Endogenous glucuronyltransferase activity of LARGE or LARGE2 required for functional modification of α-dystroglycan in cells and tissues

J Biol Chem. 2014 Oct 10;289(41):28138-48. doi: 10.1074/jbc.M114.597831. Epub 2014 Aug 19.

Abstract

Mutations in the LARGE gene have been identified in congenital muscular dystrophy (CMD) patients with brain abnormalities. Both LARGE and its paralog, LARGE2 (also referred to as GYLTL1B) are bifunctional glycosyltransferases with xylosyltransferase (Xyl-T) and glucuronyltransferase (GlcA-T) activities, and are capable of forming polymers consisting of [-3Xyl-α1,3GlcAβ1-] repeats. LARGE-dependent modification of α-dystroglycan (α-DG) with these polysaccharides is essential for the ability of α-DG to act as a receptor for ligands in the extracellular matrix. Here we report on the endogenous enzymatic activities of LARGE and LARGE2 in mice and humans, using a newly developed assay for GlcA-T activity. We show that normal mouse and human cultured cells have endogenous LARGE GlcA-T, and that this activity is absent in cells from the Large(myd) (Large-deficient) mouse model of muscular dystrophy, as well as in cells from CMD patients with mutations in the LARGE gene. We also demonstrate that GlcA-T activity is significant in the brain, heart, and skeletal muscle of wild-type and Large2(-/-) mice, but negligible in the corresponding tissues of the Large(myd) mice. Notably, GlcA-T activity is substantial, though reduced, in the kidneys of both the Large(myd) and Large2(-/-) mice, consistent with the observation of α-DG/laminin binding in these contexts. This study is the first to test LARGE activity in samples as small as cryosections and, moreover, provides the first direct evidence that not only LARGE, but also LARGE2, is vital to effective functional modification of α-DG in vivo.

Keywords: Dystroglycan; Extracellular Matrix; Glucuronyltransferase; Glycosyltransferase; LARGE; Laminin; Muscular Dystrophy; Post-translational Modification (PTM).

Publication types

  • Case Reports
  • Research Support, American Recovery and Reinvestment Act
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Brain / enzymology
  • Brain / pathology
  • Cells, Cultured
  • Child
  • Disease Models, Animal
  • Dystroglycans / genetics
  • Dystroglycans / metabolism*
  • Enzyme Assays
  • Female
  • Fibroblasts / enzymology
  • Fibroblasts / pathology
  • Gene Expression Regulation
  • Glycosyltransferases / genetics
  • Glycosyltransferases / metabolism*
  • Humans
  • Kidney / enzymology
  • Kidney / pathology
  • Laminin / genetics
  • Laminin / metabolism*
  • Mice
  • Mice, Knockout
  • Muscle, Skeletal / enzymology
  • Muscle, Skeletal / pathology
  • Muscular Dystrophies / enzymology*
  • Muscular Dystrophies / genetics
  • Muscular Dystrophies / pathology
  • Myocardium / enzymology
  • Myocardium / pathology
  • N-Acetylglucosaminyltransferases / genetics
  • N-Acetylglucosaminyltransferases / metabolism*
  • Organ Specificity
  • Protein Binding

Substances

  • Laminin
  • Dystroglycans
  • Glycosyltransferases
  • Large1 protein, mouse
  • Large2 protein, mouse
  • N-Acetylglucosaminyltransferases