Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation

Abstract Background Microglia-evoked neuroinflammation contributes to neurodegenerative diseases such as multiple sclerosis (MS). Metabolic reprogramming, including changes in polyunsaturated fatty acids (PUFAs), plays a critical role in MS pathophysiology. Previous studies identified reduced plasma...

Full description

Saved in:
Bibliographic Details
Main Authors: Xiao-Xi Zhu, Pei-Juan Wang, Shan Chao, Wei-Jia Tang, Long-You Zhao, Li-Mei Yu, Fan Yang
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Journal of Translational Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12967-025-06296-7
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849762143022350336
author Xiao-Xi Zhu
Pei-Juan Wang
Shan Chao
Wei-Jia Tang
Long-You Zhao
Li-Mei Yu
Fan Yang
author_facet Xiao-Xi Zhu
Pei-Juan Wang
Shan Chao
Wei-Jia Tang
Long-You Zhao
Li-Mei Yu
Fan Yang
author_sort Xiao-Xi Zhu
collection DOAJ
description Abstract Background Microglia-evoked neuroinflammation contributes to neurodegenerative diseases such as multiple sclerosis (MS). Metabolic reprogramming, including changes in polyunsaturated fatty acids (PUFAs), plays a critical role in MS pathophysiology. Previous studies identified reduced plasma α-dimorphecolic acid (α-DIPA), a linoleic acid derivative, in MS patients. This study investigated the anti-inflammatory effects of α-DIPA on microglia and the underlying pathways. Methods Lipopolysaccharide (LPS)-induced BV-2 microglial inflammation was used as an in vitro model. α-DIPA effects were assessed via ELISA for nitric oxide (NO) release, flow cytometry was used to examine cell proliferation, activation and polarization, and transcriptomic analysis was applied to identify key signaling pathways regulated by α-DIPA. Results ELISA results showed that exogenous α-DIPA treatment significantly inhibited LPS-induced NO release from BV-2 cells in a concentration-dependent manner. Moreover, flow cytometry analysis suggested that 40 µM α-DIPA treatment significantly repressed LPS-induced BV-2 cell proliferation, activation, as well as M1 and M2 type polarization. Furthermore, transcriptome analysis revealed that exogenous α-DIPA extensively and drastically decreased the transcriptional level of numerous genes that are involved in the regulation of inflammatory responses, for instance, proinflammatory genes such as Tnf and Ccl3 related to IL-17 and TNF-α signaling. In addition, we also observed that the expression of multiple genes in NF-κB signaling were also inhibited greatly by α-DIPA, such as Nfkb2 and Nfkbia. Notably, α-DIPA robustly suppressed LPS-induced mRNA expression of abundant genes participating in the ferroptosis pathway, including Acsl4, Slc7a11, Me1, and Hmox1. Interestingly, the expressions of multiple ferroptosis-related genes were regulated specifically by α-DIPA but not LPS, such as Acsl5, Acsl6, Alox5, Cars, Dpp3, Dpp10, Slc2a5, and Slc7a1. Conclusion α-DIPA inhibits microglial inflammation likely through regulating the pathways of the ferroptosis and NF-κB signaling. These results provided preliminary evidence for α-DIPA as a potential therapeutic candidate for neurodegenerative diseases like MS.
format Article
id doaj-art-ea459da0ffb2419a9c6e175a1af4b959
institution DOAJ
issn 1479-5876
language English
publishDate 2025-03-01
publisher BMC
record_format Article
series Journal of Translational Medicine
spelling doaj-art-ea459da0ffb2419a9c6e175a1af4b9592025-08-20T03:05:49ZengBMCJournal of Translational Medicine1479-58762025-03-0123112110.1186/s12967-025-06296-7Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammationXiao-Xi Zhu0Pei-Juan Wang1Shan Chao2Wei-Jia Tang3Long-You Zhao4Li-Mei Yu5Fan Yang6Key Laboratory of Cell Engineering in Guizhou Province, Affiliated Hospital of Zunyi Medical UniversityDepartment of Psychiatry, Nantong Fourth People’s HospitalResearch Center for Lin He Academician New Medicine, Institutes for Shanghai Pudong Decoding LifeResearch Center for Lin He Academician New Medicine, Institutes for Shanghai Pudong Decoding LifeLishui Key Laboratory of Brain Health and Severe Brain Disorders. Lishui Second People’s HospitalKey Laboratory of Cell Engineering in Guizhou Province, Affiliated Hospital of Zunyi Medical UniversityLishui Key Laboratory of Brain Health and Severe Brain Disorders. Lishui Second People’s HospitalAbstract Background Microglia-evoked neuroinflammation contributes to neurodegenerative diseases such as multiple sclerosis (MS). Metabolic reprogramming, including changes in polyunsaturated fatty acids (PUFAs), plays a critical role in MS pathophysiology. Previous studies identified reduced plasma α-dimorphecolic acid (α-DIPA), a linoleic acid derivative, in MS patients. This study investigated the anti-inflammatory effects of α-DIPA on microglia and the underlying pathways. Methods Lipopolysaccharide (LPS)-induced BV-2 microglial inflammation was used as an in vitro model. α-DIPA effects were assessed via ELISA for nitric oxide (NO) release, flow cytometry was used to examine cell proliferation, activation and polarization, and transcriptomic analysis was applied to identify key signaling pathways regulated by α-DIPA. Results ELISA results showed that exogenous α-DIPA treatment significantly inhibited LPS-induced NO release from BV-2 cells in a concentration-dependent manner. Moreover, flow cytometry analysis suggested that 40 µM α-DIPA treatment significantly repressed LPS-induced BV-2 cell proliferation, activation, as well as M1 and M2 type polarization. Furthermore, transcriptome analysis revealed that exogenous α-DIPA extensively and drastically decreased the transcriptional level of numerous genes that are involved in the regulation of inflammatory responses, for instance, proinflammatory genes such as Tnf and Ccl3 related to IL-17 and TNF-α signaling. In addition, we also observed that the expression of multiple genes in NF-κB signaling were also inhibited greatly by α-DIPA, such as Nfkb2 and Nfkbia. Notably, α-DIPA robustly suppressed LPS-induced mRNA expression of abundant genes participating in the ferroptosis pathway, including Acsl4, Slc7a11, Me1, and Hmox1. Interestingly, the expressions of multiple ferroptosis-related genes were regulated specifically by α-DIPA but not LPS, such as Acsl5, Acsl6, Alox5, Cars, Dpp3, Dpp10, Slc2a5, and Slc7a1. Conclusion α-DIPA inhibits microglial inflammation likely through regulating the pathways of the ferroptosis and NF-κB signaling. These results provided preliminary evidence for α-DIPA as a potential therapeutic candidate for neurodegenerative diseases like MS.https://doi.org/10.1186/s12967-025-06296-7FerroptosisNF-κB signalingα-dimorphecolic acidMicroglial inflammationMultiple sclerosisMetabolomics
spellingShingle Xiao-Xi Zhu
Pei-Juan Wang
Shan Chao
Wei-Jia Tang
Long-You Zhao
Li-Mei Yu
Fan Yang
Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation
Journal of Translational Medicine
Ferroptosis
NF-κB signaling
α-dimorphecolic acid
Microglial inflammation
Multiple sclerosis
Metabolomics
title Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation
title_full Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation
title_fullStr Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation
title_full_unstemmed Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation
title_short Transcriptomic profiling identifies ferroptosis and NF-κB signaling involved in α-dimorphecolic acid regulation of microglial inflammation
title_sort transcriptomic profiling identifies ferroptosis and nf κb signaling involved in α dimorphecolic acid regulation of microglial inflammation
topic Ferroptosis
NF-κB signaling
α-dimorphecolic acid
Microglial inflammation
Multiple sclerosis
Metabolomics
url https://doi.org/10.1186/s12967-025-06296-7
work_keys_str_mv AT xiaoxizhu transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation
AT peijuanwang transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation
AT shanchao transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation
AT weijiatang transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation
AT longyouzhao transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation
AT limeiyu transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation
AT fanyang transcriptomicprofilingidentifiesferroptosisandnfkbsignalinginvolvedinadimorphecolicacidregulationofmicroglialinflammation