Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3

Benzo[a]pyrene (BaP), a polycyclic aromatic hydrocarbon and a potent environmental pollutant, has been implicated in the dysregulation of lipid metabolism and metabolic diseases, warranting investigation into its effects on liver functions, particularly regarding fibroblast growth factor 21 (FGF21)...

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Main Authors: Mengdi Zhang, Xiaoli Lv, Chaojie Wang, Lei Wang, Han Wang, Xue Wang, Yulu Du, Jun Li, Xiuli Han, Lei Fan, Yuxia Hu, Tuya Bai, Weizhong Huangfu, Fuhou Chang
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2025.1595566/full
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author Mengdi Zhang
Mengdi Zhang
Xiaoli Lv
Xiaoli Lv
Chaojie Wang
Chaojie Wang
Lei Wang
Lei Wang
Han Wang
Han Wang
Xue Wang
Xue Wang
Yulu Du
Yulu Du
Jun Li
Jun Li
Jun Li
Xiuli Han
Xiuli Han
Xiuli Han
Lei Fan
Lei Fan
Yuxia Hu
Yuxia Hu
Yuxia Hu
Tuya Bai
Tuya Bai
Weizhong Huangfu
Fuhou Chang
Fuhou Chang
author_facet Mengdi Zhang
Mengdi Zhang
Xiaoli Lv
Xiaoli Lv
Chaojie Wang
Chaojie Wang
Lei Wang
Lei Wang
Han Wang
Han Wang
Xue Wang
Xue Wang
Yulu Du
Yulu Du
Jun Li
Jun Li
Jun Li
Xiuli Han
Xiuli Han
Xiuli Han
Lei Fan
Lei Fan
Yuxia Hu
Yuxia Hu
Yuxia Hu
Tuya Bai
Tuya Bai
Weizhong Huangfu
Fuhou Chang
Fuhou Chang
author_sort Mengdi Zhang
collection DOAJ
description Benzo[a]pyrene (BaP), a polycyclic aromatic hydrocarbon and a potent environmental pollutant, has been implicated in the dysregulation of lipid metabolism and metabolic diseases, warranting investigation into its effects on liver functions, particularly regarding fibroblast growth factor 21 (FGF21) mediated pathways. This study aimed to elucidate the effects of BaP on liver lipid metabolism and FGF21 expression via the aryl hydrocarbon receptor (AhR), with a focus on the regulatory interactions between BaP and xenobiotic response elements (XRE) within the promoter region of FGF21. Utilizing HepG2 cells, lipid accumulation was assessed through Oil Red O and Nile Red staining, while the expression of FGF21 protein was quantified by Western blotting and immunofluorescence techniques. Additionally, various truncated plasmids of the FGF21 promoter were synthesized for a dual-luciferase reporter assay to determine the relative luciferase activity and the modulation of FGF21 expression by BaP. The results revealed dose-dependent effects of BaP on lipid metabolism; specifically, low concentrations of BaP upregulated FGF21 expression by enhancing promoter activity in regions containing the XRE1 sequence, whereas higher BaP concentrations downregulated FGF21 expression via inhibition of promoter activity in regions with the XRE3 sequence. In conclusion, low doses of BaP facilitate AhR binding to XRE1, promoting FGF21 expression, while high doses disrupt this interaction through XRE3, culminating in decreased expression levels. These findings suggest a nuanced role of BaP in lipid metabolism regulation, with potential implications for understanding metabolic disorders associated with environmental pollutants. The study elucidates the relationship between AhR and FGF-21, providing an experimental basis for the search of new targets for the prevention and treatment of nonalcoholic fatty liver disease (NAFLD).
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spelling doaj-art-3133146cded445efb8b7ced76f856bde2025-08-20T03:55:48ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122025-07-011610.3389/fphar.2025.15955661595566Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3Mengdi Zhang0Mengdi Zhang1Xiaoli Lv2Xiaoli Lv3Chaojie Wang4Chaojie Wang5Lei Wang6Lei Wang7Han Wang8Han Wang9Xue Wang10Xue Wang11Yulu Du12Yulu Du13Jun Li14Jun Li15Jun Li16Xiuli Han17Xiuli Han18Xiuli Han19Lei Fan20Lei Fan21Yuxia Hu22Yuxia Hu23Yuxia Hu24Tuya Bai25Tuya Bai26Weizhong Huangfu27Fuhou Chang28Fuhou Chang29College of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCenter for New Drug Safety Evaluation and Research, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCenter for New Drug Safety Evaluation and Research, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaCenter for New Drug Safety Evaluation and Research, Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaAffiliated Hospital of Inner Mongolia Medical University, Hohhot, ChinaCollege of Pharmacy, Inner Mongolia Medical University, Hohhot, ChinaInner Mongolia Autonomous Region Engineering Research Center of New Pharmaceutical Screening, Inner Mongolia Medical University, Hohhot, ChinaBenzo[a]pyrene (BaP), a polycyclic aromatic hydrocarbon and a potent environmental pollutant, has been implicated in the dysregulation of lipid metabolism and metabolic diseases, warranting investigation into its effects on liver functions, particularly regarding fibroblast growth factor 21 (FGF21) mediated pathways. This study aimed to elucidate the effects of BaP on liver lipid metabolism and FGF21 expression via the aryl hydrocarbon receptor (AhR), with a focus on the regulatory interactions between BaP and xenobiotic response elements (XRE) within the promoter region of FGF21. Utilizing HepG2 cells, lipid accumulation was assessed through Oil Red O and Nile Red staining, while the expression of FGF21 protein was quantified by Western blotting and immunofluorescence techniques. Additionally, various truncated plasmids of the FGF21 promoter were synthesized for a dual-luciferase reporter assay to determine the relative luciferase activity and the modulation of FGF21 expression by BaP. The results revealed dose-dependent effects of BaP on lipid metabolism; specifically, low concentrations of BaP upregulated FGF21 expression by enhancing promoter activity in regions containing the XRE1 sequence, whereas higher BaP concentrations downregulated FGF21 expression via inhibition of promoter activity in regions with the XRE3 sequence. In conclusion, low doses of BaP facilitate AhR binding to XRE1, promoting FGF21 expression, while high doses disrupt this interaction through XRE3, culminating in decreased expression levels. These findings suggest a nuanced role of BaP in lipid metabolism regulation, with potential implications for understanding metabolic disorders associated with environmental pollutants. The study elucidates the relationship between AhR and FGF-21, providing an experimental basis for the search of new targets for the prevention and treatment of nonalcoholic fatty liver disease (NAFLD).https://www.frontiersin.org/articles/10.3389/fphar.2025.1595566/fullbenzo[a]pyrenfibroblast growth factor 21aryl hydrocarbon receptorxenobiotic response element 1xenobiotic response element 3hepatic lipid metabolism
spellingShingle Mengdi Zhang
Mengdi Zhang
Xiaoli Lv
Xiaoli Lv
Chaojie Wang
Chaojie Wang
Lei Wang
Lei Wang
Han Wang
Han Wang
Xue Wang
Xue Wang
Yulu Du
Yulu Du
Jun Li
Jun Li
Jun Li
Xiuli Han
Xiuli Han
Xiuli Han
Lei Fan
Lei Fan
Yuxia Hu
Yuxia Hu
Yuxia Hu
Tuya Bai
Tuya Bai
Weizhong Huangfu
Fuhou Chang
Fuhou Chang
Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3
Frontiers in Pharmacology
benzo[a]pyren
fibroblast growth factor 21
aryl hydrocarbon receptor
xenobiotic response element 1
xenobiotic response element 3
hepatic lipid metabolism
title Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3
title_full Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3
title_fullStr Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3
title_full_unstemmed Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3
title_short Molecular mechanisms of dose-dependent regulation of hepatic lipid metabolism by BaP through modulation of AhR binding to XRE1 or XRE3
title_sort molecular mechanisms of dose dependent regulation of hepatic lipid metabolism by bap through modulation of ahr binding to xre1 or xre3
topic benzo[a]pyren
fibroblast growth factor 21
aryl hydrocarbon receptor
xenobiotic response element 1
xenobiotic response element 3
hepatic lipid metabolism
url https://www.frontiersin.org/articles/10.3389/fphar.2025.1595566/full
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