PUBLICATION

Analysis of Mucolipidosis II/III GNPTAB Missense Mutations Identifies Domains of UDP-GlcNAc:Lysosomal Enzyme GlcNAc-1-Phosphotransferase Involved in Catalytic Function and Lysosomal Enzyme Recognition

Authors
Qian, Y., van Meel, E., Flanagan-Steet, H., Yox, A., Steet, R., Kornfeld, S.
ID
ZDB-PUB-141217-9
Date
2015
Source
The Journal of biological chemistry   290(5): 3045-56 (Journal)
Registered Authors
Flanagan-Steet, Heather, Steet, Richard
Keywords
GlcNAc-1-phosphotransferase, Golgi, Notch domains, enzyme, genetic disease, lysosomal storage disease, mannose 6-phosphate, mucolipidosis II, mucolipidosis III αβ, zebrafish
MeSH Terms
  • Animals
  • Humans
  • Lysosomes/metabolism*
  • Mucolipidoses/enzymology*
  • Mucolipidoses/genetics*
  • Mucolipidoses/metabolism
  • Mutation, Missense/genetics*
  • Transferases (Other Substituted Phosphate Groups)/genetics*
  • Transferases (Other Substituted Phosphate Groups)/metabolism*
  • Zebrafish
PubMed
25505245 Full text @ J. Biol. Chem.
Abstract
UDP-GlcNAc:lysosomal enzyme GlcNAc-1-phosphotransferase tags newly synthesized lysosomal enzymes with mannose 6-phosphate recognition markers, which are required for their targeting to the endo-lysosomal system. GNPTAB encodes the α and β subunits of GlcNAc-1-phosphotransferase and mutations in this gene cause the lysosomal storage disorders mucolipidosis II and III αβ. Prior investigation of missense mutations in GNPTAB uncovered amino acids in the N-terminal region and within the DMAP domain involved in Golgi retention of GlcNAc-1-phosphotransferase and its ability to specifically recognize lysosomal hydrolases, respectively. Here, we undertook a comprehensive analysis of the remaining missense mutations in GNPTAB reported in mucolipidosis II and III αβ patients using cell- and zebrafish-based approaches. We show that the Stealth domain harbors the catalytic site, since some mutations in these regions greatly impaired the activity of the enzyme without affecting its Golgi localization and proteolytic processing. We also demonstrate a role for the Notch repeat 1 in lysosomal hydrolase recognition, since missense mutations in conserved cysteine residues in this domain do not affect the catalytic activity, but impair mannose phosphorylation of certain lysosomal hydrolases. Rescue experiments using mRNA bearing Notch repeat 1 mutations in GNPTAB-deficient zebrafish revealed selective effects on hydrolase recognition that differ from the DMAP mutation. Finally, the mutant R587P, located in the spacer between Notch 2 and DMAP, was partially rescued by overexpression of the γ subunit, suggesting a role for this region in γ subunit binding. These studies provide new insight into the functions of the different domains of the α and β subunits.
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