ATF3 induction prevents precocious activation of skeletal muscle stem cell by regulating H2B expression

Suyang Zhang, Feng Yang, Yile Huang, Liangqiang He, Yuying Li, Yi Ching Esther Wan, Yingzhe Ding, Kui Ming Chan, Ting Xie, Hao Sun () and Huating Wang ()
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Suyang Zhang: Chinese University of Hong Kong
Feng Yang: Chinese University of Hong Kong
Yile Huang: Chinese University of Hong Kong
Liangqiang He: Hong Kong Science Park, New Territories
Yuying Li: Chinese University of Hong Kong
Yi Ching Esther Wan: City University of Hong Kong
Yingzhe Ding: Chinese University of Hong Kong
Kui Ming Chan: City University of Hong Kong
Ting Xie: The Hong Kong University of Science and Technology
Hao Sun: Chinese University of Hong Kong
Huating Wang: Chinese University of Hong Kong

Nature Communications, 2023, vol. 14, issue 1, 1-21

Abstract: Abstract Skeletal muscle stem cells (also called satellite cells, SCs) are important for maintaining muscle tissue homeostasis and damage-induced regeneration. However, it remains poorly understood how SCs enter cell cycle to become activated upon injury. Here we report that AP-1 family member ATF3 (Activating Transcription Factor 3) prevents SC premature activation. Atf3 is rapidly and transiently induced in SCs upon activation. Short-term deletion of Atf3 in SCs accelerates acute injury-induced regeneration, however, its long-term deletion exhausts the SC pool and thus impairs muscle regeneration. The Atf3 loss also provokes SC activation during voluntary exercise and enhances the activation during endurance exercise. Mechanistically, ATF3 directly activates the transcription of Histone 2B genes, whose reduction accelerates nucleosome displacement and gene transcription required for SC activation. Finally, the ATF3-dependent H2B expression also prevents genome instability and replicative senescence in SCs. Therefore, this study has revealed a previously unknown mechanism for preserving the SC population by actively suppressing precocious activation, in which ATF3 is a key regulator.

Date: 2023
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DOI: 10.1038/s41467-023-40465-w

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