Mitochondrial function in skeletal myofibers is controlled by a TRF2-SIRT3 axis over lifetime

Aging Cell. 2020 Mar;19(3):e13097. doi: 10.1111/acel.13097. Epub 2020 Jan 28.

Abstract

Telomere shortening follows a developmentally regulated process that leads to replicative senescence of dividing cells. However, whether telomere changes are involved in postmitotic cell function and aging remains elusive. In this study, we discovered that the level of the TRF2 protein, a key telomere-capping protein, declines in human skeletal muscle over lifetime. In cultured human myotubes, TRF2 downregulation did not trigger telomere dysfunction, but suppressed expression of the mitochondrial Sirtuin 3 gene (SIRT3) leading to mitochondrial respiration dysfunction and increased levels of reactive oxygen species. Importantly, restoring the Sirt3 level in TRF2-compromised myotubes fully rescued mitochondrial functions. Finally, targeted ablation of the Terf2 gene in mouse skeletal muscle leads to mitochondrial dysfunction and sirt3 downregulation similarly to those of TRF2-compromised human myotubes. Altogether, these results reveal a TRF2-SIRT3 axis controlling muscle mitochondrial function. We propose that this axis connects developmentally regulated telomere changes to muscle redox metabolism.

Keywords: aging; mitochondria; postmitotic cells; skeletal muscle; telomeres.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aging / metabolism*
  • Animals
  • Cells, Cultured
  • Down-Regulation / genetics
  • Female
  • Gene Knockdown Techniques
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Mitochondria / metabolism*
  • Muscle Fibers, Skeletal / metabolism*
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / genetics
  • Sirtuin 3 / metabolism*
  • Telomere / metabolism
  • Telomere Shortening / genetics*
  • Telomeric Repeat Binding Protein 2 / genetics
  • Telomeric Repeat Binding Protein 2 / metabolism*
  • Young Adult

Substances

  • Reactive Oxygen Species
  • Sirt3 protein, mouse
  • TERF2 protein, human
  • TRF2 protein, mouse
  • Telomeric Repeat Binding Protein 2
  • SIRT3 protein, human
  • Sirtuin 3