Cargando…

Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body

BACKGROUND: Daily rhythms in mammals are programmed by a master clock in the suprachiasmatic nucleus (SCN). The SCN contains two main compartments (shell and core), but the role of each region in system-level coordination remains ill defined. Herein, we use a functional assay to investigate how down...

Descripción completa

Detalles Bibliográficos
Autores principales: Evans, Jennifer A., Suen, Ting-Chung, Callif, Ben L., Mitchell, Andrew S., Castanon-Cervantes, Oscar, Baker, Kimberly M., Kloehn, Ian, Baba, Kenkichi, Teubner, Brett J. W., Ehlen, J. Christopher, Paul, Ketema N., Bartness, Timothy J., Tosini, Gianluca, Leise, Tanya, Davidson, Alec J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4489020/
https://www.ncbi.nlm.nih.gov/pubmed/26099272
http://dx.doi.org/10.1186/s12915-015-0157-x
_version_ 1782379275474698240
author Evans, Jennifer A.
Suen, Ting-Chung
Callif, Ben L.
Mitchell, Andrew S.
Castanon-Cervantes, Oscar
Baker, Kimberly M.
Kloehn, Ian
Baba, Kenkichi
Teubner, Brett J. W.
Ehlen, J. Christopher
Paul, Ketema N.
Bartness, Timothy J.
Tosini, Gianluca
Leise, Tanya
Davidson, Alec J.
author_facet Evans, Jennifer A.
Suen, Ting-Chung
Callif, Ben L.
Mitchell, Andrew S.
Castanon-Cervantes, Oscar
Baker, Kimberly M.
Kloehn, Ian
Baba, Kenkichi
Teubner, Brett J. W.
Ehlen, J. Christopher
Paul, Ketema N.
Bartness, Timothy J.
Tosini, Gianluca
Leise, Tanya
Davidson, Alec J.
author_sort Evans, Jennifer A.
collection PubMed
description BACKGROUND: Daily rhythms in mammals are programmed by a master clock in the suprachiasmatic nucleus (SCN). The SCN contains two main compartments (shell and core), but the role of each region in system-level coordination remains ill defined. Herein, we use a functional assay to investigate how downstream tissues interpret region-specific outputs by using in vivo exposure to long day photoperiods to temporally dissociate the SCN. We then analyze resulting changes in the rhythms of clocks located throughout the brain and body to examine whether they maintain phase synchrony with the SCN shell or core. RESULTS: Nearly all of the 17 tissues examined in the brain and body maintain phase synchrony with the SCN shell, but not the SCN core, which indicates that downstream oscillators are set by cues controlled specifically by the SCN shell. Interestingly, we also found that SCN dissociation diminished the amplitude of rhythms in core clock gene and protein expression in brain tissues by 50–75 %, which suggests that light-driven changes in the functional organization of the SCN markedly influence the strength of rhythms in downstream tissues. CONCLUSIONS: Overall, our results reveal that body clocks receive time-of-day cues specifically from the SCN shell, which may be an adaptive design principle that serves to maintain system-level phase relationships in a changing environment. Further, we demonstrate that lighting conditions alter the amplitude of the molecular clock in downstream tissues, which uncovers a new form of plasticity that may contribute to seasonal changes in physiology and behavior. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-015-0157-x) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4489020
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-44890202015-07-03 Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body Evans, Jennifer A. Suen, Ting-Chung Callif, Ben L. Mitchell, Andrew S. Castanon-Cervantes, Oscar Baker, Kimberly M. Kloehn, Ian Baba, Kenkichi Teubner, Brett J. W. Ehlen, J. Christopher Paul, Ketema N. Bartness, Timothy J. Tosini, Gianluca Leise, Tanya Davidson, Alec J. BMC Biol Research Article BACKGROUND: Daily rhythms in mammals are programmed by a master clock in the suprachiasmatic nucleus (SCN). The SCN contains two main compartments (shell and core), but the role of each region in system-level coordination remains ill defined. Herein, we use a functional assay to investigate how downstream tissues interpret region-specific outputs by using in vivo exposure to long day photoperiods to temporally dissociate the SCN. We then analyze resulting changes in the rhythms of clocks located throughout the brain and body to examine whether they maintain phase synchrony with the SCN shell or core. RESULTS: Nearly all of the 17 tissues examined in the brain and body maintain phase synchrony with the SCN shell, but not the SCN core, which indicates that downstream oscillators are set by cues controlled specifically by the SCN shell. Interestingly, we also found that SCN dissociation diminished the amplitude of rhythms in core clock gene and protein expression in brain tissues by 50–75 %, which suggests that light-driven changes in the functional organization of the SCN markedly influence the strength of rhythms in downstream tissues. CONCLUSIONS: Overall, our results reveal that body clocks receive time-of-day cues specifically from the SCN shell, which may be an adaptive design principle that serves to maintain system-level phase relationships in a changing environment. Further, we demonstrate that lighting conditions alter the amplitude of the molecular clock in downstream tissues, which uncovers a new form of plasticity that may contribute to seasonal changes in physiology and behavior. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-015-0157-x) contains supplementary material, which is available to authorized users. BioMed Central 2015-06-23 /pmc/articles/PMC4489020/ /pubmed/26099272 http://dx.doi.org/10.1186/s12915-015-0157-x Text en © Evans et al. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Evans, Jennifer A.
Suen, Ting-Chung
Callif, Ben L.
Mitchell, Andrew S.
Castanon-Cervantes, Oscar
Baker, Kimberly M.
Kloehn, Ian
Baba, Kenkichi
Teubner, Brett J. W.
Ehlen, J. Christopher
Paul, Ketema N.
Bartness, Timothy J.
Tosini, Gianluca
Leise, Tanya
Davidson, Alec J.
Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
title Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
title_full Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
title_fullStr Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
title_full_unstemmed Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
title_short Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
title_sort shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4489020/
https://www.ncbi.nlm.nih.gov/pubmed/26099272
http://dx.doi.org/10.1186/s12915-015-0157-x
work_keys_str_mv AT evansjennifera shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT suentingchung shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT callifbenl shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT mitchellandrews shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT castanoncervantesoscar shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT bakerkimberlym shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT kloehnian shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT babakenkichi shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT teubnerbrettjw shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT ehlenjchristopher shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT paulketeman shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT bartnesstimothyj shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT tosinigianluca shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT leisetanya shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody
AT davidsonalecj shellneuronsofthemastercircadianclockcoordinatethephaseoftissueclocksthroughoutthebrainandbody