Comparative kinetic isotope effects on first- and second-order rate constants of soybean lipoxygenase variants uncover a substrate-binding network

J Biol Chem. 2019 Nov 29;294(48):18069-18076. doi: 10.1074/jbc.RA119.010826. Epub 2019 Oct 17.

Abstract

Lipoxygenases are widespread enzymes found in virtually all eukaryotes, including fungi, and, more recently, in prokaryotes. These enzymes act on long-chain polyunsaturated fatty acid substrates (C18 to C20), raising questions regarding how the substrate threads its way from solvent to the active site. Herein, we report a comparison of the temperature dependence of isotope effects on first- and second-order rate constants among single-site variants of the prototypic plant enzyme soybean lipoxygenase-1 substituted at amino acid residues inferred to impact substrate binding. We created 10 protein variants including four amino acid positions, Val-750, Ile-552, Ile-839, and Trp-500, located within a previously proposed substrate portal. The conversion of these bulky hydrophobic side chains to smaller side chains is concluded to increase the mobility of flanking helices, giving rise to increased off rates for substrate dissociation from the enzyme. In this manner, we identified a specific "binding network" that can regulate movement of the substrate from the solvent to the active site. Taken together with our previous findings on C-H and O2 activation of soybean lipoxygenase-1, these results support the emergence of multiple complementary networks within a single protein scaffold that modulate different steps along the enzymatic reaction coordinate.

Keywords: enzyme kinetics; enzyme mechanism; fatty acid binding protein; fatty acid hydroperoxide; intra-protein network; isotope effect; lipoxygenase; site-directed mutagenesis; soybean lipoxygenase (SLO).

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • Catalytic Domain
  • Glycine max / enzymology*
  • Glycine max / genetics
  • Lipoxygenase / chemistry*
  • Lipoxygenase / genetics
  • Mutation, Missense
  • Soybean Proteins / chemistry*
  • Soybean Proteins / genetics

Substances

  • Soybean Proteins
  • Lipoxygenase

Associated data

  • PDB/1F8N