RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans

Abstract Sleep and wakefulness are fundamental behavioral states of which the underlying molecular principles are becoming slowly elucidated. Transitions between these states require the coordination of multiple neurochemical and modulatory systems. In Caenorhabditis elegans sleep occurs during a la...

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Autores principales: Petrus Van der Auwera, Lotte Frooninckx, Kristen Buscemi, Ryan T. Vance, Jan Watteyne, Olivier Mirabeau, Liesbet Temmerman, Wouter De Haes, Luca Fancsalszky, Alexander Gottschalk, David M. Raizen, Matthew D. Nelson, Liliane Schoofs, Isabel Beets
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Publicado: Nature Portfolio 2020
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spelling oai:doaj.org-article:faf1af4379f7461bb1601a19c3f0244f2021-12-02T17:40:44ZRPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans10.1038/s41598-020-66536-22045-2322https://doaj.org/article/faf1af4379f7461bb1601a19c3f0244f2020-06-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-66536-2https://doaj.org/toc/2045-2322Abstract Sleep and wakefulness are fundamental behavioral states of which the underlying molecular principles are becoming slowly elucidated. Transitions between these states require the coordination of multiple neurochemical and modulatory systems. In Caenorhabditis elegans sleep occurs during a larval transition stage called lethargus and is induced by somnogenic neuropeptides. Here, we identify two opposing neuropeptide/receptor signaling pathways: NLP-22 promotes behavioral quiescence, whereas NLP-2 promotes movement during lethargus, by signaling through gonadotropin-releasing hormone (GnRH) related receptors. Both NLP-2 and NLP-22 belong to the RPamide neuropeptide family and share sequence similarities with neuropeptides of the bilaterian GnRH, adipokinetic hormone (AKH) and corazonin family. RPamide neuropeptides dose-dependently activate the GnRH/AKH-like receptors GNRR-3 and GNRR-6 in a cellular receptor activation assay. In addition, nlp-22-induced locomotion quiescence requires the receptor gnrr-6. By contrast, wakefulness induced by nlp-2 overexpression is diminished by deletion of either gnrr-3 or gnrr-6. nlp-2 is expressed in a pair of olfactory AWA neurons and cycles with larval periodicity, as reported for nlp-22, which is expressed in RIA. Our data suggest that the somnogenic NLP-22 neuropeptide signals through GNRR-6, and that both GNRR-3 and GNRR-6 are required for the wake-promoting action of NLP-2 neuropeptides.Petrus Van der AuweraLotte FrooninckxKristen BuscemiRyan T. VanceJan WatteyneOlivier MirabeauLiesbet TemmermanWouter De HaesLuca FancsalszkyAlexander GottschalkDavid M. RaizenMatthew D. NelsonLiliane SchoofsIsabel BeetsNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-15 (2020)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Petrus Van der Auwera
Lotte Frooninckx
Kristen Buscemi
Ryan T. Vance
Jan Watteyne
Olivier Mirabeau
Liesbet Temmerman
Wouter De Haes
Luca Fancsalszky
Alexander Gottschalk
David M. Raizen
Matthew D. Nelson
Liliane Schoofs
Isabel Beets
RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans
description Abstract Sleep and wakefulness are fundamental behavioral states of which the underlying molecular principles are becoming slowly elucidated. Transitions between these states require the coordination of multiple neurochemical and modulatory systems. In Caenorhabditis elegans sleep occurs during a larval transition stage called lethargus and is induced by somnogenic neuropeptides. Here, we identify two opposing neuropeptide/receptor signaling pathways: NLP-22 promotes behavioral quiescence, whereas NLP-2 promotes movement during lethargus, by signaling through gonadotropin-releasing hormone (GnRH) related receptors. Both NLP-2 and NLP-22 belong to the RPamide neuropeptide family and share sequence similarities with neuropeptides of the bilaterian GnRH, adipokinetic hormone (AKH) and corazonin family. RPamide neuropeptides dose-dependently activate the GnRH/AKH-like receptors GNRR-3 and GNRR-6 in a cellular receptor activation assay. In addition, nlp-22-induced locomotion quiescence requires the receptor gnrr-6. By contrast, wakefulness induced by nlp-2 overexpression is diminished by deletion of either gnrr-3 or gnrr-6. nlp-2 is expressed in a pair of olfactory AWA neurons and cycles with larval periodicity, as reported for nlp-22, which is expressed in RIA. Our data suggest that the somnogenic NLP-22 neuropeptide signals through GNRR-6, and that both GNRR-3 and GNRR-6 are required for the wake-promoting action of NLP-2 neuropeptides.
format article
author Petrus Van der Auwera
Lotte Frooninckx
Kristen Buscemi
Ryan T. Vance
Jan Watteyne
Olivier Mirabeau
Liesbet Temmerman
Wouter De Haes
Luca Fancsalszky
Alexander Gottschalk
David M. Raizen
Matthew D. Nelson
Liliane Schoofs
Isabel Beets
author_facet Petrus Van der Auwera
Lotte Frooninckx
Kristen Buscemi
Ryan T. Vance
Jan Watteyne
Olivier Mirabeau
Liesbet Temmerman
Wouter De Haes
Luca Fancsalszky
Alexander Gottschalk
David M. Raizen
Matthew D. Nelson
Liliane Schoofs
Isabel Beets
author_sort Petrus Van der Auwera
title RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans
title_short RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans
title_full RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans
title_fullStr RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans
title_full_unstemmed RPamide neuropeptides NLP-22 and NLP-2 act through GnRH-like receptors to promote sleep and wakefulness in C. elegans
title_sort rpamide neuropeptides nlp-22 and nlp-2 act through gnrh-like receptors to promote sleep and wakefulness in c. elegans
publisher Nature Portfolio
publishDate 2020
url https://doaj.org/article/faf1af4379f7461bb1601a19c3f0244f
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