The Muscular Dystrophy Gene TMEM5 Encodes a Ribitol β1,4-Xylosyltransferase Required for the Functional Glycosylation of Dystroglycan

J Biol Chem. 2016 Nov 18;291(47):24618-24627. doi: 10.1074/jbc.M116.751917. Epub 2016 Oct 12.

Abstract

A defect in O-mannosyl glycan is the cause of α-dystroglycanopathy, a group of congenital muscular dystrophies caused by aberrant α-dystroglycan (α-DG) glycosylation. Recently, the entire structure of O-mannosyl glycan, [3GlcAβ1-3Xylα1]n-3GlcAβ1-4Xyl-Rbo5P-1Rbo5P-3GalNAcβ1-3GlcNAcβ1-4 (phospho-6)Manα1-, which is required for the binding of α-DG to extracellular matrix ligands, has been proposed. However, the linkage of the first Xyl residue to ribitol 5-phosphate (Rbo5P) is not clear. TMEM5 is a gene product responsible for α-dystroglycanopathy and was reported as a potential enzyme involved in this linkage formation, although the experimental evidence is still incomplete. Here, we report that TMEM5 is a xylosyltransferase that forms the Xylβ1-4Rbo5P linkage on O-mannosyl glycan. The anomeric configuration and linkage position of the product (β1,4 linkage) was determined by NMR analysis. The introduction of two missense mutations in TMEM5 found in α-dystroglycanopathy patients impaired xylosyltransferase activity. Furthermore, the disruption of the TMEM5 gene by CRISPR/Cas9 abrogated the elongation of the (-3GlcAβ1-3Xylα1-) unit on O-mannosyl glycan. Based on these results, we concluded that TMEM5 acts as a UDP-d-xylose:ribitol-5-phosphate β1,4-xylosyltransferase in the biosynthetic pathway of O-mannosyl glycan.

Keywords: O-mannosyl glycan; TMEM5; dystroglycan; glycoconjugate; glycosylation; glycosyltransferase; muscular dystrophy; xylosyltransferase.

MeSH terms

  • Cell Line
  • Dystroglycans / chemistry
  • Dystroglycans / genetics
  • Dystroglycans / metabolism*
  • Glycosylation
  • Humans
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Muscular Dystrophies / genetics
  • Muscular Dystrophies / metabolism*
  • Mutation, Missense
  • Nuclear Magnetic Resonance, Biomolecular
  • Pentosyltransferases
  • Transferases (Other Substituted Phosphate Groups) / chemistry
  • Transferases (Other Substituted Phosphate Groups) / genetics
  • Transferases (Other Substituted Phosphate Groups) / metabolism*

Substances

  • Membrane Proteins
  • Dystroglycans
  • Pentosyltransferases
  • RXYLT1 protein, human
  • Transferases (Other Substituted Phosphate Groups)