Zhibin Zhang, Hechen Shen, Shijie Zhang, Jianghui Zhou, Meng Zhang, Yuchao Wang, Yue Zheng, Yun C. Chang, Xiaoyu Liang, Xiaomin Hu, Wenqing Gao
Myocardial infarction (MI) elicits a robust inflammatory response that exacerbates cardiac injury and impairs functional recovery, making immunomodulation a key strategy for improving post-MI outcomes. We isolated extracellular vesicles (EVs) from normoxic and hypoxia/reoxygenation-treated cardiomyocytes, profiled their microRNA cargo, and examined their effects on LPS-stimulated RAW264.7 macrophages and a murine MI model using gain- and loss-of-function approaches targeting miR-199b-3p and fibrinogen-like protein 2 (Fgl2). Hypoxia/reoxygenation-derived EVs were enriched in intraluminal miR-199b-3p and were efficiently taken up by macrophages; miR-199b-3p directly targeted Fgl2, suppressed TLR4/NF-κB activation, limited M1 polarization, restored phagocytic function, and reduced pro-inflammatory cytokine release. In MI mice, hypoxia/reoxygenation-EVs or a miR-199b-3p agomir decreased cardiac Fgl2 expression, inflammatory cytokine levels, infarct size, and apoptosis, and improved left ventricular function, whereas Fgl2 overexpression largely abrogated these benefits. Cardiomyocyte-derived hypoxia/reoxygenation-EVs deliver miR-199b-3p to restrain Fgl2-dependent inflammatory signaling and post-infarction injury, highlighting the EV/miR-199b-3p/Fgl2 axis as a potential therapeutic target for improving outcomes after MI. • Hypoxia-preconditioned cardiomyocyte EVs protect against myocardial ischemic injury. • EVs reprogram macrophage polarization from pro-inflammatory M1 to reparative M2. • miR-199b-3p inhibits Fgl2-mediated NF-κB activation to suppress cardiac inflammation. • Reveals EV-mediated immunomodulation as a promising therapeutic strategy for MI.