Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.

Drosophila circadian behavior relies on the network of heterogeneous groups of clock neurons. Short- and long-range signaling within the pacemaker circuit coordinates molecular and neural rhythms of clock neurons to generate coherent behavioral output. The neurochemistry of circadian behavior is com...

Full description

Bibliographic Details
Main Authors: Anatoly Kozlov, Rafael Koch, Emi Nagoshi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-06-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1008312
_version_ 1818735107080454144
author Anatoly Kozlov
Rafael Koch
Emi Nagoshi
author_facet Anatoly Kozlov
Rafael Koch
Emi Nagoshi
author_sort Anatoly Kozlov
collection DOAJ
description Drosophila circadian behavior relies on the network of heterogeneous groups of clock neurons. Short- and long-range signaling within the pacemaker circuit coordinates molecular and neural rhythms of clock neurons to generate coherent behavioral output. The neurochemistry of circadian behavior is complex and remains incompletely understood. Here we demonstrate that the gaseous messenger nitric oxide (NO) is a signaling molecule linking circadian pacemaker to rhythmic locomotor activity. We show that mutants lacking nitric oxide synthase (NOS) have behavioral arrhythmia in constant darkness, although molecular clocks in the main pacemaker neurons are unaffected. Behavioral phenotypes of mutants are due in part to the malformation of neurites of the main pacemaker neurons, s-LNvs. Using cell-type selective and stage-specific gain- and loss-of-function of NOS, we also demonstrate that NO secreted from diverse cellular clusters affect behavioral rhythms. Furthermore, we identify the perineurial glia, one of the two glial subtypes that form the blood-brain barrier, as the major source of NO that regulates circadian locomotor output. These results reveal for the first time the critical role of NO signaling in the Drosophila circadian system and highlight the importance of neuro-glial interaction in the neural circuit output.
first_indexed 2024-12-18T00:15:59Z
format Article
id doaj.art-272ac33cbf7a46cc9d3be9b839c15c6b
institution Directory Open Access Journal
issn 1553-7390
1553-7404
language English
last_indexed 2024-12-18T00:15:59Z
publishDate 2020-06-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Genetics
spelling doaj.art-272ac33cbf7a46cc9d3be9b839c15c6b2022-12-21T21:27:31ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-06-01166e100831210.1371/journal.pgen.1008312Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.Anatoly KozlovRafael KochEmi NagoshiDrosophila circadian behavior relies on the network of heterogeneous groups of clock neurons. Short- and long-range signaling within the pacemaker circuit coordinates molecular and neural rhythms of clock neurons to generate coherent behavioral output. The neurochemistry of circadian behavior is complex and remains incompletely understood. Here we demonstrate that the gaseous messenger nitric oxide (NO) is a signaling molecule linking circadian pacemaker to rhythmic locomotor activity. We show that mutants lacking nitric oxide synthase (NOS) have behavioral arrhythmia in constant darkness, although molecular clocks in the main pacemaker neurons are unaffected. Behavioral phenotypes of mutants are due in part to the malformation of neurites of the main pacemaker neurons, s-LNvs. Using cell-type selective and stage-specific gain- and loss-of-function of NOS, we also demonstrate that NO secreted from diverse cellular clusters affect behavioral rhythms. Furthermore, we identify the perineurial glia, one of the two glial subtypes that form the blood-brain barrier, as the major source of NO that regulates circadian locomotor output. These results reveal for the first time the critical role of NO signaling in the Drosophila circadian system and highlight the importance of neuro-glial interaction in the neural circuit output.https://doi.org/10.1371/journal.pgen.1008312
spellingShingle Anatoly Kozlov
Rafael Koch
Emi Nagoshi
Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.
PLoS Genetics
title Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.
title_full Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.
title_fullStr Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.
title_full_unstemmed Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.
title_short Nitric oxide mediates neuro-glial interaction that shapes Drosophila circadian behavior.
title_sort nitric oxide mediates neuro glial interaction that shapes drosophila circadian behavior
url https://doi.org/10.1371/journal.pgen.1008312
work_keys_str_mv AT anatolykozlov nitricoxidemediatesneuroglialinteractionthatshapesdrosophilacircadianbehavior
AT rafaelkoch nitricoxidemediatesneuroglialinteractionthatshapesdrosophilacircadianbehavior
AT eminagoshi nitricoxidemediatesneuroglialinteractionthatshapesdrosophilacircadianbehavior