Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway

Ethnopharmacological relevanceCelastrol, a bioactive compound from Tripterygium wilfordii Hook.f., is known for its anti-inflammatory and immunomodulatory effects, but its immunotoxicity is underexplored. This study investigates the mechanisms of celastrol-induced immunotoxicity, focusing on the PI3...

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Main Authors: Shaohui Geng, Jingqi Wen, Chunli Shen, Li Liu, Yijin Jiang, Jingyuan Fu, Yiwei Guan, Zi Ye, Yuanhao Wu, Chen Li, Guangrui Huang
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2025.1567193/full
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author Shaohui Geng
Jingqi Wen
Chunli Shen
Li Liu
Yijin Jiang
Jingyuan Fu
Yiwei Guan
Zi Ye
Yuanhao Wu
Chen Li
Guangrui Huang
author_facet Shaohui Geng
Jingqi Wen
Chunli Shen
Li Liu
Yijin Jiang
Jingyuan Fu
Yiwei Guan
Zi Ye
Yuanhao Wu
Chen Li
Guangrui Huang
author_sort Shaohui Geng
collection DOAJ
description Ethnopharmacological relevanceCelastrol, a bioactive compound from Tripterygium wilfordii Hook.f., is known for its anti-inflammatory and immunomodulatory effects, but its immunotoxicity is underexplored. This study investigates the mechanisms of celastrol-induced immunotoxicity, focusing on the PI3K-Akt signaling pathway, a key regulator of immune function.Materials and methodsAn integrative approach combining network toxicology, molecular docking, and experimental biology identified molecular targets in celastrol-induced immune dysfunction. Network toxicology mapped key pathways, and molecular docking predicted interactions with immune-related proteins. High-dose celastrol (10 mg/kg) was administered to C57BL/6J mice, followed by a histopathological analysis of the thymus and spleen. RNA-Seq evaluated gene expression in immune pathways, and IHC/mIHC validated PI3K-Akt signaling pathway protein expression.ResultsNetwork toxicology identified the PI3K-Akt signaling pathway as a key target of celastrol’s immunotoxic effects. High-dose celastrol caused histopathological damage in the thymus and spleen, including lymphocyte depletion and immune cell infiltration. RNA-Seq showed upregulation of critical genes in the PI3K-Akt signaling pathway (Egfr, Pik3c, Akt3), linked to cell proliferation and survival. IHC confirmed increased expression of EGFR, AKT, PIK3, and mTOR, with decreased PTEN. mIHC revealed elevated macrophage activation and inflammation. In contrast, low-dose celastrol suppressed PI3K-Akt signaling by downregulating mTOR, indicating dose-dependent modulation of immune function.ConclusionOur study demonstrates the dose-dependent immunotoxic effects of celastrol, which is toxic in high doses caused by activation of the PI3K-Akt signaling pathway, while low doses offer protection by blocking this signaling pathway. These findings emphasize the importance of dose selection in therapeutic and safety contexts, enhancing understanding of celastrol’s biological effects and its clinical potential in immune-related diseases.
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spelling doaj-art-e6cf904c8d02426b918b17990a41195d2025-08-20T01:57:15ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122025-05-011610.3389/fphar.2025.15671931567193Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathwayShaohui Geng0Jingqi Wen1Chunli Shen2Li Liu3Yijin Jiang4Jingyuan Fu5Yiwei Guan6Zi Ye7Yuanhao Wu8Chen Li9Guangrui Huang10School of Life Science, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Traditional Chinese Medicine, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Acupuncture, Moxibustion and Tuina, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Life Science, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Chinese Pharmacy, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Chinese Pharmacy, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Chinese Pharmacy, Beijing University of Chinese Medicine, Beijing, ChinaSchool of Chinese Pharmacy, Beijing University of Chinese Medicine, Beijing, ChinaThe First Affiliated Hospital of Tianjin University of Traditional Chinese Medicine, Tianjin, ChinaDepartment of Dermatology, Tianjin Institute of Integrative Dermatology, Tianjin Academy of Traditional Chinese Medicine Affiliated Hospital, Tianjin, ChinaSchool of Life Science, Beijing University of Chinese Medicine, Beijing, ChinaEthnopharmacological relevanceCelastrol, a bioactive compound from Tripterygium wilfordii Hook.f., is known for its anti-inflammatory and immunomodulatory effects, but its immunotoxicity is underexplored. This study investigates the mechanisms of celastrol-induced immunotoxicity, focusing on the PI3K-Akt signaling pathway, a key regulator of immune function.Materials and methodsAn integrative approach combining network toxicology, molecular docking, and experimental biology identified molecular targets in celastrol-induced immune dysfunction. Network toxicology mapped key pathways, and molecular docking predicted interactions with immune-related proteins. High-dose celastrol (10 mg/kg) was administered to C57BL/6J mice, followed by a histopathological analysis of the thymus and spleen. RNA-Seq evaluated gene expression in immune pathways, and IHC/mIHC validated PI3K-Akt signaling pathway protein expression.ResultsNetwork toxicology identified the PI3K-Akt signaling pathway as a key target of celastrol’s immunotoxic effects. High-dose celastrol caused histopathological damage in the thymus and spleen, including lymphocyte depletion and immune cell infiltration. RNA-Seq showed upregulation of critical genes in the PI3K-Akt signaling pathway (Egfr, Pik3c, Akt3), linked to cell proliferation and survival. IHC confirmed increased expression of EGFR, AKT, PIK3, and mTOR, with decreased PTEN. mIHC revealed elevated macrophage activation and inflammation. In contrast, low-dose celastrol suppressed PI3K-Akt signaling by downregulating mTOR, indicating dose-dependent modulation of immune function.ConclusionOur study demonstrates the dose-dependent immunotoxic effects of celastrol, which is toxic in high doses caused by activation of the PI3K-Akt signaling pathway, while low doses offer protection by blocking this signaling pathway. These findings emphasize the importance of dose selection in therapeutic and safety contexts, enhancing understanding of celastrol’s biological effects and its clinical potential in immune-related diseases.https://www.frontiersin.org/articles/10.3389/fphar.2025.1567193/fullcelastrolimmunotoxicityPI3K-Akt signaling pathwaynetwork toxicologymolecular docking
spellingShingle Shaohui Geng
Jingqi Wen
Chunli Shen
Li Liu
Yijin Jiang
Jingyuan Fu
Yiwei Guan
Zi Ye
Yuanhao Wu
Chen Li
Guangrui Huang
Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway
Frontiers in Pharmacology
celastrol
immunotoxicity
PI3K-Akt signaling pathway
network toxicology
molecular docking
title Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway
title_full Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway
title_fullStr Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway
title_full_unstemmed Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway
title_short Dose-dependent immunotoxic mechanisms of celastrol via modulation of the PI3K-Akt signaling pathway
title_sort dose dependent immunotoxic mechanisms of celastrol via modulation of the pi3k akt signaling pathway
topic celastrol
immunotoxicity
PI3K-Akt signaling pathway
network toxicology
molecular docking
url https://www.frontiersin.org/articles/10.3389/fphar.2025.1567193/full
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