NDUFS3 depletion permits complex I maturation and reveals TMEM126A/OPA7 as an assembly factor binding the ND4-module intermediate

Cell Rep. 2021 Apr 20;35(3):109002. doi: 10.1016/j.celrep.2021.109002.

Abstract

Complex I (CI) is the largest enzyme of the mitochondrial respiratory chain, and its defects are the main cause of mitochondrial disease. To understand the mechanisms regulating the extremely intricate biogenesis of this fundamental bioenergetic machine, we analyze the structural and functional consequences of the ablation of NDUFS3, a non-catalytic core subunit. We show that, in diverse mammalian cell types, a small amount of functional CI can still be detected in the complete absence of NDUFS3. In addition, we determine the dynamics of CI disassembly when the amount of NDUFS3 is gradually decreased. The process of degradation of the complex occurs in a hierarchical and modular fashion in which the ND4 module remains stable and bound to TMEM126A. We, thus, uncover the function of TMEM126A, the product of a disease gene causing recessive optic atrophy as a factor necessary for the correct assembly and function of CI.

Keywords: CI; CI modules; NDUFS3; SILAC; TMEM126A; assembly factor; optic atrophy type 7; respiratory complex I.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • CRISPR-Cas Systems
  • Cell Line, Tumor
  • Electron Transport Complex I / deficiency
  • Electron Transport Complex I / genetics*
  • Gene Editing
  • Gene Expression Regulation
  • Gene Knockout Techniques
  • HCT116 Cells
  • Humans
  • Melanocytes / metabolism
  • Melanocytes / pathology
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Mice
  • Mitochondria / genetics*
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Mitochondrial Membranes / chemistry
  • Mitochondrial Membranes / metabolism
  • Models, Molecular
  • NADH Dehydrogenase / deficiency
  • NADH Dehydrogenase / genetics*
  • Optic Atrophy / genetics*
  • Optic Atrophy / metabolism
  • Optic Atrophy / pathology
  • Osteoblasts / metabolism
  • Osteoblasts / pathology
  • Protein Binding
  • Protein Conformation
  • Proteomics

Substances

  • Membrane Proteins
  • TMEM126A protein, human
  • NADH Dehydrogenase
  • Electron Transport Complex I
  • NDUFS3 protein, human