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A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide

Sleep, a reversible quiescent state found in both invertebrate and vertebrate animals, disconnects animals from their environment and is highly regulated for coordination with wakeful activities, such as reproduction. The fruit fly, Drosophila melanogaster, has proven to be a valuable model for stud...

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Autores principales: Oh, Yangkyun, Yoon, Sung-Eun, Zhang, Qi, Chae, Hyo-Seok, Daubnerová, Ivana, Shafer, Orie T., Choe, Joonho, Kim, Young-Joon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4204809/
https://www.ncbi.nlm.nih.gov/pubmed/25333796
http://dx.doi.org/10.1371/journal.pbio.1001974
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author Oh, Yangkyun
Yoon, Sung-Eun
Zhang, Qi
Chae, Hyo-Seok
Daubnerová, Ivana
Shafer, Orie T.
Choe, Joonho
Kim, Young-Joon
author_facet Oh, Yangkyun
Yoon, Sung-Eun
Zhang, Qi
Chae, Hyo-Seok
Daubnerová, Ivana
Shafer, Orie T.
Choe, Joonho
Kim, Young-Joon
author_sort Oh, Yangkyun
collection PubMed
description Sleep, a reversible quiescent state found in both invertebrate and vertebrate animals, disconnects animals from their environment and is highly regulated for coordination with wakeful activities, such as reproduction. The fruit fly, Drosophila melanogaster, has proven to be a valuable model for studying the regulation of sleep by circadian clock and homeostatic mechanisms. Here, we demonstrate that the sex peptide receptor (SPR) of Drosophila, known for its role in female reproduction, is also important in stabilizing sleep in both males and females. Mutants lacking either the SPR or its central ligand, myoinhibitory peptide (MIP), fall asleep normally, but have difficulty in maintaining a sleep-like state. Our analyses have mapped the SPR sleep function to pigment dispersing factor (pdf) neurons, an arousal center in the insect brain. MIP downregulates intracellular cAMP levels in pdf neurons through the SPR. MIP is released centrally before and during night-time sleep, when the sleep drive is elevated. Sleep deprivation during the night facilitates MIP secretion from specific brain neurons innervating pdf neurons. Moreover, flies lacking either SPR or MIP cannot recover sleep after the night-time sleep deprivation. These results delineate a central neuropeptide circuit that stabilizes the sleep state by feeding a slow-acting inhibitory input into the arousal system and plays an important role in sleep homeostasis.
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spelling pubmed-42048092014-10-27 A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide Oh, Yangkyun Yoon, Sung-Eun Zhang, Qi Chae, Hyo-Seok Daubnerová, Ivana Shafer, Orie T. Choe, Joonho Kim, Young-Joon PLoS Biol Research Article Sleep, a reversible quiescent state found in both invertebrate and vertebrate animals, disconnects animals from their environment and is highly regulated for coordination with wakeful activities, such as reproduction. The fruit fly, Drosophila melanogaster, has proven to be a valuable model for studying the regulation of sleep by circadian clock and homeostatic mechanisms. Here, we demonstrate that the sex peptide receptor (SPR) of Drosophila, known for its role in female reproduction, is also important in stabilizing sleep in both males and females. Mutants lacking either the SPR or its central ligand, myoinhibitory peptide (MIP), fall asleep normally, but have difficulty in maintaining a sleep-like state. Our analyses have mapped the SPR sleep function to pigment dispersing factor (pdf) neurons, an arousal center in the insect brain. MIP downregulates intracellular cAMP levels in pdf neurons through the SPR. MIP is released centrally before and during night-time sleep, when the sleep drive is elevated. Sleep deprivation during the night facilitates MIP secretion from specific brain neurons innervating pdf neurons. Moreover, flies lacking either SPR or MIP cannot recover sleep after the night-time sleep deprivation. These results delineate a central neuropeptide circuit that stabilizes the sleep state by feeding a slow-acting inhibitory input into the arousal system and plays an important role in sleep homeostasis. Public Library of Science 2014-10-21 /pmc/articles/PMC4204809/ /pubmed/25333796 http://dx.doi.org/10.1371/journal.pbio.1001974 Text en © 2014 Oh et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Oh, Yangkyun
Yoon, Sung-Eun
Zhang, Qi
Chae, Hyo-Seok
Daubnerová, Ivana
Shafer, Orie T.
Choe, Joonho
Kim, Young-Joon
A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide
title A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide
title_full A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide
title_fullStr A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide
title_full_unstemmed A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide
title_short A Homeostatic Sleep-Stabilizing Pathway in Drosophila Composed of the Sex Peptide Receptor and Its Ligand, the Myoinhibitory Peptide
title_sort homeostatic sleep-stabilizing pathway in drosophila composed of the sex peptide receptor and its ligand, the myoinhibitory peptide
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4204809/
https://www.ncbi.nlm.nih.gov/pubmed/25333796
http://dx.doi.org/10.1371/journal.pbio.1001974
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