A Coincidence Detection Mechanism Controls PX-BAR Domain-Mediated Endocytic Membrane Remodeling via an Allosteric Structural Switch

Dev Cell. 2017 Nov 20;43(4):522-529.e4. doi: 10.1016/j.devcel.2017.10.019.

Abstract

Clathrin-mediated endocytosis occurs by bending and remodeling of the membrane underneath the coat. Bin-amphiphysin-rvs (BAR) domain proteins are crucial for endocytic membrane remodeling, but how their activity is spatiotemporally controlled is largely unknown. We demonstrate that the membrane remodeling activity of sorting nexin 9 (SNX9), a late-acting endocytic PX-BAR domain protein required for constriction of U-shaped endocytic intermediates, is controlled by an allosteric structural switch involving coincident detection of the clathrin adaptor AP2 and phosphatidylinositol-3,4-bisphosphate (PI(3,4)P2) at endocytic sites. Structural, biochemical, and cell biological data show that SNX9 is autoinhibited in solution. Binding to PI(3,4)P2 via its PX-BAR domain, and concomitant association with AP2 via sequences in the linker region, releases SNX9 autoinhibitory contacts to enable membrane constriction. Our results reveal a mechanism for restricting the latent membrane remodeling activity of BAR domain proteins to allow spatiotemporal coupling of membrane constriction to the progression of the endocytic pathway.

Keywords: BAR domain proteins; NMR spectroscopy; endocytosis; hydrogen-deuterium exchange mass spectrometry (HDX-MS); membrane remodeling; phosphoinositides.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allosteric Site
  • Animals
  • Cell Membrane / metabolism*
  • Endocytosis / physiology*
  • Humans
  • Nerve Tissue Proteins / metabolism*
  • Phosphatidylinositol Phosphates / metabolism
  • Phosphatidylinositols / metabolism
  • Protein Binding / physiology
  • Sorting Nexins / metabolism
  • Vesicular Transport Proteins / chemistry
  • Vesicular Transport Proteins / metabolism*

Substances

  • Nerve Tissue Proteins
  • Phosphatidylinositol Phosphates
  • Phosphatidylinositols
  • Sorting Nexins
  • Vesicular Transport Proteins
  • amphiphysin