A novel post-translational modification in nerve terminals: O-linked N-acetylglucosamine phosphorylation

J Proteome Res. 2011 Jun 3;10(6):2725-33. doi: 10.1021/pr1011153. Epub 2011 May 2.

Abstract

Protein phosphorylation and glycosylation are the most common post-translational modifications observed in biology, frequently on the same protein. Assembly protein AP180 is a synapse-specific phosphoprotein and O-linked beta-N-acetylglucosamine (O-GlcNAc) modified glycoprotein. AP180 is involved in the assembly of clathrin coated vesicles in synaptic vesicle endocytosis. Unlike other types of O-glycosylation, O-GlcNAc is nucleocytoplasmic and reversible. It was thought to be a terminal modification, that is, the O-GlcNAc was not found to be additionally modified in any way. We now show that AP180 purified from rat brain contains a phosphorylated O-GlcNAc (O-GlcNAc-P) within a highly conserved sequence. O-GlcNAc or O-GlcNAc-P, but not phosphorylation alone, was found at Thr-310. Analysis of synthetic GlcNAc-6-P produced identical fragmentation products to GlcNAc-P from AP180. Direct O-linkage of GlcNAc-P to a Thr residue was confirmed by electron transfer dissociation MS. A second AP180 tryptic peptide was also glycosyl phosphorylated, but the site of modification was not assigned. Sequence similarities suggest there may be a common motif within AP180 involving glycosyl phosphorylation and dual flanking phosphorylation sites within 4 amino acid residues. This novel type of protein glycosyl phosphorylation adds a new signaling mechanism to the regulation of neurotransmission and more complexity to the study of O-GlcNAc modification.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylglucosamine / metabolism*
  • Amino Acid Sequence
  • Animals
  • Conserved Sequence
  • Molecular Sequence Data
  • Monomeric Clathrin Assembly Proteins / chemistry
  • Monomeric Clathrin Assembly Proteins / metabolism
  • Peptide Fragments / chemistry
  • Phosphorylation
  • Protein Processing, Post-Translational*
  • Rats
  • Sugar Phosphates / metabolism*
  • Synapses / metabolism*
  • Tandem Mass Spectrometry

Substances

  • Monomeric Clathrin Assembly Proteins
  • Peptide Fragments
  • Sugar Phosphates
  • clathrin assembly protein AP180
  • Acetylglucosamine