Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells

Abstract Endothelial dysfunction is a hallmark of various metabolic disorders and plays a pivotal role in the progression of cardiovascular diseases, including coronary microvascular dysfunction and myocardial ischemia. Lipid droplets (LDs) have emerged as key regulators of fatty acid metabolism in...

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Main Authors: Yun-Ting Wang, Alexandra K. Moura, Rui Zuo, Zhengchao Wang, Kiana Roudbari, Jenny Z. Hu, Mi Wang, Pin-Lan Li, Yang Zhang, Xiang Li
Format: Article
Language:English
Published: Nature Publishing Group 2025-08-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02669-5
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author Yun-Ting Wang
Alexandra K. Moura
Rui Zuo
Zhengchao Wang
Kiana Roudbari
Jenny Z. Hu
Mi Wang
Pin-Lan Li
Yang Zhang
Xiang Li
author_facet Yun-Ting Wang
Alexandra K. Moura
Rui Zuo
Zhengchao Wang
Kiana Roudbari
Jenny Z. Hu
Mi Wang
Pin-Lan Li
Yang Zhang
Xiang Li
author_sort Yun-Ting Wang
collection DOAJ
description Abstract Endothelial dysfunction is a hallmark of various metabolic disorders and plays a pivotal role in the progression of cardiovascular diseases, including coronary microvascular dysfunction and myocardial ischemia. Lipid droplets (LDs) have emerged as key regulators of fatty acid metabolism in endothelial cells (ECs), but their functional role in lipotoxicity-induced EC damage in the context of coronary microvascular dysfunction remains unclear. Here, we examined the contribution of LD biogenesis to oleic acid-induced lipotoxic effects in mouse cardiac ECs (MCECs). Our findings reveal that oleic acid markedly increases LD biogenesis in MCECs via a diacylglycerol O-acyltransferase 1 (DGAT1)-dependent pathway. This process is accompanied by substantial disruptions in cellular homeostasis, including elevated endoplasmic reticulum (ER) stress, impaired mitochondrial respiration, reduced ATP production, and heightened hypoxic responses. Furthermore, oleic acid-induced lipotoxicity is primarily mediated by ferroptosis−a form of lipid peroxide-dependent, caspase-independent cell death. Notably, pharmacological inhibition or genetic knockdown of DGAT1, which diminishes LD biogenesis, exacerbates oleic acid-induced cellular stress, mitochondrial dysfunction, and ferroptosis in MCECs. These results suggest that LD biogenesis plays a protective role in mitigating lipotoxicity, preserving mitochondrial function, and preventing lipid peroxide accumulation and ferroptosis, thereby safeguarding cardiac microvascular endothelial function in the context of metabolic disorders.
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spelling doaj-art-d90a42f300164be1ab827c6076f4dbba2025-08-20T03:45:45ZengNature Publishing GroupCell Death Discovery2058-77162025-08-0111111710.1038/s41420-025-02669-5Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cellsYun-Ting Wang0Alexandra K. Moura1Rui Zuo2Zhengchao Wang3Kiana Roudbari4Jenny Z. Hu5Mi Wang6Pin-Lan Li7Yang Zhang8Xiang Li9Department of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacology and Toxicology, Virginia Commonwealth University, School of MedicineDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonDepartment of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of HoustonAbstract Endothelial dysfunction is a hallmark of various metabolic disorders and plays a pivotal role in the progression of cardiovascular diseases, including coronary microvascular dysfunction and myocardial ischemia. Lipid droplets (LDs) have emerged as key regulators of fatty acid metabolism in endothelial cells (ECs), but their functional role in lipotoxicity-induced EC damage in the context of coronary microvascular dysfunction remains unclear. Here, we examined the contribution of LD biogenesis to oleic acid-induced lipotoxic effects in mouse cardiac ECs (MCECs). Our findings reveal that oleic acid markedly increases LD biogenesis in MCECs via a diacylglycerol O-acyltransferase 1 (DGAT1)-dependent pathway. This process is accompanied by substantial disruptions in cellular homeostasis, including elevated endoplasmic reticulum (ER) stress, impaired mitochondrial respiration, reduced ATP production, and heightened hypoxic responses. Furthermore, oleic acid-induced lipotoxicity is primarily mediated by ferroptosis−a form of lipid peroxide-dependent, caspase-independent cell death. Notably, pharmacological inhibition or genetic knockdown of DGAT1, which diminishes LD biogenesis, exacerbates oleic acid-induced cellular stress, mitochondrial dysfunction, and ferroptosis in MCECs. These results suggest that LD biogenesis plays a protective role in mitigating lipotoxicity, preserving mitochondrial function, and preventing lipid peroxide accumulation and ferroptosis, thereby safeguarding cardiac microvascular endothelial function in the context of metabolic disorders.https://doi.org/10.1038/s41420-025-02669-5
spellingShingle Yun-Ting Wang
Alexandra K. Moura
Rui Zuo
Zhengchao Wang
Kiana Roudbari
Jenny Z. Hu
Mi Wang
Pin-Lan Li
Yang Zhang
Xiang Li
Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
Cell Death Discovery
title Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
title_full Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
title_fullStr Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
title_full_unstemmed Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
title_short Defective lipid droplet biogenesis exacerbates oleic acid-induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
title_sort defective lipid droplet biogenesis exacerbates oleic acid induced cellular homeostasis disruption and ferroptosis in mouse cardiac endothelial cells
url https://doi.org/10.1038/s41420-025-02669-5
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