The mitochondrial citrate carrier SLC25A1 regulates metabolic reprogramming and morphogenesis in the developing heart

Commun Biol. 2024 Oct 31;7(1):1422. doi: 10.1038/s42003-024-07110-8.

Abstract

The developing mammalian heart undergoes an important metabolic shift from glycolysis towards mitochondrial oxidation that is critical to support the increasing energetic demands of the maturing heart. Here, we describe a new mechanistic link between mitochondria and cardiac morphogenesis, uncovered by studying mitochondrial citrate carrier (SLC25A1) knockout mice. Slc25a1 null embryos displayed impaired growth, mitochondrial dysfunction and cardiac malformations that recapitulate the congenital heart defects observed in 22q11.2 deletion syndrome, a microdeletion disorder involving the SLC25A1 locus. Importantly, Slc25a1 heterozygous embryos, while overtly indistinguishable from wild type, exhibited an increased frequency of these defects, suggesting Slc25a1 haploinsuffiency and dose-dependent effects. Mechanistically, SLC25A1 may link mitochondria to transcriptional regulation of metabolism through epigenetic control of gene expression to promote metabolic remodeling in the developing heart. Collectively, this work positions SLC25A1 as a novel mitochondrial regulator of cardiac morphogenesis and metabolic maturation, and suggests a role in congenital heart disease.

MeSH terms

  • Animals
  • Anion Transport Proteins / genetics
  • Anion Transport Proteins / metabolism
  • Carrier Proteins
  • Female
  • Gene Expression Regulation, Developmental
  • Heart Defects, Congenital / genetics
  • Heart Defects, Congenital / metabolism
  • Heart* / embryology
  • Heart* / growth & development
  • Metabolic Reprogramming
  • Mice
  • Mice, Knockout*
  • Mitochondria / metabolism
  • Mitochondria, Heart / genetics
  • Mitochondria, Heart / metabolism
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Morphogenesis* / genetics

Substances

  • citrate-binding transport protein
  • Anion Transport Proteins
  • Mitochondrial Proteins
  • Carrier Proteins