Chen Miao, Zhen Wang, Jian Lin, Ziye Zhu, Jinan Wang, Baoen Chen
Mitochondrial redox homeostasis is fundamental for cellular function, and its dysregulation is associated with various diseases, including cancer. Isocitrate dehydrogenase 2 (IDH2) is a key enzyme that maintains this balance by generating NADPH. However, the mechanisms controlling IDH2 subcellular localization remain incompletely understood. Here, we identify reversible S-acylation as a critical regulator of IDH2 localization. Using chemical reporters, we demonstrate that IDH2 is S-acylated at a conserved cysteine residue, mediated by ZDHHC3 and APT1. Loss of IDH2 S-acylation disrupts its mitochondrial localization by reducing its interaction with the mitochondrial import receptor TOMM20, leading to NADPH deficiency, redox imbalance, and impaired oxidative phosphorylation. Consistently, ZDHHC3 knockout phenocopies IDH2 S-acylation deficiency, impairing its mitochondrial localization and function. Genetic ablation of IDH2 S-acylation suppresses tumor growth in vitro and in vivo. Our work establishes dynamic S-acylation of IDH2 as an essential regulator of mitochondrial redox homeostasis, thereby revealing a potential metabolic vulnerability in cancer.