Effect of rapamycin on mitochondria and lysosomes in fibroblasts from patients with mtDNA mutations

Am J Physiol Cell Physiol. 2021 Jul 1;321(1):C176-C186. doi: 10.1152/ajpcell.00471.2020. Epub 2021 Jun 9.

Abstract

Maintaining mitochondrial function and dynamics is crucial for cellular health. In muscle, defects in mitochondria result in severe myopathies where accumulation of damaged mitochondria causes deterioration and dysfunction. Importantly, understanding the role of mitochondria in disease is a necessity to determine future therapeutics. One of the most common myopathies is mitochondrial encephalopathy lactic acidosis stroke-like episodes (MELAS), which has no current treatment. Recently, patients with MELAS treated with rapamycin exhibited improved clinical outcomes. However, the cellular mechanisms of rapamycin effects in patients with MELAS are currently unknown. In this study, we used cultured skin fibroblasts as a window into the mitochondrial dysfunction evident in MELAS cells, as well as to study the mechanisms of rapamycin action, compared with control, healthy individuals. We observed that mitochondria from patients were fragmented, had a threefold decline in the average speed of motility, a twofold reduced mitochondrial membrane potential, and a 1.5- to 2-fold decline in basal respiration. Despite the reduction in mitochondrial function, mitochondrial import protein Tim23 was elevated in patient cell lines. MELAS fibroblasts exhibited increased MnSOD levels and lysosomal function when compared with healthy controls. Treatment of MELAS fibroblasts with rapamycin for 24 h resulted in increased mitochondrial respiration compared with control cells, a higher lysosome content, and a greater localization of mitochondria to lysosomes. Our studies suggest that rapamycin has the potential to improve cellular health even in the presence of mtDNA defects, primarily via an increase in lysosomal content.

Keywords: human fibroblasts; lysosomes; mitochondrial health; mitochondrial myopathies; therapeutic agent.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Case-Control Studies
  • Child, Preschool
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism
  • Female
  • Fibroblasts / drug effects*
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Gene Expression Regulation
  • Humans
  • Infant
  • Lysosomes / drug effects*
  • Lysosomes / metabolism
  • MELAS Syndrome / drug therapy
  • MELAS Syndrome / genetics*
  • MELAS Syndrome / metabolism
  • MELAS Syndrome / pathology
  • Male
  • Membrane Potential, Mitochondrial / drug effects
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondrial Membrane Transport Proteins / genetics
  • Mitochondrial Membrane Transport Proteins / metabolism
  • Mitochondrial Precursor Protein Import Complex Proteins
  • Mutation
  • Oxidative Phosphorylation / drug effects
  • Primary Cell Culture
  • Sequestosome-1 Protein / genetics
  • Sequestosome-1 Protein / metabolism
  • Sirolimus / pharmacology*
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Vacuolar Proton-Translocating ATPases / genetics
  • Vacuolar Proton-Translocating ATPases / metabolism
  • Young Adult

Substances

  • DNA, Mitochondrial
  • Mitochondrial Membrane Transport Proteins
  • Mitochondrial Precursor Protein Import Complex Proteins
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • TIMM23 protein, human
  • Superoxide Dismutase
  • Vacuolar Proton-Translocating ATPases
  • Sirolimus

Associated data

  • figshare/10.6084/m9.figshare.14745891