Xingwang Zhao, Mengjie Zhang, Jun Yin, Jingyi Liao, Denghui Li, Zhiqiang Tian, Yi You, Longlong Zhang, Bing Ni
The M1-to-M2 macrophage phenotypic switch is critical for resolving inflammation and restoring homeostasis in hypoxic lung injury, but the underlying molecular mechanisms are unclear. Here, we show that hypoxia-induced histone lactylation (Kla) upregulates FTO via HIF1a-P300 interaction; lactylation-driven FTO then promotes late-stage M2 polarization by stabilizing Arg1 mRNA through the m6A-YTHDF2 axis. Mechanistically, HIF1a/YY1 liquid-liquid phase separation (LLPS) regulates macrophage glycolysis and oxidative phosphorylation (OXPHOS) via the cGAS-STING pathway downstream of lactylation. Importantly, lactylation exerts context-dependent dual effects: physiological lactylation in wild-type mice facilitates M2 polarization, maintains metabolic balance, and promotes lung repair, whereas excessive lactylation in IL-10-deficient mice disrupts the FTO-Arg1 cascade, perturbs metabolism, blocks M2 polarization, and aggravates injury. Collectively, histone lactylation is a core switch governing macrophage polarization and metabolic homeostasis in hypoxic lung injury, with its function dictated by IL-10 status and lactylation abundance.