Guangzhen Lu, Xiaoting Wang, Xinye Wang, Hong Zhuang, Xin Zhou, Gang Zhao
Nanoplastics are widespread environmental contaminants encountered through ingestion and inhalation, raising concerns about their cardiovascular toxicity. How polystyrene nanoplastics (PS-NPs) disrupt cardiomyocyte iron homeostasis remains unclear. We hypothesized that reduced NLR family member X1 (NLRX1) links PS-NP exposure to stimulator of interferon genes (STING) signaling and nuclear receptor coactivator 4 (NCOA4)-associated iron dysregulation. We examined primary neonatal mouse ventricular cardiomyocytes and an 8-week oral-exposure mouse model. In both models, PS-NPs reduced NLRX1 and glutathione peroxidase 4 (GPX4) protein levels, increased STING phosphorylation and acyl-CoA synthetase long-chain family member 4 (ACSL4) expression, and promoted iron accumulation and lipid peroxidation. Cell viability declined, and mice developed cardiac dysfunction and fibrosis. In cardiomyocytes, NLRX1 mRNA remained unchanged. Bafilomycin A1 attenuated NLRX1 protein loss, while NLRX1 showed greater spatial association with lysosome-associated membrane protein 1 (LAMP1)-positive compartments. NLRX1 overexpression reduced STING phosphorylation, iron accumulation, and lipid peroxidation. STING silencing decreased NCOA4 and increased ferritin heavy chain 1, whereas NCOA4 silencing attenuated GPX4 downregulation and ACSL4 upregulation. Re-expression experiments supported the functional ordering of NLRX1, STING, and NCOA4. Ferrostatin-1 (Fer-1) co-treatment attenuated iron accumulation, lipid peroxidation, and GPX4/ACSL4 changes in both models. It improved cardiomyocyte viability and attenuated cardiac dysfunction and fibrosis, although the myocardial phosphorylated-to-total STING ratio remained above control levels. These findings support ferroptosis-associated cardiac injury following PS-NP exposure, with cellular evidence implicating lysosome-associated NLRX1 protein loss and a downstream STING-NCOA4 response.