Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury

This study establishes an Adverse Outcome Pathway (AOP) framework to decode pulmonary injury mechanisms induced by E-cigarette constituents, emphasizing the structural properties of propylene glycol (PG), vegetable glycerin (VG), and nicotine in driving oxidative-inflammatory cascades. Computational...

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Main Authors: Yan Chen, Hongqian Jiang, Wei Liu, Zhenguang Du, Zhenyuan Wang, Zhicheng Zhou, Fusheng Chi
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325010486
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author Yan Chen
Hongqian Jiang
Wei Liu
Zhenguang Du
Zhenyuan Wang
Zhicheng Zhou
Fusheng Chi
author_facet Yan Chen
Hongqian Jiang
Wei Liu
Zhenguang Du
Zhenyuan Wang
Zhicheng Zhou
Fusheng Chi
author_sort Yan Chen
collection DOAJ
description This study establishes an Adverse Outcome Pathway (AOP) framework to decode pulmonary injury mechanisms induced by E-cigarette constituents, emphasizing the structural properties of propylene glycol (PG), vegetable glycerin (VG), and nicotine in driving oxidative-inflammatory cascades. Computational toxicogenomics leveraging the Comparative Toxicogenomics Database (CTD) identified 1214 chemical-gene interactions specific to PG/VG pyrolysis byproducts (formaldehyde, acrolein) and nicotine, with 83.7 % overlap with lung injury-associated genes from public repositories. Furthermore, analysis revealed Hippo pathway inhibition in lung tissues harvested from patients with lung cancer attributable to long-term smoking. Similarly, in vitro experiments revealed that exposure of bronchial epithelial cells to E-cigarette components suppressed of Hippo pathway kinases. This suppression induced the nuclear translocation of YAP/TAZ and consequently led to the hypersecretion of pro-inflammatory cytokines, including IL-6 and TNF-α. Moreover, a murine model subjected to chronic E-cigarette aerosol exposure manifested oxidative lung injury and neutrophilic infiltration. These findings collectively imply that E-cigarette exposure can induce lung injury, and upon prolonged exposure, may be associated with an increased risk of cancer development. Quantitative weight-of-evidence (QWOE) modeling delineated the following cascade: 1) PG/VG thermal degradation generates reactive carbonyls (KE1: oxidative stress), 2) nicotine synergistically amplifies inflammation (KE2: chronic inflammation), and 3) Hippo/YAP axis suppression (KE3) drives genomic instability via impaired DNA repair fidelity. This AOP framework establishes a predictive paradigm linking structural properties of nicotine delivery systems to signaling perturbations, advancing toxicity assessment for next-generation tobacco products.
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spelling doaj-art-65e476c71ca2427fb413135ec30dd6532025-08-20T03:41:53ZengElsevierEcotoxicology and Environmental Safety0147-65132025-09-0130211870310.1016/j.ecoenv.2025.118703Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injuryYan Chen0Hongqian Jiang1Wei Liu2Zhenguang Du3Zhenyuan Wang4Zhicheng Zhou5Fusheng Chi6The People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaThe People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaThe People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaThe People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaThe People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaCorresponding authors.; The People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaCorresponding authors.; The People’s Hospital of Liaoning Province Postgraduate Training Base, Jinzhou Medical University, Shenyang 110000, ChinaThis study establishes an Adverse Outcome Pathway (AOP) framework to decode pulmonary injury mechanisms induced by E-cigarette constituents, emphasizing the structural properties of propylene glycol (PG), vegetable glycerin (VG), and nicotine in driving oxidative-inflammatory cascades. Computational toxicogenomics leveraging the Comparative Toxicogenomics Database (CTD) identified 1214 chemical-gene interactions specific to PG/VG pyrolysis byproducts (formaldehyde, acrolein) and nicotine, with 83.7 % overlap with lung injury-associated genes from public repositories. Furthermore, analysis revealed Hippo pathway inhibition in lung tissues harvested from patients with lung cancer attributable to long-term smoking. Similarly, in vitro experiments revealed that exposure of bronchial epithelial cells to E-cigarette components suppressed of Hippo pathway kinases. This suppression induced the nuclear translocation of YAP/TAZ and consequently led to the hypersecretion of pro-inflammatory cytokines, including IL-6 and TNF-α. Moreover, a murine model subjected to chronic E-cigarette aerosol exposure manifested oxidative lung injury and neutrophilic infiltration. These findings collectively imply that E-cigarette exposure can induce lung injury, and upon prolonged exposure, may be associated with an increased risk of cancer development. Quantitative weight-of-evidence (QWOE) modeling delineated the following cascade: 1) PG/VG thermal degradation generates reactive carbonyls (KE1: oxidative stress), 2) nicotine synergistically amplifies inflammation (KE2: chronic inflammation), and 3) Hippo/YAP axis suppression (KE3) drives genomic instability via impaired DNA repair fidelity. This AOP framework establishes a predictive paradigm linking structural properties of nicotine delivery systems to signaling perturbations, advancing toxicity assessment for next-generation tobacco products.http://www.sciencedirect.com/science/article/pii/S0147651325010486Electronic cigaretteLung injuryHippo Signaling PathwayAdverse outcome pathwayPopulation disease risk prediction
spellingShingle Yan Chen
Hongqian Jiang
Wei Liu
Zhenguang Du
Zhenyuan Wang
Zhicheng Zhou
Fusheng Chi
Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury
Ecotoxicology and Environmental Safety
Electronic cigarette
Lung injury
Hippo Signaling Pathway
Adverse outcome pathway
Population disease risk prediction
title Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury
title_full Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury
title_fullStr Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury
title_full_unstemmed Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury
title_short Adverse outcome pathway (AOP) framework for predicting toxic mechanisms in E-cigarette-induced lung injury
title_sort adverse outcome pathway aop framework for predicting toxic mechanisms in e cigarette induced lung injury
topic Electronic cigarette
Lung injury
Hippo Signaling Pathway
Adverse outcome pathway
Population disease risk prediction
url http://www.sciencedirect.com/science/article/pii/S0147651325010486
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