Single-particle electron microscopy structure of UDP-glucose:glycoprotein glucosyltransferase suggests a selectivity mechanism for misfolded proteins

J Biol Chem. 2017 Jul 7;292(27):11499-11507. doi: 10.1074/jbc.M117.789495. Epub 2017 May 10.

Abstract

The enzyme UDP-glucose:glycoprotein glucosyltransferase (UGGT) mediates quality control of glycoproteins in the endoplasmic reticulum by attaching glucose to N-linked glycan of misfolded proteins. As a sensor, UGGT ensures that misfolded proteins are recognized by the lectin chaperones and do not leave the secretory pathway. The structure of UGGT and the mechanism of its selectivity for misfolded proteins have been unknown for 25 years. Here, we used negative-stain electron microscopy and small-angle X-ray scattering to determine the structure of UGGT from Drosophila melanogaster at 18-Å resolution. Three-dimensional reconstructions revealed a cage-like structure with a large central cavity. Particle classification revealed flexibility that precluded determination of a high-resolution structure. Introduction of biotinylation sites into a fungal UGGT expressed in Escherichia coli allowed identification of the catalytic and first thioredoxin-like domains. We also used hydrogen-deuterium exchange mass spectrometry to map the binding site of an accessory protein, Sep15, to the first thioredoxin-like domain. The UGGT structural features identified suggest that the central cavity contains the catalytic site and is lined with hydrophobic surfaces. This enhances the binding of misfolded substrates with exposed hydrophobic residues and excludes folded proteins with hydrophilic surfaces. In conclusion, we have determined the UGGT structure, which enabled us to develop a plausible functional model of the mechanism for UGGT's selectivity for misfolded glycoproteins.

Keywords: ER quality control; chaperone; electron microscopy (EM); glycoprotein biosynthesis; major histocompatibility complex (MHC).

MeSH terms

  • Animals
  • Deuterium Exchange Measurement
  • Drosophila Proteins / chemistry
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster
  • Glucosyltransferases / chemistry*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Hydrophobic and Hydrophilic Interactions
  • Protein Domains
  • Protein Folding*
  • Selenoproteins / chemistry
  • Selenoproteins / genetics
  • Selenoproteins / metabolism
  • Uridine Diphosphate Sugars / chemistry*
  • Uridine Diphosphate Sugars / genetics
  • Uridine Diphosphate Sugars / metabolism

Substances

  • CG7484 protein, Drosophila
  • Drosophila Proteins
  • Selenoproteins
  • Uridine Diphosphate Sugars
  • Glucosyltransferases
  • mannosylglycoprotein 1,3-glucosyltransferase