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Zebrafish caudal fin amputation induces a metabolic switch necessary for cell identity transitions and cell cycle re-entry to support blastema formation and bone regeneration

Ana S. Brandão, Jorge Borbinha, View ORCID ProfileTelmo Pereira, Patrícia H. Brito, Raquel Lourenço, Anabela Bensimon-Brito, View ORCID ProfileAntónio Jacinto
doi: https://doi.org/10.1101/2022.01.26.477895
Ana S. Brandão
1CEDOC, NOVA Medical School, NOVA University of Lisbon, Campo Mártires da Pátria 130, Lisboa 1169-056, Portugal
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  • For correspondence: ana.brandao@nms.unl.pt antonio.jacinto@nms.unl.pt
Jorge Borbinha
1CEDOC, NOVA Medical School, NOVA University of Lisbon, Campo Mártires da Pátria 130, Lisboa 1169-056, Portugal
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Telmo Pereira
1CEDOC, NOVA Medical School, NOVA University of Lisbon, Campo Mártires da Pátria 130, Lisboa 1169-056, Portugal
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  • ORCID record for Telmo Pereira
Patrícia H. Brito
2UCIBIO, Dept. Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade NOVA de Lisboa, 2819-516 Caparica, Portugal
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Raquel Lourenço
1CEDOC, NOVA Medical School, NOVA University of Lisbon, Campo Mártires da Pátria 130, Lisboa 1169-056, Portugal
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Anabela Bensimon-Brito
3INSERM, ATIP-Avenir, Aix Marseille Univ, Marseille Medical Genetics, Marseille, France
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António Jacinto
1CEDOC, NOVA Medical School, NOVA University of Lisbon, Campo Mártires da Pátria 130, Lisboa 1169-056, Portugal
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  • ORCID record for António Jacinto
  • For correspondence: ana.brandao@nms.unl.pt antonio.jacinto@nms.unl.pt
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Abstract

Regeneration depends on the ability of mature cells at the injury site to respond to injury, generating tissue-specific progenitors that incorporate the blastema and proliferate to reconstitute the original organ architecture. The metabolic microenvironment has been tightly connected to cell function and identity during development and tumorigenesis. Yet, the link between metabolism and cell identity at the mechanistic level in a regenerative context remains unclear. The adult zebrafish caudal fin, and bone cells specifically, have been crucial for the understanding of mature cell contribution to tissue regeneration. Here, we use this model to explore the relevance of glucose metabolism for the cell fate transitions preceding new osteoblast formation and blastema assembly. We show that injury triggers a shift in the metabolic profile at early stages of regeneration, enhancing glycolysis at the expense of mitochondrial oxidation. This metabolic switch mediates transcriptional changes that make mature osteoblast amenable to be reprogramed into pre-osteoblasts and induces cell cycle re-entry and progression. Manipulation of the metabolic profile led to severe reduction of the pre-osteoblast pool, diminishing their capacity to generate new osteoblasts, and to a complete abrogation of blastema formation. Overall, our data indicate that metabolic alterations have a powerful instructive role in regulating genetic programs that dictate fate decisions and stimulate proliferation, thereby providing a deeper understanding on the mechanisms regulating blastema formation and bone regeneration.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 27, 2022.
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Zebrafish caudal fin amputation induces a metabolic switch necessary for cell identity transitions and cell cycle re-entry to support blastema formation and bone regeneration
Ana S. Brandão, Jorge Borbinha, Telmo Pereira, Patrícia H. Brito, Raquel Lourenço, Anabela Bensimon-Brito, António Jacinto
bioRxiv 2022.01.26.477895; doi: https://doi.org/10.1101/2022.01.26.477895
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Zebrafish caudal fin amputation induces a metabolic switch necessary for cell identity transitions and cell cycle re-entry to support blastema formation and bone regeneration
Ana S. Brandão, Jorge Borbinha, Telmo Pereira, Patrícia H. Brito, Raquel Lourenço, Anabela Bensimon-Brito, António Jacinto
bioRxiv 2022.01.26.477895; doi: https://doi.org/10.1101/2022.01.26.477895

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