Zhaorong Yue, Qinghong Liu, Yanni Wang, Ruyue Wang, Zhongqing Li, Manjie Xu, Piao Luo, Jiaxuan Li, Jiawen Xu, Wenjun Xu, Weizhong Zhang, Jianing He, Jiayi Chen, Shahab Uddin, Yang Li, Xin Wang, Hongyu Li
Realgar (As4S4) has long been used in traditional medicine, yet its clinical application remains limited due to poor bioavailability and toxicity. Realgar transforming solution (RTS), a bioleached product generated through microbial transformation of realgar, exhibits enhanced anti-tumor activity; however, its underlying mechanism remains unclear. This study investigated whether ferroptosis contributes to the anti-leukemic effects of RTS in NB4 cells, focusing on iron homeostasis and the solute carrier family 7 member 11 (SLC7A11)/glutathione peroxidase 4 (GPX4) antioxidant axis. NB4 cells were treated with RTS, arsenic trioxide (ATO), or realgar, and cell viability was assessed by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay. Transcriptomic profiling, biochemical assays, fluorescence probes, flow cytometry, and Western blotting were employed to evaluate ferroptosis-related changes. RTS inhibited NB4 cell viability more effectively than ATO or realgar at comparable arsenic concentrations. Transcriptomic analysis indicated significant enrichment of ferroptosis-related pathways. RTS decreased glutathione and superoxide dismutase levels, increased malondialdehyde accumulation and lipid peroxidation, disrupted mitochondrial membrane potential, and elevated intracellular total iron and mitochondrial Fe2+ levels. Additionally, RTS downregulated SLC7A11 and GPX4 and altered the expression of iron metabolism-related proteins, including transferrin receptor protein 1, nuclear receptor coactivator 4, ferritin heavy chain 1, ferroportin 1, iron-responsive element-binding protein 2, and heme oxygenase 1. Moreover, ferrostatin-1 and deferoxamine mesylate partially rescued RTS-induced cytotoxicity and alleviated oxidative damage and iron overload. These results indicate that RTS induces ferroptosis-associated cell death in NB4 cells by disrupting iron homeostasis and inhibiting the SLC7A11/GPX4 axis, supporting further investigation of RTS as a modernized arsenic-based anti-leukemic formulation.