
Zou, Maosheng
Zhou, Meng
E, Qiukai
Fei, Shujia
Chen, Wei
Li, Jing
Zhang, Xuesen
Liu, Xiaoqiu
author_sort Fan, Zhihao
collection PubMed
description Obesity induced by a high-fat diet (HFD) leads to the excessive consumption of primordial follicles (PFs) in the ovaries. There is systemic chronic inflammation under HFD conditions, but no previous studies have explored whether there is a certain causal relationship between HFD-induced chronic inflammation and the overactivation of PFs. Here, we showed that HFD causes disorders of intestinal microflora in mice, with five Gram-negative bacteria showing the most profound increase at the genus level compared to the normal diet (ND) groups and contributes to the production of endotoxin. Endotoxin promotes M1 macrophage infiltration in the ovaries, where they exhibit proinflammatory actions by secreting cytokines IL-6, IL-8, and TNFα. These cytokines then boost the activation of PFs by activating Signal Transducer and Activator of Transcription 3 (STAT3) signaling in follicles. Interestingly, transplantation of the HFD intestinal microflora to the ND mice partly replicates ovarian macrophage infiltration, proinflammation, and the overactivation of PFs. Conversely, transplanting the ND fecal microbiota to the HFD mice can alleviate ovarian inflammation and rescue the excessive consumption of PFs. Our findings uncover a novel and critical function of gut microbes in the process of PF overactivation under HFD conditions, and may provide a new theoretical basis for the microbial treatment of patients with premature ovarian insufficiency caused by HFD.
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spelling pubmed-91009592022-05-14 Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries Fan, Zhihao Zhang, Xiaoqian Shang, Yanxing Zou, Maosheng Zhou, Meng E, Qiukai Fei, Shujia Chen, Wei Li, Jing Zhang, Xuesen Liu, Xiaoqiu Int J Mol Sci Article Obesity induced by a high-fat diet (HFD) leads to the excessive consumption of primordial follicles (PFs) in the ovaries. There is systemic chronic inflammation under HFD conditions, but no previous studies have explored whether there is a certain causal relationship between HFD-induced chronic inflammation and the overactivation of PFs. Here, we showed that HFD causes disorders of intestinal microflora in mice, with five Gram-negative bacteria showing the most profound increase at the genus level compared to the normal diet (ND) groups and contributes to the production of endotoxin. Endotoxin promotes M1 macrophage infiltration in the ovaries, where they exhibit proinflammatory actions by secreting cytokines IL-6, IL-8, and TNFα. These cytokines then boost the activation of PFs by activating Signal Transducer and Activator of Transcription 3 (STAT3) signaling in follicles. Interestingly, transplantation of the HFD intestinal microflora to the ND mice partly replicates ovarian macrophage infiltration, proinflammation, and the overactivation of PFs. Conversely, transplanting the ND fecal microbiota to the HFD mice can alleviate ovarian inflammation and rescue the excessive consumption of PFs. Our findings uncover a novel and critical function of gut microbes in the process of PF overactivation under HFD conditions, and may provide a new theoretical basis for the microbial treatment of patients with premature ovarian insufficiency caused by HFD. MDPI 2022-04-27 /pmc/articles/PMC9100959/ /pubmed/35563189 http://dx.doi.org/10.3390/ijms23094797 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Fan, Zhihao
Zhang, Xiaoqian
Shang, Yanxing
Zou, Maosheng
Zhou, Meng
E, Qiukai
Fei, Shujia
Chen, Wei
Li, Jing
Zhang, Xuesen
Liu, Xiaoqiu
Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries
title Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries
title_full Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries
title_fullStr Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries
title_full_unstemmed Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries
title_short Intestinal Flora Changes Induced by a High-Fat Diet Promote Activation of Primordial Follicles through Macrophage Infiltration and Inflammatory Factor Secretion in Mouse Ovaries
title_sort intestinal flora changes induced by a high-fat diet promote activation of primordial follicles through macrophage infiltration and inflammatory factor secretion in mouse ovaries
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9100959/
https://www.ncbi.nlm.nih.gov/pubmed/35563189
http://dx.doi.org/10.3390/ijms23094797
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