Phosphatidic acid induces conformational changes in Sec18 protomers that prevent SNARE priming

J Biol Chem. 2019 Mar 1;294(9):3100-3116. doi: 10.1074/jbc.RA118.006552. Epub 2019 Jan 7.

Abstract

Eukaryotic cell homeostasis requires transfer of cellular components among organelles and relies on membrane fusion catalyzed by SNARE proteins. Inactive SNARE bundles are reactivated by hexameric N-ethylmaleimide-sensitive factor, vesicle-fusing ATPase (Sec18/NSF)-driven disassembly that enables a new round of membrane fusion. We previously found that phosphatidic acid (PA) binds Sec18 and thereby sequesters it from SNAREs and that PA dephosphorylation dissociates Sec18 from the membrane, allowing it to engage SNARE complexes. We now report that PA also induces conformational changes in Sec18 protomers and that hexameric Sec18 cannot bind PA membranes. Molecular dynamics (MD) analyses revealed that the D1 and D2 domains of Sec18 contain PA-binding sites and that the residues needed for PA binding are masked in hexameric Sec18. Importantly, these simulations also disclosed that a major conformational change occurs in the linker region between the D1 and D2 domains, which is distinct from the conformational changes that occur in hexameric Sec18 during SNARE priming. Together, these findings indicate that PA regulates Sec18 function by altering its architecture and stabilizing membrane-bound Sec18 protomers.

Keywords: Lipin1; NSF; Pah1; SNARE proteins; Sec17; Sec18; diacylglycerol; membrane fusion; membrane lipid; phosphatidic acid.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adenosine Triphosphatases / chemistry*
  • Adenosine Triphosphatases / metabolism*
  • Adenosine Triphosphate / metabolism
  • Molecular Dynamics Simulation
  • N-Ethylmaleimide-Sensitive Proteins / metabolism
  • Phosphatidic Acids / metabolism
  • Phosphatidic Acids / pharmacology*
  • Phosphorylation
  • Protein Domains
  • Protein Multimerization
  • Protein Structure, Secondary / drug effects
  • Protein Subunits / chemistry*
  • Protein Subunits / metabolism*
  • SNARE Proteins / chemistry
  • SNARE Proteins / metabolism*
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / chemistry*
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Substrate Specificity
  • Vesicular Transport Proteins / chemistry*
  • Vesicular Transport Proteins / metabolism*

Substances

  • Phosphatidic Acids
  • Protein Subunits
  • SNARE Proteins
  • Saccharomyces cerevisiae Proteins
  • Vesicular Transport Proteins
  • Adenosine Triphosphate
  • Adenosine Triphosphatases
  • SEC18 protein, S cerevisiae
  • N-Ethylmaleimide-Sensitive Proteins

Associated data

  • PDB/3J94
  • PDB/1E32