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  3. Mitochondrial dynamics govern whole-body regeneration through stem cell pluripotency and mitonuclear balance

Mitochondrial dynamics govern whole-body regeneration through stem cell pluripotency and mitonuclear balance

  • Nat Commun. 2024 Dec 13;15(1):10681. doi: 10.1038/s41467-024-54720-1.
Xue Pan # 1 2 3 4,  Yun Zhao # 2 3 4 5,  Yucong Li # 2 3 4 5,  Jiajia Chen 1 2 3 4,  Wenya Zhang 2 3 4 5,  Ling Yang 6,  Yuanyi Zhou Xiong 2 3 4 5,  Yuqing Ying 1 2 3 4,  Hao Xu 1 2 3 4,  Yuhong Zhang 2 3 4,  Chong Gao 2 3 4,  Yuhan Sun 2 3,  Nan Li 6,  Liangyi Chen 7 8 9 10,  Zhixing Chen 11 12,  Kai Lei 13 14 15
Affiliations

Affiliations

  • 1 College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China.
  • 2 Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, Zhejiang, China.
  • 3 Key Laboratory of Growth Regulation and Translational Research of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou, Zhejiang, China.
  • 4 Institute of Biology, Westlake Institute for Advanced Study, Hangzhou, Zhejiang, China.
  • 5 Fudan University, Shanghai, China.
  • 6 HPC Center, Westlake University, Hangzhou, Zhejiang, China.
  • 7 College of Future Technology, Institute of Molecular Medicine, Beijing Key Laboratory of Cardiometabolic Molecular Medicine, National Biomedical Imaging Center, Peking University, Beijing, China. lychen@pku.edu.cn.
  • 8 Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China. lychen@pku.edu.cn.
  • 9 State Key Laboratory of Membrane Biology, Peking University, Beijing, China. lychen@pku.edu.cn.
  • 10 PKU-Nanjing Institute of Translational Medicine, Nanjing, China. lychen@pku.edu.cn.
  • 11 College of Future Technology, Institute of Molecular Medicine, Beijing Key Laboratory of Cardiometabolic Molecular Medicine, National Biomedical Imaging Center, Peking University, Beijing, China. zhixingchen@pku.edu.cn.
  • 12 Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China. zhixingchen@pku.edu.cn.
  • 13 Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, Zhejiang, China. leikai@westlake.edu.cn.
  • 14 Key Laboratory of Growth Regulation and Translational Research of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou, Zhejiang, China. leikai@westlake.edu.cn.
  • 15 Institute of Biology, Westlake Institute for Advanced Study, Hangzhou, Zhejiang, China. leikai@westlake.edu.cn.
  • # Contributed equally.
PMID: 39672898 DOI: 10.1038/s41467-024-54720-1
Abstract

Tissue regeneration is a complex process involving large changes in cell proliferation, fate determination, and differentiation. Mitochondrial dynamics and metabolism play a crucial role in development and wound repair, but their function in large-scale regeneration remains poorly understood. Planarians offer an excellent model to investigate this process due to their remarkable regenerative abilities. In this study, we examine mitochondrial dynamics during planarian regeneration. We find that knockdown of the mitochondrial fusion gene, opa1, impairs both tissue regeneration and stem cell pluripotency. Interestingly, the regeneration defects caused by opa1 knockdown are rescued by simultaneous knockdown of the mitochondrial fission gene, drp1, which partially restores mitochondrial dynamics. Furthermore, we discover that Mitolow stem cells exhibit an enrichment of pluripotency due to their fate choices at earlier stages. Transcriptomic analysis reveals the delicate mitonuclear balance in metabolism and mitochondrial proteins in regeneration, controlled by mitochondrial dynamics. These findings highlight the importance of maintaining mitochondrial dynamics in large-scale tissue regeneration and suggest the potential for manipulating these dynamics to enhance stem cell functionality and regenerative processes.

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