ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis

Maintaining cholesterol homeostasis is critical for preserving adipocyte function during the progression of obesity. Despite this, the regulatory role of cholesterol esterification in governing adipocyte expandability has been understudied. Acyl-coenzyme A (CoA):cholesterol acyltransferase/Sterol O-...

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Main Authors: Qing Liu, Xiaolin Wu, Wei Duan, Xiaohan Pan, Martin Wabitsch, Ming Lu, Jing Li, Li-Hao Huang, Zhangsen Zhou, Yuyan Zhu
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Journal of Lipid Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S0022227524001858
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author Qing Liu
Xiaolin Wu
Wei Duan
Xiaohan Pan
Martin Wabitsch
Ming Lu
Jing Li
Li-Hao Huang
Zhangsen Zhou
Yuyan Zhu
author_facet Qing Liu
Xiaolin Wu
Wei Duan
Xiaohan Pan
Martin Wabitsch
Ming Lu
Jing Li
Li-Hao Huang
Zhangsen Zhou
Yuyan Zhu
author_sort Qing Liu
collection DOAJ
description Maintaining cholesterol homeostasis is critical for preserving adipocyte function during the progression of obesity. Despite this, the regulatory role of cholesterol esterification in governing adipocyte expandability has been understudied. Acyl-coenzyme A (CoA):cholesterol acyltransferase/Sterol O-acyltransferase 1 (ACAT1/SOAT1) is the dominant enzyme to synthesize cholesteryl ester in most tissues. Our previous study demonstrated that knockdown of either ACAT1 or ACAT2 impaired adipogenesis. However, the underlying mechanism of how ACAT1 mediates adipogenesis remains unclear. Here, we reported that ACAT1 is the dominant isoform in white adipose tissue of both humans and mice, and knocking out ACAT1 reduced fat mass in mice. Furthermore, ACAT1-deficiency inhibited the early stage of adipogenesis via attenuating PPARγ pathway. Mechanistically, ACAT1 deficiency inhibited SREBP2-mediated cholesterol uptake and thus reduced intracellular and plasma membrane cholesterol levels during adipogenesis. Replenishing cholesterol could rescue adipogenic master gene–Pparγ′s—transcription in ACAT1-deficient cells during adipogenesis. Finally, overexpression of catalytically functional ACAT1, not the catalytic-dead ACAT1, rescued cholesterol levels and efficiently rescued the transcription of PPARγ as well as the adipogenesis in ACAT1-deficient preadipocytes. In summary, our study revealed the indispensable role of ACAT1 in adipogenesis via regulating intracellular cholesterol homeostasis.
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spelling doaj-art-8965204e2bdc40ddb7795e82d6408da42025-08-20T02:27:46ZengElsevierJournal of Lipid Research0022-22752024-12-01651210068010.1016/j.jlr.2024.100680ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasisQing Liu0Xiaolin Wu1Wei Duan2Xiaohan Pan3Martin Wabitsch4Ming Lu5Jing Li6Li-Hao Huang7Zhangsen Zhou8Yuyan Zhu9Department of Food Science and Nutrition, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong Kong; Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong KongDepartment of Food Science and Nutrition, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong Kong; Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong KongShanghai Institute of Nutrition and Health, Chinese Academy of Sciences, Shanghai, ChinaDepartment of Food Science and Nutrition, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong Kong; Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong KongDivision of Pediatric Endocrinology and Diabetes, Department of Pediatrics and Adolescent Medicine, University of Ulm, Ulm, GermanyShanghai Institute of Nutrition and Health, Chinese Academy of Sciences, Shanghai, ChinaDepartment of Computing, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong KongShanghai Key Laboratory of Metabolic Remodeling and Health, Institute of Metabolism and Integrative Biology, Liver Cancer Institute Zhongshan Hospital, Fudan University, Shanghai, ChinaShanghai Institute of Nutrition and Health, Chinese Academy of Sciences, Shanghai, ChinaDepartment of Food Science and Nutrition, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong Kong; Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong Kong; Research Institute for Future Food, The Hong Kong Polytechnic University, Kowloon, Hung Hom, Hong Kong; The Hong Kong Polytechnic University Shenzhen Research Institute, The Hong Kong Polytechnic University, Shenzhen, China; For correspondence: Yuyan ZhuMaintaining cholesterol homeostasis is critical for preserving adipocyte function during the progression of obesity. Despite this, the regulatory role of cholesterol esterification in governing adipocyte expandability has been understudied. Acyl-coenzyme A (CoA):cholesterol acyltransferase/Sterol O-acyltransferase 1 (ACAT1/SOAT1) is the dominant enzyme to synthesize cholesteryl ester in most tissues. Our previous study demonstrated that knockdown of either ACAT1 or ACAT2 impaired adipogenesis. However, the underlying mechanism of how ACAT1 mediates adipogenesis remains unclear. Here, we reported that ACAT1 is the dominant isoform in white adipose tissue of both humans and mice, and knocking out ACAT1 reduced fat mass in mice. Furthermore, ACAT1-deficiency inhibited the early stage of adipogenesis via attenuating PPARγ pathway. Mechanistically, ACAT1 deficiency inhibited SREBP2-mediated cholesterol uptake and thus reduced intracellular and plasma membrane cholesterol levels during adipogenesis. Replenishing cholesterol could rescue adipogenic master gene–Pparγ′s—transcription in ACAT1-deficient cells during adipogenesis. Finally, overexpression of catalytically functional ACAT1, not the catalytic-dead ACAT1, rescued cholesterol levels and efficiently rescued the transcription of PPARγ as well as the adipogenesis in ACAT1-deficient preadipocytes. In summary, our study revealed the indispensable role of ACAT1 in adipogenesis via regulating intracellular cholesterol homeostasis.http://www.sciencedirect.com/science/article/pii/S0022227524001858adipocytescholesterol/metabolismcholesterol/traffickinglipid raftsnuclear receptors/SREBPPPARγ
spellingShingle Qing Liu
Xiaolin Wu
Wei Duan
Xiaohan Pan
Martin Wabitsch
Ming Lu
Jing Li
Li-Hao Huang
Zhangsen Zhou
Yuyan Zhu
ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
Journal of Lipid Research
adipocytes
cholesterol/metabolism
cholesterol/trafficking
lipid rafts
nuclear receptors/SREBP
PPARγ
title ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
title_full ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
title_fullStr ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
title_full_unstemmed ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
title_short ACAT1/SOAT1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
title_sort acat1 soat1 maintains adipogenic ability in preadipocytes by regulating cholesterol homeostasis
topic adipocytes
cholesterol/metabolism
cholesterol/trafficking
lipid rafts
nuclear receptors/SREBP
PPARγ
url http://www.sciencedirect.com/science/article/pii/S0022227524001858
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