Molecular mechanisms of inhalable iron-containing particles driving lung carcinogenesis through the LCN2 signaling axis revealed by transcriptomic analysis

转录组分析揭示了吸入性含铁颗粒通过LCN2信号通路驱动肺癌发生的分子机制

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Abstract

BACKGROUND: Iron, an essential trace element ubiquitously present in living organisms, is integral to various biological processes. Epidemiological studies have shown an elevated relative risk of lung cancer among male individuals with occupational exposure to high iron environments (such as those working near iron and steel production facilities). This suggests that respirable iron-containing particulate matters (RICPMs) may pose a potential carcinogenic risk; nevertheless, the underlying mechanisms remain poorly understood. The objective of this study is to explore the potential carcinogenic mechanisms of RICPM through integrative bioinformatics analyses combined with experimental validation. METHODS: Sequencing data of a welding fume-exposed mouse model (GSE34056) were downloaded from the Gene Expression Omnibus (GEO) database. Ferroptosis-related genes were retrieved from The Cancer Genome Atlas-lung adenocarcinoma (TCGA-LUAD), Molecular Signatures Database (MSIGDB), and GeneCards® Human Gene Database (GENECARDS) databases. Key genes were screened and analyzed for expression profiles, single-gene pan-cancer relevance, single-gene Gene Set Enrichment Analysis (GSEA), and drug sensitivity. Experimental validations included measurements of reactive oxygen species (ROS), lipocalin-2 (LCN2) expression, ferroptosis-associated antioxidant genes [glutathione peroxidase 4 (GPX4), ferritin heavy chain 1 (FTH1)], and mitochondrial ultrastructure changes via transmission electron microscopy (TEM). RESULTS: Nano-Fe(2)O(3) particles induced overexpression of LCN2 in bronchial epithelial cells, adenovirus 12-SV40 2B immortalized (BEAS-2B) cells, a phenomenon observed across multiple cancer types. The results indicate that RICPM may contribute to lung carcinogenesis through ROS-mediated chemical carcinogenesis pathway, upregulation of ferroptosis resistance mechanisms (e.g., GPX4 and FTH1 overexpression), inhibition of ferroptosis, and mitochondrial damage leading to impaired electron transport chain (ETC). Correlation analyses revealed significant associations between LCN2 and various pro-inflammatory cytokines. Drug sensitivity analyses suggested that high LCN2 expression may be linked to increased resistance to anticancer agents. CONCLUSIONS: The findings elucidate the potential carcinogenic pathways of RICPM and underscore LCN2 as a key mediator, which offer fresh perspectives on the pathogenesis of lung cancer in individuals exposed to high-iron environments and identify prospective therapeutic targets for the prevention and treatment of lung cancer.

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