Tetrahedral intermediates in thiamin diphosphate-dependent decarboxylations exist as a 1',4'-imino tautomeric form of the coenzyme, unlike the michaelis complex or the free coenzyme

Biochemistry. 2004 Jun 1;43(21):6565-75. doi: 10.1021/bi049549r.

Abstract

Two circular dichroism signals observed on thiamin diphosphate (ThDP)-dependent enzymes, a positive band in the 300-305 nm range and a negative one in the 320-330 nm range, were investigated on yeast pyruvate decarboxylase (YPDC) and on the E1 subunit of the Escherichia coli pyruvate dehydrogenase complex (PDHc-E1). Addition of the tetrahedral ThDP-acetaldehyde adduct, 2-alpha-hydroxyethylThDP, to PDHc-E1 generates the positive band at 300 nm, consistent with the formation of the 1',4'-iminopyrimidine tautomer, as also demonstrated for phosphonolactylthiamin diphosphate, a stable analogue of the tetrahedral ThDP-pyruvate adduct 2-alpha-lactylThDP (Jordan, F. et al. (2003) J. Am. Chem. Soc. 125, 12732-12738). Therefore, we suggest that all tetrahedral ThDP-bound covalent complexes will also prefer this tautomer, and that the 4'-aminopyrimidine of ThDP participates in multiple steps of acid-base catalysis on ThDP enzymes. Studies with YPDC and PDHc-E1, and their active center variants, in conjunction with chemical models, enabled assignment of the negative band at 330 nm to a charge-transfer transition between the 4'-aminopyrimidine tautomer (presumed electron donor) and the thiazolium ring (presumed electron acceptor) of ThDP, with no significant contributions from any amino acid side chain of the proteins. However, in both YPDC and PDHc-E1, the presence of substrate or substrate surrogate was required to enable detection, suggesting that the band at 320-330 nm be used as a reporter for the Michaelis complex, involving the amino tautomer, on both enzymes. As the positive band near 300 nm reports on the 1',4'-imino tautomer of ThDP, methods are now available for kinetic monitoring of both tautomeric forms.

Publication types

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

MeSH terms

  • Binding Sites
  • Catalysis
  • Circular Dichroism
  • Coenzymes / chemistry*
  • Coenzymes / metabolism*
  • Decarboxylation
  • Fungal Proteins / chemistry
  • Fungal Proteins / metabolism
  • Models, Chemical
  • Models, Molecular
  • Phosphonoacetic Acid / analogs & derivatives*
  • Phosphonoacetic Acid / chemistry
  • Point Mutation
  • Protein Conformation
  • Pyruvate Decarboxylase / chemistry
  • Pyruvate Decarboxylase / metabolism
  • Pyruvate Dehydrogenase Complex / chemistry
  • Pyruvate Dehydrogenase Complex / genetics
  • Pyruvate Dehydrogenase Complex / metabolism
  • Thiamine Pyrophosphate / chemistry*
  • Thiamine Pyrophosphate / metabolism
  • Titrimetry

Substances

  • Coenzymes
  • Fungal Proteins
  • Pyruvate Dehydrogenase Complex
  • pyruvate dehydrogenase multienzyme complex E1
  • methylacetylphosphonate
  • Pyruvate Decarboxylase
  • Phosphonoacetic Acid
  • Thiamine Pyrophosphate