The BAF53A-BACH1-GCLM axis regulates glutathione metabolism and enhances ferroptosis resistance in esophageal squamous cell carcinoma

BAF53A-BACH1-GCLM轴调节谷胱甘肽代谢并增强食管鳞状细胞癌的铁死亡抵抗力

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Abstract

OBJECTIVE: Esophageal squamous cell carcinoma (ESCC), a highly lethal malignancy, exhibits poor survival rates and limited treatment options. Ferroptosis, a regulated form of cell death driven by lipid peroxidation, emerges as a potential therapeutic target. However, the mechanisms suppressing ferroptosis in ESCC remain poorly understood. METHODS: Short hairpin RNA (shRNA) was employed to knock down BAF53A and BACH1 in ESCC cell lines, followed by assessments of cell proliferation, colony formation, and ferroptosis sensitivity. Glutathione (GSH) metabolism was evaluated by measuring GSH/GSSG and NADP(+)/NADPH ratios, reactive oxygen species (ROS) levels, and lipid peroxidation through flow cytometry and fluorescence imaging. Molecular interactions were evaluated using co-immunoprecipitation and chromatin immunoprecipitation sequencing (ChIP-seq) to identify transcriptional targets of the BAF53A-BACH1 complex. RESULTS: BAF53A was elevated in ESCC, and its depletion impaired cell proliferation and colony formation ability of cells. Knockdown of BAF53A disrupted GSH metabolism, leading to increased ROS levels, reduced GSH/GSSG and NADP(+)/NADPH ratios, and enhanced ferroptosis sensitivity. Mechanistically, BAF53A collaborated with BACH1 to transcriptionally activate glutamate-cysteine ligase modifier subunit (GCLM), a key enzyme in GSH biosynthesis. Overexpression of GCLM restored redox balance and cell viability in BAF53A- or BACH1-silenced cells. CONCLUSIONS: The BAF53A-BACH1-GCLM axis constitutes a novel egulatory pathway that integrates chromatin remodeling, transcriptional regulatione, and ferroptosis resistance in ESCC. Targeting this axis may offer a promising approach to exploit metabolic vulnerabilities and enhance ferroptosis sensitivity in ESCC treatment.

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