Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway

<b>Background/Objectives:</b> Studies have shown that Atractylenolide I (AT-I) can exert anti-inflammatory and anti-oxidative effects, protecting against the development of various kinds of cardiovascular diseases. However, whether AT-I prevents nicotine-induced atherogenesis is unknown....

Full description

Saved in:
Bibliographic Details
Main Authors: Huan-Huan Li, Xian Liu, Yu-Ping Wang, Xi Xu, Lin Zhu, Wei Zhang, Kun Ren
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/15/5/329
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849327145735684096
author Huan-Huan Li
Xian Liu
Yu-Ping Wang
Xi Xu
Lin Zhu
Wei Zhang
Kun Ren
author_facet Huan-Huan Li
Xian Liu
Yu-Ping Wang
Xi Xu
Lin Zhu
Wei Zhang
Kun Ren
author_sort Huan-Huan Li
collection DOAJ
description <b>Background/Objectives:</b> Studies have shown that Atractylenolide I (AT-I) can exert anti-inflammatory and anti-oxidative effects, protecting against the development of various kinds of cardiovascular diseases. However, whether AT-I prevents nicotine-induced atherogenesis is unknown. This study was designed to explore the effects of AT-I on nicotine-induced macrophage pyroptosis and the progression of atherosclerosis. <b>Methods:</b> RT-qPCR and Western blot were used to detect the mRNA and protein levels of TXNIP and pyroptosis-related factors in THP-1-derived macrophages. ELISA was used to detect the secretion of pro-inflammatory cytokines. Hoechst/PI double-staining assay was used to assess plasma membrane integrity. The ROS assay kit, LDH release assay kit, and caspase-1 activity assay kit were used to detect ROS production, LDH release, and caspase-1 activity. Oil Red O, HE, and Masson staining were used to evaluate lipid accumulation, lesion size, and plaque stability in HFD-fed apoE<sup>−/−</sup> mice. <b>Results:</b> AT-I treatment significantly decreased pyroptosis-related factors expression, disrupted plasma membrane integrity, and down-regulated pro-inflammatory cytokines secretion, thereby inhibiting nicotine-induced pyroptosis of THP-1-derived macrophages. In addition, AT-I decreased ROS production and the expression of TLR4 and TXNIP. Lentivirus overexpression of TLR4 or TXNIP, or pre-treatment with ROS agonist, mainly reversed the anti-pyroptotic effects of AT-I in nicotine-treated THP-1-derived macrophages. Additionally, administering AT-I to HFD-fed apoE<sup>−/−</sup> mice markedly decreased nicotine-induced up-regulation of pyroptosis-related proteins in the aortas. Enzymatic methods and ELISA assay suggested that AT-I improved dyslipidemia and inflammation in vivo. Oil Red O, HE, and Masson staining showed that AT-I alleviated lipid accumulation, decreased plaque size, and increased plaque stability. <b>Conclusions:</b> Taken together, AT-I can be regarded as a potential phytomedicine that protects against macrophage pyroptosis and atherosclerosis triggered by nicotine.
format Article
id doaj-art-1cde72fecf3f4814b9a61b37c2022931
institution Kabale University
issn 2218-1989
language English
publishDate 2025-05-01
publisher MDPI AG
record_format Article
series Metabolites
spelling doaj-art-1cde72fecf3f4814b9a61b37c20229312025-08-20T03:47:58ZengMDPI AGMetabolites2218-19892025-05-0115532910.3390/metabo15050329Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 PathwayHuan-Huan Li0Xian Liu1Yu-Ping Wang2Xi Xu3Lin Zhu4Wei Zhang5Kun Ren6College of Traditional Chinese Medicine, Anhui University of Chinese Medicine, Hefei 230012, ChinaCollege of Nursing, Anhui University of Chinese Medicine, Hefei 230012, ChinaCollege of Nursing, Anhui University of Chinese Medicine, Hefei 230012, ChinaCollege of Nursing, Anhui University of Chinese Medicine, Hefei 230012, ChinaCollege of Pharmacy, Anhui University of Chinese Medicine, Hefei 230012, ChinaCollege of Pharmacy, Anhui University of Chinese Medicine, Hefei 230012, ChinaCollege of Nursing, Anhui University of Chinese Medicine, Hefei 230012, China<b>Background/Objectives:</b> Studies have shown that Atractylenolide I (AT-I) can exert anti-inflammatory and anti-oxidative effects, protecting against the development of various kinds of cardiovascular diseases. However, whether AT-I prevents nicotine-induced atherogenesis is unknown. This study was designed to explore the effects of AT-I on nicotine-induced macrophage pyroptosis and the progression of atherosclerosis. <b>Methods:</b> RT-qPCR and Western blot were used to detect the mRNA and protein levels of TXNIP and pyroptosis-related factors in THP-1-derived macrophages. ELISA was used to detect the secretion of pro-inflammatory cytokines. Hoechst/PI double-staining assay was used to assess plasma membrane integrity. The ROS assay kit, LDH release assay kit, and caspase-1 activity assay kit were used to detect ROS production, LDH release, and caspase-1 activity. Oil Red O, HE, and Masson staining were used to evaluate lipid accumulation, lesion size, and plaque stability in HFD-fed apoE<sup>−/−</sup> mice. <b>Results:</b> AT-I treatment significantly decreased pyroptosis-related factors expression, disrupted plasma membrane integrity, and down-regulated pro-inflammatory cytokines secretion, thereby inhibiting nicotine-induced pyroptosis of THP-1-derived macrophages. In addition, AT-I decreased ROS production and the expression of TLR4 and TXNIP. Lentivirus overexpression of TLR4 or TXNIP, or pre-treatment with ROS agonist, mainly reversed the anti-pyroptotic effects of AT-I in nicotine-treated THP-1-derived macrophages. Additionally, administering AT-I to HFD-fed apoE<sup>−/−</sup> mice markedly decreased nicotine-induced up-regulation of pyroptosis-related proteins in the aortas. Enzymatic methods and ELISA assay suggested that AT-I improved dyslipidemia and inflammation in vivo. Oil Red O, HE, and Masson staining showed that AT-I alleviated lipid accumulation, decreased plaque size, and increased plaque stability. <b>Conclusions:</b> Taken together, AT-I can be regarded as a potential phytomedicine that protects against macrophage pyroptosis and atherosclerosis triggered by nicotine.https://www.mdpi.com/2218-1989/15/5/329Atractylenolide Inicotinemacrophagepyroptosisatherosclerosis
spellingShingle Huan-Huan Li
Xian Liu
Yu-Ping Wang
Xi Xu
Lin Zhu
Wei Zhang
Kun Ren
Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway
Metabolites
Atractylenolide I
nicotine
macrophage
pyroptosis
atherosclerosis
title Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway
title_full Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway
title_fullStr Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway
title_full_unstemmed Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway
title_short Atractylenolide I Inhibits Nicotine-Induced Macrophage Pyroptosis and Alleviates Atherogenesis by Suppressing the TLR4/ROS/TXNIP/NLRP3 Pathway
title_sort atractylenolide i inhibits nicotine induced macrophage pyroptosis and alleviates atherogenesis by suppressing the tlr4 ros txnip nlrp3 pathway
topic Atractylenolide I
nicotine
macrophage
pyroptosis
atherosclerosis
url https://www.mdpi.com/2218-1989/15/5/329
work_keys_str_mv AT huanhuanli atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway
AT xianliu atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway
AT yupingwang atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway
AT xixu atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway
AT linzhu atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway
AT weizhang atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway
AT kunren atractylenolideiinhibitsnicotineinducedmacrophagepyroptosisandalleviatesatherogenesisbysuppressingthetlr4rostxnipnlrp3pathway