TTC19 Plays a Husbandry Role on UQCRFS1 Turnover in the Biogenesis of Mitochondrial Respiratory Complex III

Mol Cell. 2017 Jul 6;67(1):96-105.e4. doi: 10.1016/j.molcel.2017.06.001. Epub 2017 Jun 29.

Abstract

Loss-of-function mutations in TTC19 (tetra-tricopeptide repeat domain 19) have been associated with severe neurological phenotypes and mitochondrial respiratory chain complex III deficiency. We previously demonstrated the mitochondrial localization of TTC19 and its link with complex III biogenesis. Here we provide detailed insight into the mechanistic role of TTC19, by investigating a Ttc19?/? mouse model that shows progressive neurological and metabolic decline, decreased complex III activity, and increased production of reactive oxygen species. By using both the Ttc19?/? mouse model and a range of human cell lines, we demonstrate that TTC19 binds to the fully assembled complex III dimer, i.e., after the incorporation of the iron-sulfur Rieske protein (UQCRFS1). The in situ maturation of UQCRFS1 produces N-terminal polypeptides, which remain bound to holocomplex III. We show that, in normal conditions, these UQCRFS1 fragments are rapidly removed, but when TTC19 is absent they accumulate within complex III, causing its structural and functional impairment.

Keywords: Rieske protein; TTC19; UQCRFS1; complex III deficiency; mitochondrial complex III; mitochondrial disease; mitochondrial quality control; mitochondrial respiratory chain; mouse model.

MeSH terms

  • Animals
  • Behavior, Animal
  • Disease Models, Animal
  • Electron Transport Complex III / deficiency
  • Electron Transport Complex III / genetics
  • Electron Transport Complex III / metabolism*
  • Female
  • Genotype
  • HeLa Cells
  • Humans
  • Iron-Sulfur Proteins / genetics
  • Iron-Sulfur Proteins / metabolism*
  • Kinetics
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / enzymology*
  • Mitochondrial Diseases
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Motor Activity
  • Nerve Degeneration
  • Nervous System / metabolism
  • Nervous System / pathology
  • Nervous System / physiopathology
  • Phenotype
  • Protein Binding
  • Protein Stability
  • Proteolysis
  • Reactive Oxygen Species / metabolism

Substances

  • Iron-Sulfur Proteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • Rieske iron-sulfur protein
  • TTC19 protein, human
  • UQCRFS1 protein, human
  • UQCRFS1 protein, mouse
  • tetratricopeptide 19 protein, mouse
  • Electron Transport Complex III

Supplementary concepts

  • Mitochondrial Complex III Deficiency