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Slowpoke functions in circadian output cells to regulate rest:activity rhythms

The circadian system produces ~24-hr oscillations in behavioral and physiological processes to ensure that they occur at optimal times of day and in the correct temporal order. At its core, the circadian system is composed of dedicated central clock neurons that keep time through a cell-autonomous m...

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Autores principales: Ruiz, Daniela, Bajwa, Saffia T., Vanani, Naisarg, Bajwa, Tanvir A., Cavanaugh, Daniel J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7993846/
https://www.ncbi.nlm.nih.gov/pubmed/33765072
http://dx.doi.org/10.1371/journal.pone.0249215
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author Ruiz, Daniela
Bajwa, Saffia T.
Vanani, Naisarg
Bajwa, Tanvir A.
Cavanaugh, Daniel J.
author_facet Ruiz, Daniela
Bajwa, Saffia T.
Vanani, Naisarg
Bajwa, Tanvir A.
Cavanaugh, Daniel J.
author_sort Ruiz, Daniela
collection PubMed
description The circadian system produces ~24-hr oscillations in behavioral and physiological processes to ensure that they occur at optimal times of day and in the correct temporal order. At its core, the circadian system is composed of dedicated central clock neurons that keep time through a cell-autonomous molecular clock. To produce rhythmic behaviors, time-of-day information generated by clock neurons must be transmitted across output pathways to regulate the downstream neuronal populations that control the relevant behaviors. An understanding of the manner through which the circadian system enacts behavioral rhythms therefore requires the identification of the cells and molecules that make up the output pathways. To that end, we recently characterized the Drosophila pars intercerebralis (PI) as a major circadian output center that lies downstream of central clock neurons in a circuit controlling rest:activity rhythms. We have conducted single-cell RNA sequencing (scRNAseq) to identify potential circadian output genes expressed by PI cells, and used cell-specific RNA interference (RNAi) to knock down expression of ~40 of these candidate genes selectively within subsets of PI cells. We demonstrate that knockdown of the slowpoke (slo) potassium channel in PI cells reliably decreases circadian rest:activity rhythm strength. Interestingly, slo mutants have previously been shown to have aberrant rest:activity rhythms, in part due to a necessary function of slo within central clock cells. However, rescue of slo in all clock cells does not fully reestablish behavioral rhythms, indicating that expression in non-clock neurons is also necessary. Our results demonstrate that slo exerts its effects in multiple components of the circadian circuit, including PI output cells in addition to clock neurons, and we hypothesize that it does so by contributing to the generation of daily neuronal activity rhythms that allow for the propagation of circadian information throughout output circuits.
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spelling pubmed-79938462021-04-05 Slowpoke functions in circadian output cells to regulate rest:activity rhythms Ruiz, Daniela Bajwa, Saffia T. Vanani, Naisarg Bajwa, Tanvir A. Cavanaugh, Daniel J. PLoS One Research Article The circadian system produces ~24-hr oscillations in behavioral and physiological processes to ensure that they occur at optimal times of day and in the correct temporal order. At its core, the circadian system is composed of dedicated central clock neurons that keep time through a cell-autonomous molecular clock. To produce rhythmic behaviors, time-of-day information generated by clock neurons must be transmitted across output pathways to regulate the downstream neuronal populations that control the relevant behaviors. An understanding of the manner through which the circadian system enacts behavioral rhythms therefore requires the identification of the cells and molecules that make up the output pathways. To that end, we recently characterized the Drosophila pars intercerebralis (PI) as a major circadian output center that lies downstream of central clock neurons in a circuit controlling rest:activity rhythms. We have conducted single-cell RNA sequencing (scRNAseq) to identify potential circadian output genes expressed by PI cells, and used cell-specific RNA interference (RNAi) to knock down expression of ~40 of these candidate genes selectively within subsets of PI cells. We demonstrate that knockdown of the slowpoke (slo) potassium channel in PI cells reliably decreases circadian rest:activity rhythm strength. Interestingly, slo mutants have previously been shown to have aberrant rest:activity rhythms, in part due to a necessary function of slo within central clock cells. However, rescue of slo in all clock cells does not fully reestablish behavioral rhythms, indicating that expression in non-clock neurons is also necessary. Our results demonstrate that slo exerts its effects in multiple components of the circadian circuit, including PI output cells in addition to clock neurons, and we hypothesize that it does so by contributing to the generation of daily neuronal activity rhythms that allow for the propagation of circadian information throughout output circuits. Public Library of Science 2021-03-25 /pmc/articles/PMC7993846/ /pubmed/33765072 http://dx.doi.org/10.1371/journal.pone.0249215 Text en © 2021 Ruiz et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ruiz, Daniela
Bajwa, Saffia T.
Vanani, Naisarg
Bajwa, Tanvir A.
Cavanaugh, Daniel J.
Slowpoke functions in circadian output cells to regulate rest:activity rhythms
title Slowpoke functions in circadian output cells to regulate rest:activity rhythms
title_full Slowpoke functions in circadian output cells to regulate rest:activity rhythms
title_fullStr Slowpoke functions in circadian output cells to regulate rest:activity rhythms
title_full_unstemmed Slowpoke functions in circadian output cells to regulate rest:activity rhythms
title_short Slowpoke functions in circadian output cells to regulate rest:activity rhythms
title_sort slowpoke functions in circadian output cells to regulate rest:activity rhythms
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7993846/
https://www.ncbi.nlm.nih.gov/pubmed/33765072
http://dx.doi.org/10.1371/journal.pone.0249215
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