Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling

Introduction: High palmitic acid (PA) levels trigger metainflammation, facilitating the onset and progression of chronic metabolic diseases. Recently, exosomes were identified as new inflammation mediators. However, the mechanism by which macrophage exosomes mediate PA-induced inflammation remains u...

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Main Authors: Huiyu Luo, Jiexian Wang, Fengjuan Lin, Yuguo Liu, Xinglong Wu, Gan Li, Chuhong Su, Junbin Chen, Fei Xiong, Jiaqi Mo, Zhongdaixi Zheng, Xiangyi Zheng, Qing Li, Longying Zha
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Language:English
Published: Elsevier 2025-05-01
Series:Journal of Advanced Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S2090123224002613
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author Huiyu Luo
Jiexian Wang
Fengjuan Lin
Yuguo Liu
Xinglong Wu
Gan Li
Chuhong Su
Junbin Chen
Fei Xiong
Jiaqi Mo
Zhongdaixi Zheng
Xiangyi Zheng
Qing Li
Longying Zha
author_facet Huiyu Luo
Jiexian Wang
Fengjuan Lin
Yuguo Liu
Xinglong Wu
Gan Li
Chuhong Su
Junbin Chen
Fei Xiong
Jiaqi Mo
Zhongdaixi Zheng
Xiangyi Zheng
Qing Li
Longying Zha
author_sort Huiyu Luo
collection DOAJ
description Introduction: High palmitic acid (PA) levels trigger metainflammation, facilitating the onset and progression of chronic metabolic diseases. Recently, exosomes were identified as new inflammation mediators. However, the mechanism by which macrophage exosomes mediate PA-induced inflammation remains unclear. Objectives: To explore how PA induces metainflammation through macrophage exosomes. Methods: Exosomes secreted by RAW264.7 mouse macrophages stimulated with PA (ExosPA) or not (Exos) were prepared by ultracentrifugation. The differential miRNAs between ExosPA and Exos were identified by high-throughput sequencing, and their targeted mRNAs and proteins were bioinformatically analyzed and verified by qPCR and western blot. Mouse macrophages and metabolic cells (AML-12 hepatocytes, C2C12 myocytes or 3T3-L1 adipocytes) were treated with ExosPA or Exos. The verified miRNAs and its targeted molecules related to inflammation were analyzed in recipient cells. Furthers, exosomes were prepared from primary peritoneal macrophages isolated from AIN93G diet-fed (Control PM-Exos) or HPD-fed (PA PM-Exos) mice. Control or PA PM-Exos were then tail vein injected (30 μg) into mice (n = 10), once a week for 2 weeks. The verified miRNA and its targets in blood, blood exosomes, and metabolic tissues were detected. Finally, measured the levels of miRNA, inflammatory factors, and fatty acids in the blood of 20 obese/overweight individuals and 20 healthy individuals. Results: ExoPA activate NF-κB signaling and enhance inflammatory enzyme/cytokine production in macrophages and metabolic cells. ExoPA enrich miR-3064-5p and target to inhibit IκBα as verified by exosome inhibitors and miR-3064-5p mimics and inhibitors. HPD elevates exosomal miR-3064-5p, macrophage exosomal miR-3064-5p, and inflammatory cytokine levels in mice circulation. PA PM-Exos from HPD-fed mice triggered inflammation in the circulation and metabolic tissues/organs of chow diet-fed mice. Overweight/obese individuals exhibit increased levels of circulating palmitoleic acid, exosomal miR-3064-5p, and high-sensitivity C-reactive proteins. Conclusions: Macrophage exosomes transferring miR-3064-5p to target IκBα and activate NF-κB signaling in metabolic cells is a mechanism of PA-induced metainflammation.
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spelling doaj-art-520ee4f4f466438fbdf411e468cc7a252025-08-20T02:19:47ZengElsevierJournal of Advanced Research2090-12322025-05-017150151910.1016/j.jare.2024.06.024Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signalingHuiyu Luo0Jiexian Wang1Fengjuan Lin2Yuguo Liu3Xinglong Wu4Gan Li5Chuhong Su6Junbin Chen7Fei Xiong8Jiaqi Mo9Zhongdaixi Zheng10Xiangyi Zheng11Qing Li12Longying Zha13Department of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR China; Department of Clinical Nutrition, The First People’s Hospital of Chenzhou, Hengyang Medical School, University of South China, 423000 Chenzhou, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR China; Department of Clinical Nutrition, Zhujiang Hospital, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Health Management Medicine, Guangzhou Panyu District Health Management Center (Guangzhou Panyu District Rehabilitation Hospital), Guangzhou 511450, Guangdong, PR ChinaDepartment of Clinical Nutrition, Nanfang Hospital, Southern Medical University, Guangzhou 510515, Guangdong, PR ChinaDepartment of Nutrition and Food Hygiene, Guangdong Provincial Key Laboratory of Tropical Disease Research, National Medical Products Administration (NMPA) Key Laboratory for Safety Evaluation of Cosmetics, School of Public Health, Southern Medical University, Guangzhou 510515, Guangdong, PR China; Corresponding author at: Department of Nutrition and Food Hygiene, School of Public Health, Southern Medical University, 1838 Guangzhou Avenue North, Guangzhou 510515, Guangdong, PR China.Introduction: High palmitic acid (PA) levels trigger metainflammation, facilitating the onset and progression of chronic metabolic diseases. Recently, exosomes were identified as new inflammation mediators. However, the mechanism by which macrophage exosomes mediate PA-induced inflammation remains unclear. Objectives: To explore how PA induces metainflammation through macrophage exosomes. Methods: Exosomes secreted by RAW264.7 mouse macrophages stimulated with PA (ExosPA) or not (Exos) were prepared by ultracentrifugation. The differential miRNAs between ExosPA and Exos were identified by high-throughput sequencing, and their targeted mRNAs and proteins were bioinformatically analyzed and verified by qPCR and western blot. Mouse macrophages and metabolic cells (AML-12 hepatocytes, C2C12 myocytes or 3T3-L1 adipocytes) were treated with ExosPA or Exos. The verified miRNAs and its targeted molecules related to inflammation were analyzed in recipient cells. Furthers, exosomes were prepared from primary peritoneal macrophages isolated from AIN93G diet-fed (Control PM-Exos) or HPD-fed (PA PM-Exos) mice. Control or PA PM-Exos were then tail vein injected (30 μg) into mice (n = 10), once a week for 2 weeks. The verified miRNA and its targets in blood, blood exosomes, and metabolic tissues were detected. Finally, measured the levels of miRNA, inflammatory factors, and fatty acids in the blood of 20 obese/overweight individuals and 20 healthy individuals. Results: ExoPA activate NF-κB signaling and enhance inflammatory enzyme/cytokine production in macrophages and metabolic cells. ExoPA enrich miR-3064-5p and target to inhibit IκBα as verified by exosome inhibitors and miR-3064-5p mimics and inhibitors. HPD elevates exosomal miR-3064-5p, macrophage exosomal miR-3064-5p, and inflammatory cytokine levels in mice circulation. PA PM-Exos from HPD-fed mice triggered inflammation in the circulation and metabolic tissues/organs of chow diet-fed mice. Overweight/obese individuals exhibit increased levels of circulating palmitoleic acid, exosomal miR-3064-5p, and high-sensitivity C-reactive proteins. Conclusions: Macrophage exosomes transferring miR-3064-5p to target IκBα and activate NF-κB signaling in metabolic cells is a mechanism of PA-induced metainflammation.http://www.sciencedirect.com/science/article/pii/S2090123224002613ExosomesMacrophageMetainflammationIκBαNF-κB
spellingShingle Huiyu Luo
Jiexian Wang
Fengjuan Lin
Yuguo Liu
Xinglong Wu
Gan Li
Chuhong Su
Junbin Chen
Fei Xiong
Jiaqi Mo
Zhongdaixi Zheng
Xiangyi Zheng
Qing Li
Longying Zha
Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling
Journal of Advanced Research
Exosomes
Macrophage
Metainflammation
IκBα
NF-κB
title Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling
title_full Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling
title_fullStr Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling
title_full_unstemmed Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling
title_short Macrophage exosomes mediate palmitic acid-induced metainflammation by transferring miR-3064-5p to target IκBα and activate NF-κB signaling
title_sort macrophage exosomes mediate palmitic acid induced metainflammation by transferring mir 3064 5p to target iκbα and activate nf κb signaling
topic Exosomes
Macrophage
Metainflammation
IκBα
NF-κB
url http://www.sciencedirect.com/science/article/pii/S2090123224002613
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