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Here, we show that highly malignant osteosarcoma (OS) cells respond to ferroptotic stress by secreting EVs enriched with Alpha\u2010enolase (ENO1). These EVs\u2010ENO1 not only bolster the antioxidant capacity of tumor cells but also confer widespread ferroptosis resistance to macrophages and neutrophils, fostering an immunosuppressive niche. To disrupt this metabolic defense, we developed an OS\u2010targeting lipid nanoparticle (LNP) system for the synergistic delivery of BAP1 mRNA and ENO1 siRNA. We demonstrate that this dual\u2010delivery platform enhances ferroptosis through two complementary regulatory pathways, BAP1\/SLC7A11 and ENO1\/GPX4, leading to potent lipid peroxidation and tumor cell death. In syngeneic orthotopic and lung metastasis models, these targeted LNPs significantly suppress tumor progression and catalyze anti\u2010tumor immunity by activating M1\u2010type macrophages and cytotoxic T cells. 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