ALKBH5-mediated m6A modification of IL-11 drives macrophage-to-myofibroblast transition and pathological cardiac fibrosis in mice

ALKBH5-mediated m6A modification of IL-11 drives macrophage-to-myofibroblast transition and pathological cardiac fibrosis in mice

05 March 2024 | Tao Zhuang, Mei-Hua Chen, Ruo-Xi Wu, Jing Wang, Xi-De Hu, Ting Meng, Ai-Hua Wu, Yan Li, Yong-Feng Yang, Yu Lei, Dong-Hua Hu, Yan-Xiu Li, Li Zhang, Ai-Jun Sun, Wei Lu, Guan-Nan Zhang, Jun-Li Zuo & Cheng-Chao Ruan
Cardiac macrophages contribute to cardiac fibrosis, but the factors regulating their transition and activation during this process remain unclear. This study shows that cardiac macrophages derived from circulating monocytes preferentially commit to macrophage-to-myofibroblast transition (MMT) under angiotensin II (Ang II)-induced hypertension, with increased expression of the RNA N6-methyladenosine demethylase ALKBH5. Macrophage-specific knockout of ALKBH5 inhibits Ang II-induced MMT and ameliorates cardiac fibrosis and dysfunction. Mechanistically, ALKBH5 mediates m6A demethylation of IL-11 mRNA, increasing its stability and protein levels. Overexpression of IL-11 in macrophages reverses the phenotype in ALKBH5-deficient mice. Targeted delivery of ALKBH5 or IL-11 receptor α (IL11RA1) siRNA to monocytes/macrophages attenuates MMT and cardiac fibrosis under hypertensive stress. These results suggest that the ALKBH5/IL-11/IL11RA1/MMT axis alters cardiac macrophage function and contributes to hypertensive cardiac fibrosis and dysfunction in mice, identifying potential targets for cardiac fibrosis therapy. The study demonstrates that cardiac macrophages from circulating monocytes may trans-differentiate into myofibroblasts under hypertensive conditions for fibrosis development, with an ALKBH5/IL-11 molecular axis modulating this transition. The findings highlight the role of ALKBH5 in regulating MMT through m6A modification of IL-11 mRNA, and the potential of targeting this pathway for therapeutic intervention in cardiac fibrosis.Cardiac macrophages contribute to cardiac fibrosis, but the factors regulating their transition and activation during this process remain unclear. This study shows that cardiac macrophages derived from circulating monocytes preferentially commit to macrophage-to-myofibroblast transition (MMT) under angiotensin II (Ang II)-induced hypertension, with increased expression of the RNA N6-methyladenosine demethylase ALKBH5. Macrophage-specific knockout of ALKBH5 inhibits Ang II-induced MMT and ameliorates cardiac fibrosis and dysfunction. Mechanistically, ALKBH5 mediates m6A demethylation of IL-11 mRNA, increasing its stability and protein levels. Overexpression of IL-11 in macrophages reverses the phenotype in ALKBH5-deficient mice. Targeted delivery of ALKBH5 or IL-11 receptor α (IL11RA1) siRNA to monocytes/macrophages attenuates MMT and cardiac fibrosis under hypertensive stress. These results suggest that the ALKBH5/IL-11/IL11RA1/MMT axis alters cardiac macrophage function and contributes to hypertensive cardiac fibrosis and dysfunction in mice, identifying potential targets for cardiac fibrosis therapy. The study demonstrates that cardiac macrophages from circulating monocytes may trans-differentiate into myofibroblasts under hypertensive conditions for fibrosis development, with an ALKBH5/IL-11 molecular axis modulating this transition. The findings highlight the role of ALKBH5 in regulating MMT through m6A modification of IL-11 mRNA, and the potential of targeting this pathway for therapeutic intervention in cardiac fibrosis.
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Understanding ALKBH5-mediated m6A modification of IL-11 drives macrophage-to-myofibroblast transition and pathological cardiac fibrosis in mice