Intracellular transport of human lysosomal alpha-mannosidase and alpha-mannosidosis-related mutants

Biochem J. 2004 Jul 15;381(Pt 2):537-46. doi: 10.1042/BJ20031499.

Abstract

Human LAMAN (lysosomal a-mannosidase) was synthesized as a 120 kDa precursor in transfected COS cells [African-green-monkey kidney cells], which was partly secreted as a single-chain form and partly sorted to the lysosomes being subsequently cleaved into three peptides of 70, 40 and 15 kDa respectively. Both the secreted and the lysosomal forms contained endo H (endoglucosidase H)-resistant glycans, suggesting a common pathway through the trans-Golgi network. A fraction of LAMAN was retained intracellularly as a single-chain endo H-sensitive form, probably in the ER (endoplasmic reticulum). The inherited lack of LAMAN causes the autosomal recessive storage disease a-mannosidosis. To understand the biochemical consequences of the disease-causing mutations, 11 missense mutations and two in-frame deletions were introduced into human LAMAN cDNA by in vitro mutagenesis and the resulting proteins were expressed in COS cells. Some selected mutants were also expressed in Chinese-hamster ovary cells. T355P (Thr355Pro), P356R, W714R, R750W and L809P LAMANs as well as both deletion mutants were misfolded and arrested in the ER as inactive single-chain forms. Six of the mutants were transported to the lysosomes, either with less than 5% of normal specific activity (H72L, D196E/N and R220H LAMANs) or with more than 30% of normal specific activity (E402K LAMAN). F320L LAMAN resulted in much lower activity in Chinese-hamster ovary cells when compared with COS cells. Modelling into the three-dimensional structure revealed that the mutants with highly reduced specific activities contained substitutions of amino acids involved in the catalysis, either co-ordinating Zn2+ (His72 and Asp196), stabilizing the active-site nucleophile (Arg220) or positioning the active-site residue Asp319 (Phe320).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CHO Cells / chemistry
  • CHO Cells / metabolism
  • COS Cells / chemistry
  • COS Cells / metabolism
  • Cattle
  • Cell Line
  • Chlorocebus aethiops
  • Cricetinae
  • Genotype
  • Isoenzymes / chemistry
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Lysosomes / enzymology*
  • Mannosidases
  • Models, Molecular
  • Mutagenesis, Site-Directed / genetics
  • Phenotype
  • Protein Structure, Quaternary
  • Protein Transport / genetics
  • Protein Transport / physiology*
  • Transfection / methods
  • alpha-Mannosidase / chemistry
  • alpha-Mannosidase / genetics
  • alpha-Mannosidase / metabolism*
  • alpha-Mannosidosis / enzymology*
  • alpha-Mannosidosis / genetics

Substances

  • Isoenzymes
  • Mannosidases
  • alpha-Mannosidase