Oxidative phosphorylation is required for cardiomyocyte re-differentiation and long-term fish heart regeneration

  • Konstantinos Lekkos
  • , Zhilian Hu
  • , Phong D Nguyen
  • , Hessel Honkoop
  • , Esra Sengul
  • , Rita Alonaizan
  • , Jana Koth
  • , Jun Ying
  • , Madeleine E Lemieux
  • , Alisha Kenward
  • , Sean Keeley
  • , Bastiaan Spanjaard
  • , Brett W C Kennedy
  • , Xin Sun
  • , Katherine Banecki
  • , Helen G Potts
  • , Gennaro Ruggiero
  • , James Montgomery
  • , Daniela Panáková
  • , Jan Philipp Junker
  • Lisa C Heather, Xiaonan Wang, Juan Manuel Gonzalez-Rosa, Jeroen Bakkers, Mathilda T M Mommersteeg*
*Corresponding author for this work

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Abstract

In contrast to humans, fish can fully regenerate their hearts after cardiac injury. However, not all fish have the same regenerative potential, allowing comparative inter-species and intra-species analysis to identify the mechanisms controlling successful heart regeneration. Here we report a differential regenerative response to cardiac cryo-injury among different wild-type zebrafish strains. Correlating these data with single-cell and bulk RNA sequencing data, we identify oxidative phosphorylation (OXPHOS) as a positive regulator of long-term regenerative outcome. OXPHOS levels, driven by glycolysis through the malate-aspartate shuttle, increase as soon as cardiomyocyte proliferation decreases, and this increase is required for cardiomyocyte re-differentiation and successful long-term regeneration. Reduced upregulation of OXPHOS in Astyanax mexicanus cavefish results in the absence of a dynamic temporal sarcomere gene expression program during cardiomyocyte re-differentiation. These findings challenge the assumption that OXPHOS inhibits regeneration and reveal targetable pathways to enhance heart repair in humans after myocardial infarction.

Original languageEnglish
Pages (from-to)1363-1380
Number of pages18
JournalNature Cardiovascular Research
Volume4
Issue number10
Early online date1 Oct 2025
DOIs
Publication statusPublished - Oct 2025

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