Neuroligin trafficking deficiencies arising from mutations in the alpha/beta-hydrolase fold protein family

J Biol Chem. 2010 Sep 10;285(37):28674-82. doi: 10.1074/jbc.M110.139519. Epub 2010 Jul 8.

Abstract

Despite great functional diversity, characterization of the alpha/beta-hydrolase fold proteins that encompass a superfamily of hydrolases, heterophilic adhesion proteins, and chaperone domains reveals a common structural motif. By incorporating the R451C mutation found in neuroligin (NLGN) and associated with autism and the thyroglobulin G2320R (G221R in NLGN) mutation responsible for congenital hypothyroidism into NLGN3, we show that mutations in the alpha/beta-hydrolase fold domain influence folding and biosynthetic processing of neuroligin3 as determined by in vitro susceptibility to proteases, glycosylation processing, turnover, and processing rates. We also show altered interactions of the mutant proteins with chaperones in the endoplasmic reticulum and arrest of transport along the secretory pathway with diversion to the proteasome. Time-controlled expression of a fluorescently tagged neuroligin in hippocampal neurons shows that these mutations compromise neuronal trafficking of the protein, with the R451C mutation reducing and the G221R mutation virtually abolishing the export of NLGN3 from the soma to the dendritic spines. Although the R451C mutation causes a local folding defect, the G221R mutation appears responsible for more global misfolding of the protein, reflecting their sequence positions in the structure of the protein. Our results suggest that disease-related mutations in the alpha/beta-hydrolase fold domain share common trafficking deficiencies yet lead to discrete congenital disorders of differing severity in the endocrine and nervous systems.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Substitution
  • Animals
  • Autistic Disorder / genetics
  • Autistic Disorder / metabolism
  • Cell Adhesion Molecules, Neuronal / genetics
  • Cell Adhesion Molecules, Neuronal / metabolism*
  • Cell Line
  • Congenital Hypothyroidism / genetics
  • Congenital Hypothyroidism / metabolism
  • Dendrites / metabolism*
  • Hippocampus / metabolism*
  • Humans
  • Hydrolases
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mutation, Missense*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Protein Folding*
  • Protein Processing, Post-Translational*
  • Protein Structure, Tertiary
  • Protein Transport / genetics
  • Rats

Substances

  • Cell Adhesion Molecules, Neuronal
  • Membrane Proteins
  • Nerve Tissue Proteins
  • neuroligin 3
  • Hydrolases