Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation

Abstract Morbid obesity induces adipose stem cell (ASC) shortage that impairs visceral adipose tissue (VAT) homeostasis. Macrophages cooperate with ASCs to regulate VAT metabolism, their impact on ASC shortage remains elusive. TNF-α-induced protein 8-like 2 (TIPE2) is an important regulator in immun...

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Main Authors: Yan Tao, Jinhao Zang, Tianci Wang, Peixuan Song, Zixin Zhou, Huijie Li, Yalin Wang, Yiyang Liu, Haipeng Jie, Mei Kuang, Hui Zhao, Fuwu Wang, Shen Dai, Chun Guo, Faliang Zhu, Haiting Mao, Fengming Liu, Lining Zhang, Qun Wang
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62690-1
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author Yan Tao
Jinhao Zang
Tianci Wang
Peixuan Song
Zixin Zhou
Huijie Li
Yalin Wang
Yiyang Liu
Haipeng Jie
Mei Kuang
Hui Zhao
Fuwu Wang
Shen Dai
Chun Guo
Faliang Zhu
Haiting Mao
Fengming Liu
Lining Zhang
Qun Wang
author_facet Yan Tao
Jinhao Zang
Tianci Wang
Peixuan Song
Zixin Zhou
Huijie Li
Yalin Wang
Yiyang Liu
Haipeng Jie
Mei Kuang
Hui Zhao
Fuwu Wang
Shen Dai
Chun Guo
Faliang Zhu
Haiting Mao
Fengming Liu
Lining Zhang
Qun Wang
author_sort Yan Tao
collection DOAJ
description Abstract Morbid obesity induces adipose stem cell (ASC) shortage that impairs visceral adipose tissue (VAT) homeostasis. Macrophages cooperate with ASCs to regulate VAT metabolism, their impact on ASC shortage remains elusive. TNF-α-induced protein 8-like 2 (TIPE2) is an important regulator in immune cells, its expression in VAT macrophages and function in macrophage-ASC crosstalk are largely unknown. Here, TIPE2 loss in VAT macrophages promotes ASC ferroptosis to aggravate diet-induced obesity and metabolic disorders in male mice, which can be corrected by macrophage-specific TIPE2 restoration in VAT. Mechanistically, TIPE2-deficient macrophages propagate mitochondrial fragmentation and reduce delivery of exosomal ferritin toward ASCs, resulting in mitochondrial ROS and Fe2+ overload that dictates ASC ferroptosis. TIPE2 interacts with IP3R to constrain IP3R-Ca2+-Drp1 axis, thereby preventing excessive mitochondrial fission and enabling macrophages to protect against ASC ferroptosis. This study reveals distinct obesity-associated macrophages that dictate ASC ferroptosis, and proposes macrophage TIPE2 as therapeutic target for obesity-related diseases.
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spelling doaj-art-e3c4f7ed9f1340edac2171df95430dca2025-08-20T04:02:54ZengNature PortfolioNature Communications2041-17232025-08-0116112010.1038/s41467-025-62690-1Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentationYan Tao0Jinhao Zang1Tianci Wang2Peixuan Song3Zixin Zhou4Huijie Li5Yalin Wang6Yiyang Liu7Haipeng Jie8Mei Kuang9Hui Zhao10Fuwu Wang11Shen Dai12Chun Guo13Faliang Zhu14Haiting Mao15Fengming Liu16Lining Zhang17Qun Wang18Key Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityDepartment of Statistics, Columbia UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityDepartment of Clinical Laboratory, The Second Hospital, Cheeloo College of Medicine, Shandong UniversityKey Laboratory for Experimental Teratology of Ministry of Education, Shandong Key Laboratory of Mental Disorders, Department of Histology and Embryology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityDepartment of Physiology and Pathology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityDepartment of Clinical Laboratory, The Second Hospital, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityKey Laboratory of Infection and Immunity of Shandong Province, Department of Immunology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong UniversityAbstract Morbid obesity induces adipose stem cell (ASC) shortage that impairs visceral adipose tissue (VAT) homeostasis. Macrophages cooperate with ASCs to regulate VAT metabolism, their impact on ASC shortage remains elusive. TNF-α-induced protein 8-like 2 (TIPE2) is an important regulator in immune cells, its expression in VAT macrophages and function in macrophage-ASC crosstalk are largely unknown. Here, TIPE2 loss in VAT macrophages promotes ASC ferroptosis to aggravate diet-induced obesity and metabolic disorders in male mice, which can be corrected by macrophage-specific TIPE2 restoration in VAT. Mechanistically, TIPE2-deficient macrophages propagate mitochondrial fragmentation and reduce delivery of exosomal ferritin toward ASCs, resulting in mitochondrial ROS and Fe2+ overload that dictates ASC ferroptosis. TIPE2 interacts with IP3R to constrain IP3R-Ca2+-Drp1 axis, thereby preventing excessive mitochondrial fission and enabling macrophages to protect against ASC ferroptosis. This study reveals distinct obesity-associated macrophages that dictate ASC ferroptosis, and proposes macrophage TIPE2 as therapeutic target for obesity-related diseases.https://doi.org/10.1038/s41467-025-62690-1
spellingShingle Yan Tao
Jinhao Zang
Tianci Wang
Peixuan Song
Zixin Zhou
Huijie Li
Yalin Wang
Yiyang Liu
Haipeng Jie
Mei Kuang
Hui Zhao
Fuwu Wang
Shen Dai
Chun Guo
Faliang Zhu
Haiting Mao
Fengming Liu
Lining Zhang
Qun Wang
Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
Nature Communications
title Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
title_full Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
title_fullStr Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
title_full_unstemmed Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
title_short Obesity-associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
title_sort obesity associated macrophages dictate adipose stem cell ferroptosis and visceral fat dysfunction by propagating mitochondrial fragmentation
url https://doi.org/10.1038/s41467-025-62690-1
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