Structural and biochemical basis for novel mutations in homozygous Israeli maple syrup urine disease patients: a proposed mechanism for the thiamin-responsive phenotype

J Biol Chem. 2004 Apr 23;279(17):17792-800. doi: 10.1074/jbc.M313879200. Epub 2004 Jan 23.

Abstract

Maple syrup urine disease (MSUD) results from mutations affecting different subunits of the mitochondrial branched-chain alpha-ketoacid dehydrogenase complex. In this study, we identified seven novel mutations in MSUD patients from Israel. These include C219W-alpha (TGC to TGG) in the E1alpha subunit; H156Y-beta (CAT to TAT), V69G-beta (GTT to GGT), IVS 9 del[-7:-4], and 1109 ins 8bp (exon 10) in the E1beta subunit; and H391R (CAC to CGC) and S133stop (TCA to TGA) affecting the E2 subunit of the branched-chain alpha-ketoacid dehydrogenase complex. Recombinant E1 proteins carrying the C219W-alpha or H156Y-beta mutation show no catalytic activity with defective subunit assembly and reduced binding affinity for cofactor thiamin diphosphate. The mutant E1 harboring the V69G-beta substitution cannot be expressed, suggesting aberrant folding caused by this mutation. These E1 mutations are ubiquitously associated with the classic phenotype in homozygous-affected patients. The H391R substitution in the E2 subunit abolishes the key catalytic residue that functions as a general base in the acyltransfer reaction, resulting in a completely inactive E2 component. However, wild-type E1 activity is enhanced by E1 binding to this full-length mutant E2 in vitro. We propose that the augmented E1 activity is responsible for robust thiamin responsiveness in homozygous patients carrying the H391R E2 mutation and that the presence of a full-length mutant E2 is diagnostic of this MSUD phenotype. The present results offer a structural and biochemical basis for these novel mutations and will facilitate DNA-based diagnosis for MSUD in the Israeli population.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Alleles
  • Blotting, Western
  • Centrifugation, Density Gradient
  • DNA, Complementary / metabolism
  • Dose-Response Relationship, Drug
  • Homozygote*
  • Humans
  • Israel
  • Kinetics
  • Maple Syrup Urine Disease / genetics*
  • Methylamines / pharmacology
  • Models, Chemical
  • Models, Molecular
  • Mutation*
  • Phenotype
  • Protein Binding
  • Protein Folding
  • Protein Structure, Tertiary
  • Recombinant Proteins / metabolism
  • Thermodynamics
  • Thiamine / chemistry
  • Thiamine Pyrophosphate / chemistry

Substances

  • DNA, Complementary
  • Methylamines
  • Recombinant Proteins
  • trimethyloxamine
  • Thiamine Pyrophosphate
  • Thiamine