Heme deficiency in skeletal muscle exacerbates sarcopenia and impairs autophagy by reducing AMPK signaling

Sci Rep. 2024 Sep 27;14(1):22147. doi: 10.1038/s41598-024-73049-9.

Abstract

Heme serves as a prosthetic group in hemoproteins, including subunits of the mammalian mitochondrial electron transfer chain. The first enzyme in vertebrate heme biosynthesis, 5-aminolevulinic acid synthase 1 (ALAS1), is ubiquitously expressed and essential for producing 5-aminolevulinic acid (ALA). We previously showed that Alas1 heterozygous mice at 20-35 weeks (aged-A1+/-s) manifested impaired glucose metabolism, mitochondrial malformation in skeletal muscle, and reduced exercise tolerance, potentially linked to autophagy dysfunction. In this study, we investigated autophagy in A1+/-s and a sarcopenic phenotype in A1+/-s at 75-95 weeks (senile-A1+/-s). Senile-A1+/-s exhibited significantly reduced body and gastrocnemius muscle weight, and muscle strength, indicating an accelerated sarcopenic phenotype. Decreases in total LC3 and LC3-II protein and Map1lc3a mRNA levels were observed in aged-A1+/-s under fasting conditions and in Alas1 knockdown myocyte-differentiated C2C12 cells (A1KD-C2C12s) cultured in high- or low-glucose medium. ALA treatment largely reversed these declines. Reduced AMP-activated protein kinase (AMPK) signaling was associated with decreased autophagy in aged-A1+/-s and A1KD-C2C12s. AMPK modulation using AICAR (activator) and dorsomorphin (inhibitor) affected LC3 protein levels in an AMPK-dependent manner. Our findings suggest that heme deficiency contributes to accelerated sarcopenia-like defects and reduced autophagy in skeletal muscle, primarily due to decreased AMPK signaling.

Keywords: 5-aminolevulinic acid; 5-aminolevulinic acid synthase 1 (ALAS1); Autophagy; Heme; Sarcopenia; Skeletal muscle.

MeSH terms

  • 5-Aminolevulinate Synthetase / genetics
  • 5-Aminolevulinate Synthetase / metabolism
  • AMP-Activated Protein Kinases* / metabolism
  • Aminoimidazole Carboxamide / analogs & derivatives
  • Aminoimidazole Carboxamide / pharmacology
  • Aminolevulinic Acid / pharmacology
  • Animals
  • Autophagy*
  • Cell Line
  • Glucose / metabolism
  • Heme* / metabolism
  • Male
  • Mice
  • Muscle, Skeletal* / metabolism
  • Muscle, Skeletal* / pathology
  • Ribonucleotides / pharmacology
  • Sarcopenia* / genetics
  • Sarcopenia* / metabolism
  • Sarcopenia* / pathology
  • Signal Transduction*

Substances

  • Heme
  • AMP-Activated Protein Kinases
  • 5-Aminolevulinate Synthetase
  • Aminoimidazole Carboxamide
  • Glucose
  • AICA ribonucleotide
  • Ribonucleotides
  • Aminolevulinic Acid