Lipoxin A4yields an electrophilic 15-oxo metabolite that mediates FPR2 receptor-independent anti-inflammatory signaling

Author:

Koudelka Adolf,Buchan Gregory J.,Cechova Veronika,O’Brien James P.,Liu Heng,Woodcock Steven R.,Mullett Steven J.,Zhang Cheng,Freeman Bruce A.ORCID,Gelhaus Stacy L.ORCID

Abstract

The enzymatic oxidation of arachidonic acid is proposed to yield trihydroxytetraene species (termed lipoxins) that resolve inflammation via ligand activation of the formyl peptide receptor, FPR2. While cell and murine models activate signaling responses to synthetic lipoxins, primarily 5S,6R,15S-trihydroxy-7E,9E,11Z,13E-eicosatetraenoic acid (lipoxin A4, LXA4), there are expanding concerns about the biological formation, detection and signaling mechanisms ascribed to LXA4and related di- and tri-hydroxy ω-6 and ω-3 fatty acids. Herein, the generation and actions of LXA4and its primary 15-oxo metabolite were assessed in control, LPS-activated and arachidonic acid supplemented RAW 264.7 macrophages. Despite protein expression of all enzymes required for LXA4synthesis, both LXA4and its 15-oxo-LXA4metabolite were undetectable. Moreover, synthetic LXA4and the membrane permeable 15-oxo-LXA4methyl ester that is rapidly de-esterified to 15-oxo-LXA4, displayed no ligand activity for the putative LXA4receptor FPR2, as opposed to the FPR2 ligand WKYMVm. Alternatively, 15-oxo-LXA4, an electrophilic α,β-unsaturated ketone, alkylates nucleophilic amino acids such as cysteine to modulate redox-sensitive transcriptional regulatory protein and enzyme function. 15-oxo-LXA4activated nuclear factor (erythroid related factor 2)-like 2 (Nrf2)-regulated gene expression of anti-inflammatory and repair genes and inhibited nuclear factor (NF)-κB-regulated pro-inflammatory mediator expression. LXA4did not impact these macrophage anti-inflammatory and repair responses. In summary, these data show an absence of macrophage LXA4formation and receptor-mediated signaling actions. Rather, if LXA4were present in sufficient concentrations, this, and other more abundant mono- and poly-hydroxylated unsaturated fatty acids can be readily oxidized to electrophilic α,β-unsaturated ketone products that modulate the redox-sensitive cysteine proteome via G-protein coupled receptor-independent mechanisms.

Publisher

Cold Spring Harbor Laboratory

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