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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...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2015
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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 |
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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 |
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