Restoration of CPEB4 prevents muscle stem cell senescence during aging

Age-associated impairments in adult stem cell functions correlate with a decline in somatic tissue regeneration capacity. However, the mechanisms underlying the molecular regulation of adult stem cell aging remain elusive. Here, we provide a proteomic analysis of physiologically aged murine muscle s...

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Published inDevelopmental cell Vol. 58; no. 15; pp. 1383 - 1398.e6
Main Authors Zeng, Wenshu, Zhang, Wenxin, Tse, Erin H Y, Liu, Jing, Dong, Anqi, Lam, Kim S W, Luan, Shaoyuan, Kung, Wai Hing, Chan, Tsz Ching, Cheung, Tom H
Format Journal Article
LanguageEnglish
Published United States 07.08.2023
Subjects
Aged
Aging - physiology
Animals
Cellular Senescence
Humans
Mice
Muscle, Skeletal - physiology
Muscles
Proteome
Proteomics
RNA-Binding Proteins
senescence
quiescence
aging
muscle stem cells
CPEB4
mitochondrial metabolism
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Abstract Age-associated impairments in adult stem cell functions correlate with a decline in somatic tissue regeneration capacity. However, the mechanisms underlying the molecular regulation of adult stem cell aging remain elusive. Here, we provide a proteomic analysis of physiologically aged murine muscle stem cells (MuSCs), illustrating a pre-senescent proteomic signature. During aging, the mitochondrial proteome and activity are impaired in MuSCs. In addition, the inhibition of mitochondrial function results in cellular senescence. We identified an RNA-binding protein, CPEB4, downregulated in various aged tissues, which is required for MuSC functions. CPEB4 regulates the mitochondrial proteome and activity through mitochondrial translational control. MuSCs devoid of CPEB4 induced cellular senescence. Importantly, restoring CPEB4 expression rescued impaired mitochondrial metabolism, improved geriatric MuSC functions, and prevented cellular senescence in various human cell lines. Our findings provide the basis for the possibility that CPEB4 regulates mitochondrial metabolism to govern cellular senescence, with an implication of therapeutic intervention for age-related senescence.
AbstractList Age-associated impairments in adult stem cell functions correlate with a decline in somatic tissue regeneration capacity. However, the mechanisms underlying the molecular regulation of adult stem cell aging remain elusive. Here, we provide a proteomic analysis of physiologically aged murine muscle stem cells (MuSCs), illustrating a pre-senescent proteomic signature. During aging, the mitochondrial proteome and activity are impaired in MuSCs. In addition, the inhibition of mitochondrial function results in cellular senescence. We identified an RNA-binding protein, CPEB4, downregulated in various aged tissues, which is required for MuSC functions. CPEB4 regulates the mitochondrial proteome and activity through mitochondrial translational control. MuSCs devoid of CPEB4 induced cellular senescence. Importantly, restoring CPEB4 expression rescued impaired mitochondrial metabolism, improved geriatric MuSC functions, and prevented cellular senescence in various human cell lines. Our findings provide the basis for the possibility that CPEB4 regulates mitochondrial metabolism to govern cellular senescence, with an implication of therapeutic intervention for age-related senescence.
Author Zeng, Wenshu
Zhang, Wenxin
Liu, Jing
Dong, Anqi
Kung, Wai Hing
Luan, Shaoyuan
Tse, Erin H Y
Cheung, Tom H
Chan, Tsz Ching
Lam, Kim S W
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  givenname: Shaoyuan
  surname: Luan
  fullname: Luan, Shaoyuan
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  givenname: Wai Hing
  surname: Kung
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  givenname: Tsz Ching
  surname: Chan
  fullname: Chan, Tsz Ching
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  givenname: Tom H
  surname: Cheung
  fullname: Cheung, Tom H
  email: tcheung@ust.hk
  organization: Division of Life Science, Center for Stem Cell Research, HKUST-Nan Fung Life Sciences Joint Laboratory, State Key Laboratory of Molecular Neuroscience, Molecular Neuroscience Center, The Hong Kong University of Science and Technology, Hong Kong, China; Hong Kong Center for Neurodegenerative Diseases, Hong Kong, China; Guangdong Provincial Key Laboratory of Brain Science, Disease and Drug Development, Shenzhen-Hong Kong Institute of Brain Science, HKUST Shenzhen Research Institute, Shenzhen, China. Electronic address: tcheung@ust.hk
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Keywords senescence
quiescence
aging
muscle stem cells
CPEB4
mitochondrial metabolism
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Snippet Age-associated impairments in adult stem cell functions correlate with a decline in somatic tissue regeneration capacity. However, the mechanisms underlying...
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SubjectTerms Aged
Aging - physiology
Animals
Cellular Senescence
Humans
Mice
Muscle, Skeletal - physiology
Muscles
Proteome
Proteomics
RNA-Binding Proteins
Title Restoration of CPEB4 prevents muscle stem cell senescence during aging
URI https://www.ncbi.nlm.nih.gov/pubmed/37321216
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