Li Yang, Li Chuhan, Sun Qiang, Liu Xingyuan, Chen Fengyuan, Cheung Yeelo, Zhao Yu, Xie Ting, Chazaud Bénédicte, Sun Hao, Wang Huating
Department of Orthopaedics and Traumatology, Li Ka Shing Institute of Health Sciences, Chinese University of Hong Kong, Hong Kong SAR, China.
Center for Neuromusculoskeletal Restorative Medicine Limited, Hong Kong Science Park, Hong Kong SAR, China.
Nat Commun. 2025 Feb 3;16(1):1324. doi: 10.1038/s41467-025-56474-w.
Adult skeletal muscle stem cells (MuSCs) are indispensable for muscle regeneration and tightly regulated by macrophages (MPs) and fibro-adipogenic progenitors (FAPs) in their niche. Deregulated MuSC/MP/FAP interactions and the ensuing inflammation and fibrosis are hallmarks of dystrophic muscle. Here we demonstrate intrinsic deletion of transcription factor Yin Yang 1 (YY1) in MuSCs exacerbates dystrophic pathologies by altering composition and heterogeneity of MPs and FAPs. Further analysis reveals YY1 loss induces expression of immune genes in MuSCs, including C-C motif chemokine ligand 5 (Ccl5). Augmented CCL5 secretion promotes MP recruitment via CCL5/C-C chemokine receptor 5 (CCR5) crosstalk, which subsequently hinders FAP clearance through elevated Transforming growth factor-β1 (TGFβ1). Maraviroc-mediated pharmacological blockade of the CCL5/CCR5 axis effectively mitigates muscle dystrophy and improves muscle performance. Lastly, we demonstrate YY1 represses Ccl5 transcription by binding to its enhancer thus facilitating promoter-enhancer looping. Altogether, our study demonstrates the critical role of MuSCs in actively shaping their niche and provides novel insight into the therapeutic intervention of muscle dystrophy.
成体骨骼肌干细胞(MuSCs)对于肌肉再生不可或缺,并且在其生态位中受到巨噬细胞(MPs)和成纤维脂肪生成祖细胞(FAPs)的严格调控。MuSC/MP/FAP相互作用失调以及随之而来的炎症和纤维化是营养不良性肌肉的标志。在这里,我们证明MuSCs中转录因子阴阳1(YY1)的内在缺失通过改变MPs和FAPs的组成和异质性加剧了营养不良性病理。进一步分析表明,YY1缺失诱导MuSCs中免疫基因的表达,包括C-C基序趋化因子配体5(Ccl5)。增强的CCL5分泌通过CCL5/C-C趋化因子受体5(CCR5)串扰促进MP募集,随后通过升高的转化生长因子-β1(TGFβ1)阻碍FAP清除。马拉维若介导的CCL5/CCR5轴的药理学阻断有效减轻肌肉营养不良并改善肌肉性能。最后,我们证明YY1通过与其增强子结合来抑制Ccl5转录,从而促进启动子-增强子环化。总之,我们的研究证明了MuSCs在积极塑造其生态位中的关键作用,并为肌肉营养不良的治疗干预提供了新的见解。