A G316A mutation of manganese lipoxygenase augments hydroperoxide isomerase activity: mechanism of biosynthesis of epoxyalcohols

J Biol Chem. 2006 Jun 30;281(26):17612-23. doi: 10.1074/jbc.M510311200. Epub 2006 Apr 26.

Abstract

Lipoxygenases with R stereospecificity have a conserved Gly residue, whereas (S)-lipoxygenases have an Ala residue. Site-directed mutagenesis has shown that these residues control position and S/R stereospecificity of oxygenation. Recombinant Mn-LO was expressed in Pichia pastoris, and its conserved Gly-316 residue was mutated to Ala, Ser, Val, and Thr. The G316A mutant was catalytically active. We compared the catalytic properties of Mn-LO and the G316A mutant with 17:3n-3, 18:2n-6, 18:3n-3, and 19:3n-3 as substrates. Increasing the fatty acid chain length from C17 to C19 shifted the oxygenation by Mn-LO from the n-6 toward the n-8 carbon. The G316A mutant increased the oxygenation at the n-8 carbon of 17:3n-3 and at the n-10 carbon of the C17 and C18 fatty acids (from 1-2% to 7-11%). The most striking effect of the G316A mutant was a 2-, 7-, and 15-fold increase in transformation of the n-6 hydroperoxides of 19:3n-3, 18:3n-3, and 17:3n-3, respectively, to keto fatty acids and epoxyalcohols. The n-3 double bond was essential. An experiment under an oxygen-18 atmosphere showed that both oxygen atoms were retained in the epoxyalcohols. (R)-Hydroperoxides at n-6 of C17:3, 18:3, and 19:3 were transformed 5 times faster than S stereoisomers. The G316A mutant converted (13R)-hydroperoxylinolenic acid to 13-ketolinolenic acid (with an apparent K(m) of 0.01 mm) and to epoxyalcohols (viz. erythro- and threo-11-hydroxy-(12R,13R)-epoxy-(9Z,15Z)-octadecadienoic acids and one of the corresponding cis-epoxides as major products). A reducing lipoxygenase inhibitor stimulated the hydroperoxide isomerase activity, whereas a suicide-type lipoxygenase inhibitor reduced this activity. The n-3 double bond also appeared to influence the anaerobic formation of epoxyalcohols by Mn-LO, since 18:2n-6 and 18:3n-3 yielded different profiles of epoxyalcohols. Our results suggest that the G316A mutant augmented the hydroperoxide isomerase activity by positioning the hydroperoxy group at the n-6 carbon of n-3 fatty acids closer to the reduced catalytic metal.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alcohols / metabolism*
  • Amino Acid Sequence
  • Anaerobiosis
  • Animals
  • Conserved Sequence
  • Enzyme Activation / physiology
  • Epoxy Compounds / metabolism*
  • Fatty Acids, Omega-3 / metabolism
  • Hemin / metabolism
  • Humans
  • Intramolecular Oxidoreductases / metabolism*
  • Lipid Peroxides / metabolism
  • Lipoxygenase / chemistry
  • Lipoxygenase / genetics*
  • Lipoxygenase / metabolism*
  • Mice
  • Mutagenesis, Site-Directed
  • Oxygen / metabolism
  • Pichia
  • Stereoisomerism
  • Substrate Specificity
  • alpha-Linolenic Acid / metabolism

Substances

  • Alcohols
  • Epoxy Compounds
  • Fatty Acids, Omega-3
  • Lipid Peroxides
  • alpha-Linolenic Acid
  • Hemin
  • manganese lipoxygenase
  • Lipoxygenase
  • Intramolecular Oxidoreductases
  • hydroperoxide isomerase
  • Oxygen