Regulation of presynaptic anchoring of the scaffold protein Bassoon by phosphorylation-dependent interaction with 14-3-3 adaptor proteins

PLoS One. 2013;8(3):e58814. doi: 10.1371/journal.pone.0058814. Epub 2013 Mar 14.

Abstract

The proper organization of the presynaptic cytomatrix at the active zone is essential for reliable neurotransmitter release from neurons. Despite of the virtual stability of this tightly interconnected proteinaceous network it becomes increasingly clear that regulated dynamic changes of its composition play an important role in the processes of synaptic plasticity. Bassoon, a core component of the presynaptic cytomatrix, is a key player in structural organization and functional regulation of presynaptic release sites. It is one of the most highly phosphorylated synaptic proteins. Nevertheless, to date our knowledge about functions mediated by any one of the identified phosphorylation sites of Bassoon is sparse. In this study, we have identified an interaction of Bassoon with the small adaptor protein 14-3-3, which depends on phosphorylation of the 14-3-3 binding motif of Bassoon. In vitro phosphorylation assays indicate that phosphorylation of the critical Ser-2845 residue of Bassoon can be mediated by a member of the 90-kDa ribosomal S6 protein kinase family. Elimination of Ser-2845 from the 14-3-3 binding motif results in a significant decrease of Bassoon's molecular exchange rates at synapses of living rat neurons. We propose that the phosphorylation-induced 14-3-3 binding to Bassoon modulates its anchoring to the presynaptic cytomatrix. This regulation mechanism might participate in molecular and structural presynaptic remodeling during synaptic plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / metabolism*
  • Amino Acid Sequence
  • Animals
  • Binding Sites
  • COS Cells
  • Chlorocebus aethiops
  • HEK293 Cells
  • Humans
  • Mice
  • Mutation
  • Nerve Tissue Proteins / chemistry
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neuronal Plasticity
  • Neurons / cytology
  • Neurons / metabolism
  • Phosphorylation
  • Rats
  • Ribosomal Protein S6 Kinases / metabolism
  • Synapses / metabolism*
  • Synapses / physiology

Substances

  • 14-3-3 Proteins
  • Bsn protein, rat
  • Nerve Tissue Proteins
  • Ribosomal Protein S6 Kinases

Grants and funding

This study was supported by DFG-SFB 779, the EC contract number 222918 (REPLACES) FP7 - Thematic priority HEALTH to EDG and the European Regional Development Fonds and the Land Saxony-Anhalt (EFRE/LSA 2007-2013) to EDG and AF. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.