Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies

Nature. 2002 Jul 25;418(6896):417-22. doi: 10.1038/nature00837.

Abstract

Muscle eye brain disease (MEB) and Fukuyama congenital muscular dystrophy (FCMD) are congenital muscular dystrophies with associated, similar brain malformations. The FCMD gene, fukutin, shares some homology with fringe-like glycosyltransferases, and the MEB gene, POMGnT1, seems to be a new glycosyltransferase. Here we show, in both MEB and FCMD patients, that alpha-dystroglycan is expressed at the muscle membrane, but similar hypoglycosylation in the diseases directly abolishes binding activity of dystroglycan for the ligands laminin, neurexin and agrin. We show that this post-translational biochemical and functional disruption of alpha-dystroglycan is recapitulated in the muscle and central nervous system of mutant myodystrophy (myd) mice. We demonstrate that myd mice have abnormal neuronal migration in cerebral cortex, cerebellum and hippocampus, and show disruption of the basal lamina. In addition, myd mice reveal that dystroglycan targets proteins to functional sites in brain through its interactions with extracellular matrix proteins. These results suggest that at least three distinct mammalian genes function within a convergent post-translational processing pathway during the biosynthesis of dystroglycan, and that abnormal dystroglycan-ligand interactions underlie the pathogenic mechanism of muscular dystrophy with brain abnormalities.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Brain / abnormalities
  • Brain / metabolism
  • Brain / pathology
  • Cell Movement
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Dystroglycans
  • Extracellular Matrix Proteins / metabolism
  • Eye / metabolism
  • Female
  • Gene Deletion
  • Glycosylation
  • Humans
  • Ligands
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Mutant Strains
  • Muscles / metabolism
  • Muscular Dystrophies / congenital*
  • Muscular Dystrophies / metabolism*
  • Neurons / metabolism
  • Neurons / pathology
  • Protein Binding
  • Protein Processing, Post-Translational*

Substances

  • Cytoskeletal Proteins
  • DAG1 protein, human
  • Extracellular Matrix Proteins
  • Ligands
  • Membrane Glycoproteins
  • Dystroglycans