Structural and mechanistic insights into secretagogin-mediated exocytosis

Proc Natl Acad Sci U S A. 2020 Mar 24;117(12):6559-6570. doi: 10.1073/pnas.1919698117. Epub 2020 Mar 10.

Abstract

Secretagogin (SCGN) is a hexa-EF-hand protein that is highly expressed in the pancreas, brain, and gastrointestinal tract. SCGN is known to modulate regulated exocytosis in multiple cell lines and tissues; however, its exact functions and underlying mechanisms remain unclear. Here, we report that SCGN interacts with the plasma membrane SNARE SNAP-25, but not the assembled SNARE complex, in a Ca2+-dependent manner. The crystal structure of SCGN in complex with a SNAP-25 fragment reveals that SNAP-25 adopts a helical structure and binds to EF-hands 5 and 6 of SCGN. SCGN strongly inhibits SNARE-mediated vesicle fusion in vitro by binding to SNAP-25. SCGN promotes the plasma membrane localization of SNAP-25, but not Syntaxin-1a, in SCGN-expressing cells. Finally, SCGN controls neuronal growth and brain development in zebrafish, likely via interacting with SNAP-25 or its close homolog, SNAP-23. Our results thus provide insights into the regulation of SNAREs and suggest that aberrant synapse functions underlie multiple neurological disorders caused by SCGN deficiency.

Keywords: SNAP-25; SNARE; neurological disorder; neuronal development; regulated exocytosis.

Publication types

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

MeSH terms

  • Animals
  • Binding Sites
  • Brain / growth & development
  • Brain / metabolism
  • Calcium / metabolism
  • Cell Line
  • Cell Membrane / metabolism
  • Exocytosis*
  • Gene Expression Regulation, Developmental
  • Humans
  • Mutation
  • Protein Binding
  • Protein Conformation
  • Secretagogins / chemistry*
  • Secretagogins / genetics
  • Secretagogins / metabolism*
  • Synaptosomal-Associated Protein 25 / genetics
  • Synaptosomal-Associated Protein 25 / metabolism
  • Zebrafish

Substances

  • Secretagogins
  • Synaptosomal-Associated Protein 25
  • Calcium

Associated data

  • PDB/6JLH