Disease mutations in CMP-sialic acid transporter SLC35A1 result in abnormal α-dystroglycan O-mannosylation, independent from sialic acid

Hum Mol Genet. 2015 Apr 15;24(8):2241-6. doi: 10.1093/hmg/ddu742. Epub 2014 Dec 30.

Abstract

Binding of cellular α-dystroglycan (α-DG) to its extracellular matrix ligands is fully dependent on a unique O-mannose-linked glycan. Disrupted O-mannosylation is the hallmark of the muscular dystrophy-dystroglycanopathy (MDDG) syndromes. SLC35A1, encoding the transporter of cytidine 5'-monophosphate-sialic acid, was recently identified as MDDG candidate gene. This is surprising, since sialic acid itself is dispensable for α-DG-ligand binding. In a novel SLC35A1-deficient cell model, we demonstrated a lack of α-DG O-mannosylation, ligand binding and incorporation of sialic acids. Removal of sialic acids from HAP1 wild-type cells after incorporation or preventing sialylation during synthesis did not affect α-DG O-mannosylation or ligand binding but did affect sialylation. Lentiviral-mediated complementation with the only known disease mutation p.Q101H failed to restore deficient O-mannosylation in SLC35A1 knockout cells and partly restored sialylation. These data indicate a role for SLC35A1 in α-DG O-mannosylation that is distinct from sialic acid metabolism. In addition, human SLC35A1 deficiency can be considered as a combined disorder of α-DG O-mannosylation and sialylation, a novel variant of the MDDG syndromes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Cytidine Monophosphate / metabolism
  • Dystroglycans / metabolism*
  • Humans
  • Mannose / metabolism*
  • Mutation
  • N-Acetylneuraminic Acid / metabolism
  • Nucleotide Transport Proteins / genetics*
  • Nucleotide Transport Proteins / metabolism
  • Walker-Warburg Syndrome / genetics*
  • Walker-Warburg Syndrome / metabolism*

Substances

  • Nucleotide Transport Proteins
  • SLC35A1 protein, human
  • Dystroglycans
  • Cytidine Monophosphate
  • N-Acetylneuraminic Acid
  • Mannose