Bax assembly into rings and arcs in apoptotic mitochondria is linked to membrane pores

EMBO J. 2016 Feb 15;35(4):389-401. doi: 10.15252/embj.201593384. Epub 2016 Jan 18.

Abstract

Bax is a key regulator of apoptosis that, under cell stress, accumulates at mitochondria, where it oligomerizes to mediate the permeabilization of the mitochondrial outer membrane leading to cytochrome c release and cell death. However, the underlying mechanism behind Bax function remains poorly understood. Here, we studied the spatial organization of Bax in apoptotic cells using dual-color single-molecule localization-based super-resolution microscopy. We show that active Bax clustered into a broad distribution of distinct architectures, including full rings, as well as linear and arc-shaped oligomeric assemblies that localized in discrete foci along mitochondria. Remarkably, both rings and arcs assemblies of Bax perforated the membrane, as revealed by atomic force microscopy in lipid bilayers. Our data identify the supramolecular organization of Bax during apoptosis and support a molecular mechanism in which Bax fully or partially delineates pores of different sizes to permeabilize the mitochondrial outer membrane.

Keywords: AFM; Bcl‐2; apoptosis; pore‐forming protein; super‐resolution microscopy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis*
  • Cytochromes c / metabolism
  • HeLa Cells
  • Humans
  • Microscopy, Electron, Transmission
  • Microscopy, Fluorescence
  • Mitochondria / enzymology*
  • Mitochondrial Membranes / metabolism*
  • Mitochondrial Membranes / physiology
  • Permeability
  • Pore Forming Cytotoxic Proteins / metabolism*
  • Protein Multimerization*
  • bcl-2-Associated X Protein / metabolism*

Substances

  • BAX protein, human
  • Pore Forming Cytotoxic Proteins
  • bcl-2-Associated X Protein
  • Cytochromes c