VAP-A intrinsically disordered regions enable versatile tethering at membrane contact sites

Dev Cell. 2023 Jan 23;58(2):121-138.e9. doi: 10.1016/j.devcel.2022.12.010.

Abstract

Membrane contact sites (MCSs) are heterogeneous in shape, composition, and dynamics. Despite this diversity, VAP proteins act as receptors for multiple FFAT motif-containing proteins and drive the formation of most MCSs that involve the endoplasmic reticulum (ER). Although the VAP-FFAT interaction is well characterized, no model explains how VAP adapts to its partners in various MCSs. We report that VAP-A localization to different MCSs depends on its intrinsically disordered regions (IDRs) in human cells. VAP-A interaction with PTPIP51 and VPS13A at ER-mitochondria MCS conditions mitochondria fusion by promoting lipid transfer and cardiolipin buildup. VAP-A also enables lipid exchange at ER-Golgi MCS by interacting with oxysterol-binding protein (OSBP) and CERT. However, removing IDRs from VAP-A restricts its distribution and function to ER-mitochondria MCS. Our data suggest that IDRs do not modulate VAP-A preference toward specific partners but do adjust their geometry to MCS organization and lifetime constraints. Thus, IDR-mediated VAP-A conformational flexibility ensures membrane tethering plasticity and efficiency.

Keywords: Golgi apparatus; VAP; cryo-EM; endoplasmic reticulum; intrinsically disordered region; lipid transfer protein; membrane contact site; membrane tethering; mitochondrial fusion; protein flexibility.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Carrier Proteins / metabolism
  • Humans
  • Lipids / chemistry
  • Membrane Proteins* / metabolism
  • Vesicular Transport Proteins* / metabolism

Substances

  • Membrane Proteins
  • Vesicular Transport Proteins
  • Carrier Proteins
  • Lipids