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

Xue Pan, Yun Zhao, Yucong Li, Jiajia Chen, Wenya Zhang, Ling Yang, Yuanyi Zhou Xiong, Yuqing Ying, Hao Xu, Yuhong Zhang, Chong Gao, Yuhan Sun, Nan Li, Liangyi Chen (), Zhixing Chen () and Kai Lei ()
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Xue Pan: Zhejiang University
Yun Zhao: Westlake Laboratory of Life Sciences and Biomedicine
Yucong Li: Westlake Laboratory of Life Sciences and Biomedicine
Jiajia Chen: Zhejiang University
Wenya Zhang: Westlake Laboratory of Life Sciences and Biomedicine
Ling Yang: Westlake University
Yuanyi Zhou Xiong: Westlake Laboratory of Life Sciences and Biomedicine
Yuqing Ying: Zhejiang University
Hao Xu: Zhejiang University
Yuhong Zhang: Westlake Laboratory of Life Sciences and Biomedicine
Chong Gao: Westlake Laboratory of Life Sciences and Biomedicine
Yuhan Sun: Westlake Laboratory of Life Sciences and Biomedicine
Nan Li: Westlake University
Liangyi Chen: Peking University
Zhixing Chen: Peking University
Kai Lei: Westlake Laboratory of Life Sciences and Biomedicine

Nature Communications, 2024, vol. 15, issue 1, 1-22

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-54720-1

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