M. Y. Liu, Zhangyi Yu, Zechun He, Zhigao Zhou, Jie Liu, Lanbing Liu, Xin Wu, Jun Li, Yuanru Huang, Lilin Xiang, Xiangjie Kong, Zhibing Lu, Li Wang
Direct reprogramming of fibroblasts into induced cardiomyocytes (iCMs) offers a regenerative strategy for heart repair, but efficiency declines in adult and aged cells. Transcriptomic and epigenetic profiling identified cellular senescence as a major barrier limiting cardiac fibroblast (CF) plasticity and cardiogenic conversion. Postneonatal fibroblasts exhibited impaired activation of cardiac gene programs and persistent expression of fibrotic and inflammatory signatures. A loss-of-function screen identified Nr4a3 as a central repressor. Nr4a3 overexpression promoted senescence and suppressed iCM induction, whereas knockdown enhanced reprogramming in murine and human senescent CFs. Mechanistically, Nr4a3 depletion remodeled the chromatin landscape from a fibrotic and inflammatory state to a regenerative cardiac program. Blocking downstream Cxcl14 restored reprogramming in refractory fibroblasts. In vivo, Nr4a3 knockdown improved heart function following myocardial infarction. These findings established cellular senescence as a major barrier to cardiac reprogramming and identified Nr4a3 and its effectors as potential targets to enhance heart regeneration.