Gli1 marks a sentinel muscle stem cell population for muscle regeneration

Jiayin Peng, Lili Han, Biao Liu, Jiawen Song, Yuang Wang, Kunpeng Wang, Qian Guo, XinYan Liu, Yu Li, Jujin Zhang, Wenqing Wu, Sheng Li, Xin Fu, Cheng-le Zhuang, Weikang Zhang, Shengbao Suo, Ping Hu () and Yun Zhao ()
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Jiayin Peng: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Lili Han: University of Chinese Academy of Sciences
Biao Liu: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Jiawen Song: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Yuang Wang: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Kunpeng Wang: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Qian Guo: University of Chinese Academy of Sciences
XinYan Liu: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Yu Li: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Jujin Zhang: University of Chinese Academy of Sciences
Wenqing Wu: Chinese Academy of Sciences, University of Chinese Academy of Sciences
Sheng Li: Xinhua Hospital affiliated to Shanghai Jiao Tong University School of Medicine
Xin Fu: Xinhua Hospital affiliated to Shanghai Jiao Tong University School of Medicine
Cheng-le Zhuang: The 10th People’s Hospital affiliated to Tongji University
Weikang Zhang: Guangzhou Laboratory-Guangzhou Medical University
Shengbao Suo: Guangzhou Laboratory-Guangzhou Medical University
Ping Hu: Xinhua Hospital affiliated to Shanghai Jiao Tong University School of Medicine
Yun Zhao: Chinese Academy of Sciences, University of Chinese Academy of Sciences

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract Adult skeletal muscle regeneration is mainly driven by muscle stem cells (MuSCs), which are highly heterogeneous. Although recent studies have started to characterize the heterogeneity of MuSCs, whether a subset of cells with distinct exists within MuSCs remains unanswered. Here, we find that a population of MuSCs, marked by Gli1 expression, is required for muscle regeneration. The Gli1+ MuSC population displays advantages in proliferation and differentiation both in vitro and in vivo. Depletion of this population leads to delayed muscle regeneration, while transplanted Gli1+ MuSCs support muscle regeneration more effectively than Gli1− MuSCs. Further analysis reveals that even in the uninjured muscle, Gli1+ MuSCs have elevated mTOR signaling activity, increased cell size and mitochondrial numbers compared to Gli1− MuSCs, indicating Gli1+ MuSCs are displaying the features of primed MuSCs. Moreover, Gli1+ MuSCs greatly contribute to the formation of GAlert cells after muscle injury. Collectively, our findings demonstrate that Gli1+ MuSCs represents a distinct MuSC population which is more active in the homeostatic muscle and enters the cell cycle shortly after injury. This population functions as the tissue-resident sentinel that rapidly responds to injury and initiates muscle regeneration.

Date: 2023
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DOI: 10.1038/s41467-023-42837-8

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