Elevated FGF21 secretion, PGC-1α and ketogenic enzyme expression are hallmarks of iron-sulfur cluster depletion in human skeletal muscle

Hum Mol Genet. 2014 Jan 1;23(1):24-39. doi: 10.1093/hmg/ddt393. Epub 2013 Aug 13.

Abstract

Iron-sulfur (Fe-S) clusters are ancient enzyme cofactors found in virtually all life forms. We evaluated the physiological effects of chronic Fe-S cluster deficiency in human skeletal muscle, a tissue that relies heavily on Fe-S cluster-mediated aerobic energy metabolism. Despite greatly decreased oxidative capacity, muscle tissue from patients deficient in the Fe-S cluster scaffold protein ISCU showed a predominance of type I oxidative muscle fibers and higher capillary density, enhanced expression of transcriptional co-activator PGC-1α and increased mitochondrial fatty acid oxidation genes. These Fe-S cluster-deficient muscles showed a dramatic up-regulation of the ketogenic enzyme HMGCS2 and the secreted protein FGF21 (fibroblast growth factor 21). Enhanced muscle FGF21 expression was reflected by elevated circulating FGF21 levels in the patients, and robust FGF21 secretion could be recapitulated by respiratory chain inhibition in cultured myotubes. Our findings reveal that mitochondrial energy starvation elicits a coordinated response in Fe-S-deficient skeletal muscle that is reflected systemically by increased plasma FGF21 levels.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Acidosis, Lactic / congenital*
  • Acidosis, Lactic / genetics
  • Acidosis, Lactic / metabolism
  • Acidosis, Lactic / pathology
  • Adult
  • Aged
  • Case-Control Studies
  • Cells, Cultured
  • Energy Metabolism
  • Female
  • Fibroblast Growth Factors / genetics
  • Fibroblast Growth Factors / metabolism*
  • Gene Expression Regulation
  • Humans
  • Hydroxymethylglutaryl-CoA Synthase / genetics
  • Hydroxymethylglutaryl-CoA Synthase / metabolism*
  • Iron-Sulfur Proteins / genetics
  • Iron-Sulfur Proteins / metabolism*
  • Male
  • Middle Aged
  • Mitochondria, Muscle / metabolism
  • Mitochondria, Muscle / pathology
  • Muscle, Skeletal / metabolism*
  • Muscular Diseases / congenital*
  • Muscular Diseases / genetics
  • Muscular Diseases / metabolism
  • Muscular Diseases / pathology
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • ISCU protein, human
  • Iron-Sulfur Proteins
  • PPARGC1A protein, human
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Transcription Factors
  • fibroblast growth factor 21
  • Fibroblast Growth Factors
  • Hydroxymethylglutaryl-CoA Synthase

Supplementary concepts

  • Myopathy with Lactic Acidosis, Hereditary