Yaolu Zhang, Yingying Jiang, Yan Li, Fangfang Wu, Guanqi Chen, Zhongqiu Lu
Diquat (DQ), a widely used bipyridyl herbicide, poses a significant neurotoxic threat through poorly understood mechanisms. This study demonstrated that restoring SLC7A11 expression effectively mitigated DQ-induced neurotoxicity by suppressing ferroptosis and mitochondrial dysfunction. We employed in vivo and in vitro models to elucidate the involvement of ferroptosis and mitochondrial dysfunction in DQ-induced neurotoxicity. DQ exposure resulted in dose-dependent mortality, hippocampal injury, dysregulation of neuroinflammatory and neurotrophic marker expression, and behavioral deficits. In SH-SY5Y cells, DQ markedly reduced cell viability and induced morphological hallmarks of cytotoxicity. Transcriptomic profiling identified 81 differentially expressed genes and revealed ferroptosis as a top enriched pathway, with pronounced downregulation of SLC7A11. Mechanistically, DQ triggered ferroptosis by suppressing the SLC7A11/GSH/GPX4 axis. Lentiviral and AAV-mediated overexpression of SLC7A11 restored GPX4 and FTH1 levels; downregulated TFRC and ACSL4 expression; normalized GSH levels; and decreased reactive oxygen species, MDA, and labile Fe²⁺ levels and lipid peroxidation. It also restored the mitochondrial membrane potential and oxygen consumption rate, suppressed mitochondrial fragmentation, substantially alleviated hippocampal injury, and rescued hippocampus-dependent memory deficits. Furthermore, compared with monotherapy, the combination of SLC7A11 overexpression with the mitochondrial antioxidant mitoquinone mesylate (MitoQ) exhibited enhanced neuroprotective effects, resulting in superior restoration of intracellular ATP levels, mitochondrial dynamics proteins and ferroptotic marker levels. Together, these findings demonstrate that DQ induces neurotoxicity by suppressing the SLC7A11/GSH/GPX4 axis and activating ferroptosis associated with mitochondrial dysfunction. The enhancement of SLC7A11 expression, alone or in combination with mitochondrial antioxidants, has a strong neuroprotective effect, revealing SLC7A11 as a player in and therapeutic target for DQ-related neurotoxicity.