Quantum dynamics of hydride transfer catalyzed by bimetallic electrophilic catalysis: synchronous motion of Mg(2+) and H(-) in xylose isomerase

J Am Chem Soc. 2002 Jun 26;124(25):7268-9. doi: 10.1021/ja026383d.

Abstract

Xylose isomerase exhibits a bridged-bimetallic active-site motif in which the substrate is bound to two metals connected by a glutamate bridge, and X-ray crystallographic studies suggest that metal movement is involved in the hydride transfer rate-controlling catalytic step. Here we report classical/quantal dynamical simulations of this step that provide new insight into the metal motion. The potential energy surface is calculated by treating xylose with semiempirical molecular orbital theory augmented by a simple valence bond potential and the rest of the system by molecular mechanics. The rate constant for the hydride-transfer step was calculated by ensemble-averaged dynamical simulations including both variational transition-state theory for determination of the statistically averaged dynamical bottleneck and optimized multidimensional tunneling calculations. The dynamics calculations include 25 317 atoms, with quantized vibrational free energy in 89 active-site degrees of freedom, and with 32 atoms moving through static secondary zone transition-state configurations in the quantum tunneling simulation. Our simulations show that the average Mg-Mg distance R increases monotonically as a function of the hydride-transfer progress variable z. The range of the average R along the reaction path is consistent with the X-ray structure, thus providing a dynamical demonstration of the postulated role of Mg in catalysis. We also predicted the primary deuterium kinetic isotope effect (KIE) for the chemical step. We calculated a KIE of 3.8 for xylose at 298 K, which is consistent with somewhat smaller experimentally observed KIEs for glucose substrate at higher temperatures. More than half of our KIE is due to tunneling; neglecting quantum effects on the reaction coordinate reduces the calculated KIE to 1.8.

Publication types

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

MeSH terms

  • Aldose-Ketose Isomerases / chemistry*
  • Aldose-Ketose Isomerases / metabolism
  • Catalysis
  • Computer Simulation
  • Hydrogen / chemistry*
  • Hydrogen / metabolism
  • Kinetics
  • Magnesium / chemistry*
  • Quantum Theory
  • Xylose / chemistry
  • Xylose / metabolism

Substances

  • Hydrogen
  • Xylose
  • Aldose-Ketose Isomerases
  • xylose isomerase
  • Magnesium