Extremely elevated room-temperature kinetic isotope effects quantify the critical role of barrier width in enzymatic C-H activation

J Am Chem Soc. 2014 Jun 11;136(23):8157-60. doi: 10.1021/ja502726s. Epub 2014 Jun 2.

Abstract

The enzyme soybean lipoxygenase (SLO) has served as a prototype for hydrogen-tunneling reactions, as a result of its unusual kinetic isotope effects (KIEs) and their temperature dependencies. Using a synergy of kinetic, structural, and theoretical studies, we show how the interplay between donor-acceptor distance and active-site flexibility leads to catalytic behavior previously predicted by quantum tunneling theory. Modification of the size of two hydrophobic residues by site-specific mutagenesis in SLO reduces the reaction rate 10(4)-fold and is accompanied by an enormous and unprecedented room-temperature KIE. Fitting of the kinetic data to a non-adiabatic model implicates an expansion of the active site that cannot be compensated by donor-acceptor distance sampling. A 1.7 Å resolution X-ray structure of the double mutant further indicates an unaltered backbone conformation, almost identical side-chain conformations, and a significantly enlarged active-site cavity. These findings show the compelling property of room-temperature hydrogen tunneling within a biological context and demonstrate the very high sensitivity of such tunneling to barrier width.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Binding Sites
  • Carbon / chemistry*
  • Catalysis
  • Computer Simulation
  • Electron Transport
  • Enzyme Activation
  • Glycine max / enzymology
  • Hydrogen / chemistry*
  • Isotopes / chemistry
  • Kinetics
  • Linoleic Acids / chemistry
  • Lipoxygenase / chemistry*
  • Lipoxygenase / genetics
  • Lipoxygenase / metabolism*
  • Models, Molecular
  • Mutation
  • Protein Conformation
  • Quantum Theory
  • Substrate Specificity
  • Temperature

Substances

  • Isotopes
  • Linoleic Acids
  • Carbon
  • Hydrogen
  • Lipoxygenase