Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion

Abstract Obesity is associated with skeletal deterioration and increased fracture risk, but the underlying mechanism is unclear. Herein, it is shown that obese gut microbiota promotes skeletal deterioration by inducing bone marrow macrophages (BMMs) senescence and grancalcin (GCA) secretion. Obese m...

Full description

Saved in:
Bibliographic Details
Main Authors: Min Huang, Mei Huang, Ling Liu, Fang Yang, Chen He, Yu‐Chen Sun, Yu‐Rui Jiao, Xiang Tang, Jing Hou, Kai‐Xuan Chen, Wen‐Zhen He, Jie Wei, Hui‐Ling Chen, Xia Li, Chao Zeng, Guang‐Hua Lei, Chang‐Jun Li
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202502634
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849708952498995200
author Min Huang
Mei Huang
Ling Liu
Fang Yang
Chen He
Yu‐Chen Sun
Yu‐Rui Jiao
Xiang Tang
Jing Hou
Kai‐Xuan Chen
Wen‐Zhen He
Jie Wei
Hui‐Ling Chen
Xia Li
Chao Zeng
Guang‐Hua Lei
Chang‐Jun Li
author_facet Min Huang
Mei Huang
Ling Liu
Fang Yang
Chen He
Yu‐Chen Sun
Yu‐Rui Jiao
Xiang Tang
Jing Hou
Kai‐Xuan Chen
Wen‐Zhen He
Jie Wei
Hui‐Ling Chen
Xia Li
Chao Zeng
Guang‐Hua Lei
Chang‐Jun Li
author_sort Min Huang
collection DOAJ
description Abstract Obesity is associated with skeletal deterioration and increased fracture risk, but the underlying mechanism is unclear. Herein, it is shown that obese gut microbiota promotes skeletal deterioration by inducing bone marrow macrophages (BMMs) senescence and grancalcin (GCA) secretion. Obese mice and those receiving obese fecal microbiota transplants exhibit increased senescent macrophages and elevated GCA expression in the bone marrow. In a study of 40 participants, it is found that obese patients are associated with higher serum GCA levels. It is further revealed that obese gut‐microbiota derived lipopolysaccharides (LPS) stimulate GCA expression in senescent BMMs via activating Toll‐like receptor 4 pathway. Mice with depletion of the Gca gene are resistant to the negative effects of obesity and LPS on bone. Moreover, neutralizing antibody against GCA mitigates skeletal deterioration in obese mice and LPS‐induced chronic inflammation mouse model. The data suggest that the interaction between gut microbiota and the immune system contributes to obesity‐associated skeletal deterioration, and targeting senescent macrophages and GCA shows potential of protecting skeletal health in obese population.
format Article
id doaj-art-e0eba02be7bd4e95b766d56c4c0ca658
institution DOAJ
issn 2198-3844
language English
publishDate 2025-07-01
publisher Wiley
record_format Article
series Advanced Science
spelling doaj-art-e0eba02be7bd4e95b766d56c4c0ca6582025-08-20T03:15:29ZengWileyAdvanced Science2198-38442025-07-011228n/an/a10.1002/advs.202502634Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin SecretionMin Huang0Mei Huang1Ling Liu2Fang Yang3Chen He4Yu‐Chen Sun5Yu‐Rui Jiao6Xiang Tang7Jing Hou8Kai‐Xuan Chen9Wen‐Zhen He10Jie Wei11Hui‐Ling Chen12Xia Li13Chao Zeng14Guang‐Hua Lei15Chang‐Jun Li16Department of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Clinical Laboratory Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaHunan Key Laboratory of Joint Degeneration and Injury Changsha 410008 ChinaDepartment of Endocrine Subspecialty of Gerontology Xiangya Hospital, Central South University Changsha 410008 ChinaDepartment of General Medicine The Fifth Affiliated Hospital of Xinjiang Medical University Urumqi 830000 ChinaHunan Key Laboratory of Joint Degeneration and Injury Changsha 410008 ChinaHunan Key Laboratory of Joint Degeneration and Injury Changsha 410008 ChinaDepartment of Endocrinology Endocrinology Research Center Xiangya Hospital Central South University Changsha 410008 ChinaAbstract Obesity is associated with skeletal deterioration and increased fracture risk, but the underlying mechanism is unclear. Herein, it is shown that obese gut microbiota promotes skeletal deterioration by inducing bone marrow macrophages (BMMs) senescence and grancalcin (GCA) secretion. Obese mice and those receiving obese fecal microbiota transplants exhibit increased senescent macrophages and elevated GCA expression in the bone marrow. In a study of 40 participants, it is found that obese patients are associated with higher serum GCA levels. It is further revealed that obese gut‐microbiota derived lipopolysaccharides (LPS) stimulate GCA expression in senescent BMMs via activating Toll‐like receptor 4 pathway. Mice with depletion of the Gca gene are resistant to the negative effects of obesity and LPS on bone. Moreover, neutralizing antibody against GCA mitigates skeletal deterioration in obese mice and LPS‐induced chronic inflammation mouse model. The data suggest that the interaction between gut microbiota and the immune system contributes to obesity‐associated skeletal deterioration, and targeting senescent macrophages and GCA shows potential of protecting skeletal health in obese population.https://doi.org/10.1002/advs.202502634obesityskeletal deteriorationimmunosenescencegrancalcingut‐microbiota
spellingShingle Min Huang
Mei Huang
Ling Liu
Fang Yang
Chen He
Yu‐Chen Sun
Yu‐Rui Jiao
Xiang Tang
Jing Hou
Kai‐Xuan Chen
Wen‐Zhen He
Jie Wei
Hui‐Ling Chen
Xia Li
Chao Zeng
Guang‐Hua Lei
Chang‐Jun Li
Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion
Advanced Science
obesity
skeletal deterioration
immunosenescence
grancalcin
gut‐microbiota
title Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion
title_full Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion
title_fullStr Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion
title_full_unstemmed Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion
title_short Gut Microbiota Modulates Obesity‐Associated Skeletal Deterioration Through Macrophage Aging and Grancalcin Secretion
title_sort gut microbiota modulates obesity associated skeletal deterioration through macrophage aging and grancalcin secretion
topic obesity
skeletal deterioration
immunosenescence
grancalcin
gut‐microbiota
url https://doi.org/10.1002/advs.202502634
work_keys_str_mv AT minhuang gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT meihuang gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT lingliu gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT fangyang gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT chenhe gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT yuchensun gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT yuruijiao gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT xiangtang gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT jinghou gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT kaixuanchen gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT wenzhenhe gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT jiewei gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT huilingchen gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT xiali gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT chaozeng gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT guanghualei gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion
AT changjunli gutmicrobiotamodulatesobesityassociatedskeletaldeteriorationthroughmacrophageagingandgrancalcinsecretion