S250F variant associated with aromatic amino acid decarboxylase deficiency: molecular defects and intracellular rescue by pyridoxine

Hum Mol Genet. 2013 Apr 15;22(8):1615-24. doi: 10.1093/hmg/ddt011. Epub 2013 Jan 15.

Abstract

Dopa or aromatic amino acid decarboxylase (DDC, AADC) is a pyridoxal 5'-phosphate-dependent enzyme that catalyses the production of the neurotransmitters dopamine and serotonin. Among the so far identified mutations associated with AADC deficiency, an inherited rare neurometabolic disease, the S250F mutation is the most frequent one. Here, for the first time, the molecular basis of the deficit of the S250F variant was investigated both in vitro and in cellular systems. Ser250 is not essential for the catalytic activity of the enzyme. However, its mutation to Phe causes a ~7-fold reduction of catalytic efficiency and a conformational change in the proximity of the mutated residue that is transmitted to the active site. In cellular extracts of E. coli and mammalian cells, both the specific activity and the protein level of the variant decrease with respect to the wild-type. The results with mammalian cells indicate that the mutation does not affect intracellular mRNA levels, and are consistent with a model where S250F undergoes a degradation process via the proteasome, possibly through an ubiquitination process occurring faster than in the wild-type. Overall, biochemical and cell biology experiments show that loss of function of S250F occurs by two distinct but not exclusive mechanisms affecting activity and folding. Importantly, 4-phenylbutirric acid (4-PBA) or, to a major extent, pyridoxine increase the expression level and, in a dose-dependent manner, the decarboxylase specific activity of mutant-expressing cells. This strongly suggests that 4-PBA and/or pyridoxine administration may be of important value in therapy of patients bearing the S250F mutation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Metabolism, Inborn Errors / enzymology
  • Amino Acid Metabolism, Inborn Errors / genetics*
  • Amino Acid Metabolism, Inborn Errors / pathology
  • Animals
  • Aromatic-L-Amino-Acid Decarboxylases / deficiency
  • Aromatic-L-Amino-Acid Decarboxylases / genetics
  • CHO Cells
  • Catalysis
  • Cricetinae
  • Dopa Decarboxylase / chemistry
  • Dopa Decarboxylase / genetics*
  • Dopa Decarboxylase / metabolism
  • Dopamine / biosynthesis
  • Dopamine / metabolism
  • Gene Expression Regulation / drug effects
  • Humans
  • Mutation
  • Polymorphism, Genetic
  • Protein Conformation
  • Proteolysis
  • Pyridoxine / administration & dosage*
  • RNA, Messenger / biosynthesis*
  • RNA, Messenger / genetics
  • Serotonin / biosynthesis
  • Serotonin / metabolism

Substances

  • RNA, Messenger
  • Serotonin
  • Dopa Decarboxylase
  • Aromatic-L-Amino-Acid Decarboxylases
  • Pyridoxine
  • Dopamine

Supplementary concepts

  • Aromatic amino acid decarboxylase deficiency