Enzymatic C4-Epimerization of UDP-Glucuronic Acid: Precisely Steered Rotation of a Transient 4-Keto Intermediate for an Inverted Reaction without Decarboxylation

Angew Chem Int Ed Engl. 2023 Jan 23;62(4):e202211937. doi: 10.1002/anie.202211937. Epub 2022 Dec 15.

Abstract

UDP-glucuronic acid (UDP-GlcA) 4-epimerase illustrates an important problem regarding enzyme catalysis: balancing conformational flexibility with precise positioning. The enzyme coordinates the C4-oxidation of the substrate by NAD+ and rotation of a decarboxylation-prone β-keto acid intermediate in the active site, enabling stereoinverting reduction of the keto group by NADH. We reveal the elusive rotational landscape of the 4-keto intermediate. Distortion of the sugar ring into boat conformations induces torsional mobility in the enzyme's binding pocket. The rotational endpoints show that the 4-keto sugar has an undistorted 4 C1 chair conformation. The equatorially placed carboxylate group disfavors decarboxylation of the 4-keto sugar. Epimerase variants lead to decarboxylation upon removal of the binding interactions with the carboxylate group in the opposite rotational isomer of the substrate. Substitutions R185A/D convert the epimerase into UDP-xylose synthases that decarboxylate UDP-GlcA in stereospecific, configuration-retaining reactions.

Keywords: Carbohydrates; Enzyme Catalysis; Epimerase; QM/MM; UDP-Glucuronic Acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Decarboxylation
  • Glucuronic Acid
  • Ketoses
  • NAD / chemistry
  • Racemases and Epimerases* / metabolism
  • Rotation
  • Uridine Diphosphate Glucuronic Acid* / metabolism

Substances

  • Uridine Diphosphate Glucuronic Acid
  • Glucuronic Acid
  • Racemases and Epimerases
  • Ketoses
  • NAD