Biosynthesis of a linoleic acid allylic epoxide: mechanistic comparison with its chemical synthesis and leukotriene A biosynthesis

J Lipid Res. 2009 Jul;50(7):1448-55. doi: 10.1194/jlr.M900025-JLR200. Epub 2009 Feb 24.

Abstract

Biosynthesis of the leukotriene A (LTA) class of epoxide is a lipoxygenase-catalyzed transformation requiring a fatty acid hydroperoxide substrate containing at least three double bonds. Here, we report on biosynthesis of a dienoic analog of LTA epoxides via a different enzymatic mechanism. Beginning with homolytic cleavage of the hydroperoxide moiety, a catalase/peroxidase-related hemoprotein from Anabaena PCC 7120, which occurs in a fusion protein with a linoleic acid 9R-lipoxygenase, dehydrates 9R-hydroperoxylinoleate to a highly unstable epoxide. Using methods we developed for isolating extremely labile compounds, we prepared and purified the epoxide and characterized its structure as 9R,10R-epoxy-octadeca-11E,13E-dienoate. This epoxide hydrolyzes to stable 9,14-diols that were reported before in linoleate autoxidation (Hamberg, M. 1983. Autoxidation of linoleic acid: Isolation and structure of four dihydroxy octadecadienoic acids. Biochim. Biophys. Acta 752: 353-356) and in incubations with the Anabaena enzyme (Lang, I., C. Göbel, A. Porzel, I. Heilmann, and I. Feussner. 2008. A lipoxygenase with linoleate diol synthase activity from Nostoc sp. PCC 7120. Biochem. J. 410: 347-357). We also prepared an equivalent epoxide from 13S-hydroperoxylinoleate using a "biomimetic" chemical method originally described for LTA(4) synthesis and showed that like LTA(4), the C18.2 epoxide conjugates readily with glutathione, a potential metabolic fate in vivo. We compare and contrast the mechanisms of LTA-type allylic epoxide synthesis by lipoxygenase, catalase/peroxidase, and chemical transformations. These findings provide new insights into the reactions of linoleic acid hydroperoxides and extend the known range of catalytic activities of catalase-related hemoproteins.

Publication types

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

MeSH terms

  • Anabaena / chemistry
  • Anabaena / enzymology*
  • Anabaena / genetics
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Catalase / genetics
  • Catalase / metabolism
  • Epoxy Compounds* / chemical synthesis
  • Epoxy Compounds* / chemistry
  • Epoxy Compounds* / metabolism
  • Glutathione / metabolism
  • Leukotriene A4 / biosynthesis*
  • Linoleic Acid* / biosynthesis
  • Linoleic Acid* / chemical synthesis
  • Linoleic Acid* / chemistry
  • Lipoxygenase / genetics
  • Lipoxygenase / metabolism
  • Molecular Structure
  • Nuclear Magnetic Resonance, Biomolecular
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism

Substances

  • Bacterial Proteins
  • Epoxy Compounds
  • Leukotriene A4
  • Recombinant Fusion Proteins
  • Linoleic Acid
  • Catalase
  • Lipoxygenase
  • Glutathione