Serotonin-induced stereospecific formation and bioactivity of the eicosanoid 17,18-epoxyeicosatetraenoic acid in the regulation of pharyngeal pumping of C. elegans.


Journal

Biochimica et biophysica acta. Molecular and cell biology of lipids
ISSN: 1879-2618
Titre abrégé: Biochim Biophys Acta Mol Cell Biol Lipids
Pays: Netherlands
ID NLM: 101731727

Informations de publication

Date de publication:
05 2023
Historique:
received: 26 01 2023
revised: 21 02 2023
accepted: 22 02 2023
medline: 28 3 2023
pubmed: 14 3 2023
entrez: 13 3 2023
Statut: ppublish

Résumé

17,18-Epoxyeicosatetraenoic acid (17,18-EEQ), the most abundant eicosanoid generated by cytochrome P450 (CYP) enzymes in C. elegans, is a potential signaling molecule in the regulation of pharyngeal pumping activity of this nematode. As a chiral molecule, 17,18-EEQ can exist in two stereoisomers, the 17(R),18(S)- and 17(S),18(R)-EEQ enantiomers. Here we tested the hypothesis that 17,18-EEQ may function as a second messenger of the feeding-promoting neurotransmitter serotonin and stimulates pharyngeal pumping and food uptake in a stereospecific manner. Serotonin treatment of wildtype worms induced a more than twofold increase of free 17,18-EEQ levels. As revealed by chiral lipidomics analysis, this increase was almost exclusively due to an enhanced release of the (R,S)-enantiomer of 17,18-EEQ. In contrast to the wildtype strain, serotonin failed to induce 17,18-EEQ formation as well as to accelerate pharyngeal pumping in mutant strains defective in the serotonin SER-7 receptor. However, the pharyngeal activity of the ser-7 mutant remained fully responsive to exogenous 17,18-EEQ administration. Short term incubations of well-fed and starved wildtype nematodes showed that both racemic 17,18-EEQ and 17(R),18(S)-EEQ were able to increase pharyngeal pumping frequency and the uptake of fluorescence-labeled microspheres, while 17(S),18(R)-EEQ and also 17,18-dihydroxyeicosatetraenoic acid (17,18-DHEQ, the hydrolysis product of 17,18-EEQ) were ineffective. Taken together, these results show that serotonin induces 17,18-EEQ formation in C. elegans via the SER-7 receptor and that both the formation of this epoxyeicosanoid and its subsequent stimulatory effect on pharyngeal activity proceed with high stereospecificity confined to the (R,S)-enantiomer.

Identifiants

pubmed: 36914111
pii: S1388-1981(23)00028-8
doi: 10.1016/j.bbalip.2023.159304
pii:
doi:

Substances chimiques

17,18-epoxy-5,8,11,14-eicosatetraenoic acid 131339-23-6
Serotonin 333DO1RDJY
Caenorhabditis elegans Proteins 0
Eicosanoids 0
Cytochrome P-450 Enzyme System 9035-51-2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

159304

Informations de copyright

Copyright © 2023 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare no conflict of interest.

Auteurs

Yiwen Zhou (Y)

Humboldt-Universität zu Berlin, Institue of Biology, Ecology, Philippstr. 13, 10115 Berlin, Germany.

Michael Rothe (M)

Lipidomix GmbH, Robert-Rössle-Str. 10, 13125 Berlin, Germany.

Wolf-Hagen Schunck (WH)

Max Delbrück Center for Molecular Medicine, Robert-Rössle-Str. 10, 13125 Berlin, Germany.

Liliane Ruess (L)

Humboldt-Universität zu Berlin, Institue of Biology, Ecology, Philippstr. 13, 10115 Berlin, Germany.

Ralph Menzel (R)

Humboldt-Universität zu Berlin, Institue of Biology, Ecology, Philippstr. 13, 10115 Berlin, Germany. Electronic address: ralph.menzel@biologie.hu-berlin.de.

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Classifications MeSH