B4GAT1 is the priming enzyme for the LARGE-dependent functional glycosylation of α-dystroglycan

Elife. 2014 Oct 3:3:e03943. doi: 10.7554/eLife.03943.

Abstract

Recent studies demonstrated that mutations in B3GNT1, an enzyme proposed to be involved in poly-N-acetyllactosamine synthesis, were causal for congenital muscular dystrophy with hypoglycosylation of α-dystroglycan (secondary dystroglycanopathies). Since defects in the O-mannosylation protein glycosylation pathway are primarily responsible for dystroglycanopathies and with no established O-mannose initiated structures containing a β3 linked GlcNAc known, we biochemically interrogated this human enzyme. Here we report this enzyme is not a β-1,3-N-acetylglucosaminyltransferase with catalytic activity towards β-galactose but rather a β-1,4-glucuronyltransferase, designated B4GAT1, towards both α- and β-anomers of xylose. The dual-activity LARGE enzyme is capable of extending products of B4GAT1 and we provide experimental evidence that B4GAT1 is the priming enzyme for LARGE. Our results further define the functional O-mannosylated glycan structure and indicate that B4GAT1 is involved in the initiation of the LARGE-dependent repeating disaccharide that is necessary for extracellular matrix protein binding to O-mannosylated α-dystroglycan that is lacking in secondary dystroglycanopathies.

Keywords: B3GNT1; B4GAT1; O-mannosylation; alpha-dystroglycan; biochemistry; congenital muscular dystrophy; glycosylation; human; human biology; medicine.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Biocatalysis
  • Disaccharides / metabolism
  • Dystroglycans / metabolism*
  • Glycosylation
  • HEK293 Cells
  • Humans
  • Kinetics
  • Models, Biological
  • Molecular Sequence Data
  • N-Acetylglucosaminyltransferases / chemistry
  • N-Acetylglucosaminyltransferases / metabolism*
  • Pentosyltransferases / metabolism
  • Solubility
  • Stereoisomerism
  • Substrate Specificity
  • Trisaccharides / metabolism
  • UDP Xylose-Protein Xylosyltransferase
  • Uridine Diphosphate Glucuronic Acid / metabolism
  • Xylose / chemistry
  • Xylose / metabolism

Substances

  • Disaccharides
  • Trisaccharides
  • Dystroglycans
  • Uridine Diphosphate Glucuronic Acid
  • Xylose
  • LARGE1 protein, human
  • N-Acetylglucosaminyltransferases
  • B4GAT1 protein, human
  • Pentosyltransferases