MICOS assembly controls mitochondrial inner membrane remodeling and crista junction redistribution to mediate cristae formation

EMBO J. 2020 Jul 15;39(14):e104105. doi: 10.15252/embj.2019104105. Epub 2020 Jun 22.

Abstract

Mitochondrial function is critically dependent on the folding of the mitochondrial inner membrane into cristae; indeed, numerous human diseases are associated with aberrant crista morphologies. With the MICOS complex, OPA1 and the F1 Fo -ATP synthase, key players of cristae biogenesis have been identified, yet their interplay is poorly understood. Harnessing super-resolution light and 3D electron microscopy, we dissect the roles of these proteins in the formation of cristae in human mitochondria. We individually disrupted the genes of all seven MICOS subunits in human cells and re-expressed Mic10 or Mic60 in the respective knockout cell line. We demonstrate that assembly of the MICOS complex triggers remodeling of pre-existing unstructured cristae and de novo formation of crista junctions (CJs) on existing cristae. We show that the Mic60-subcomplex is sufficient for CJ formation, whereas the Mic10-subcomplex controls lamellar cristae biogenesis. OPA1 stabilizes tubular CJs and, along with the F1 Fo -ATP synthase, fine-tunes the positioning of the MICOS complex and CJs. We propose a new model of cristae formation, involving the coordinated remodeling of an unstructured crista precursor into multiple lamellar cristae.

Keywords: MINFLUX; cristae biogenesis; electron microscopy; nanoscopy; super-resolution microscopy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • HeLa Cells
  • Humans
  • Membrane Cofactor Protein / genetics
  • Membrane Cofactor Protein / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mitochondrial Membranes / metabolism*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Mitochondrial Proton-Translocating ATPases / genetics
  • Mitochondrial Proton-Translocating ATPases / metabolism
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism*

Substances

  • CD46 protein, human
  • Membrane Cofactor Protein
  • Membrane Proteins
  • Mitochondrial Proteins
  • Multiprotein Complexes
  • F1F0-ATP synthase
  • Mitochondrial Proton-Translocating ATPases