Revising the structure of a new eicosanoid from human platelets to 8,9-11,12-diepoxy-13-hydroxyeicosadienoic acid

J Biol Chem. 2019 Jun 7;294(23):9225-9238. doi: 10.1074/jbc.RA119.008915. Epub 2019 May 6.

Abstract

Eicosanoids are critical mediators of fever, pain, and inflammation generated by immune and tissue cells. We recently described a new bioactive eicosanoid generated by cyclooxygenase-1 (COX-1) turnover during platelet activation that can stimulate human neutrophil integrin expression. On the basis of mass spectrometry (MS/MS and MS3), stable isotope labeling, and GC-MS analysis, we previously proposed a structure of 8-hydroxy-9,11-dioxolane eicosatetraenoic acid (DXA3). Here, we achieved enzymatic synthesis and 1H NMR characterization of this compound with results in conflict with the previously proposed structural assignment. Accordingly, by using LC-MS, we screened autoxidation reactions of 11-hydroperoxy-eicosatetraenoic acid (11-HpETE) and thereby identified a candidate sharing the precise reverse-phase chromatographic and MS characteristics of the platelet product. We optimized these methods to increase yield, allowing full structural analysis by 1H NMR. The revised assignment is presented here as 8,9-11,12-diepoxy-13-hydroxyeicosadienoic acid, abbreviated to 8,9-11,12-DiEp-13-HEDE or DiEpHEDE, substituted for the previous name DXA3 We found that in platelets, the lipid likely forms via dioxolane ring opening with rearrangement to the diepoxy moieties followed by oxygen insertion at C13. We present its enzymatic biosynthetic pathway and MS/MS fragmentation pattern and, using the synthetic compound, demonstrate that it has bioactivity. For the platelet lipid, we estimate 16 isomers based on our current knowledge (and four isomers for the synthetic lipid). Determining the exact isomeric structure of the platelet lipid remains to be undertaken.

Keywords: 8,9–11,12-diepoxy-13-hydroxyeicosadienoic acid (8,9–11,12-DiEp-13-HEDE); 8-hydroxy-9,11-dioxolane eicosatetraenoic acid (DXA3); DiEpHEDE; cyclooxygenase (COX); eicosanoid; immunity; leukocyte-regulating lipid; lipid; lipid metabolism; platelet.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blood Platelets / metabolism*
  • Chromatography, High Pressure Liquid
  • Cyclooxygenase 1 / metabolism
  • Eicosanoids / analysis
  • Eicosanoids / chemistry*
  • Gas Chromatography-Mass Spectrometry
  • Humans
  • Hydroxyeicosatetraenoic Acids / analysis
  • Hydroxyeicosatetraenoic Acids / chemical synthesis
  • Hydroxyeicosatetraenoic Acids / chemistry*
  • Isomerism
  • Magnetic Resonance Spectroscopy
  • Molecular Conformation
  • Tandem Mass Spectrometry

Substances

  • Eicosanoids
  • Hydroxyeicosatetraenoic Acids
  • Cyclooxygenase 1