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Temperature–amplitude coupling for stable biological rhythms at different temperatures

Most biological processes accelerate with temperature, for example cell division. In contrast, the circadian rhythm period is robust to temperature fluctuation, termed temperature compensation. Temperature compensation is peculiar because a system-level property (i.e., the circadian period) is stabl...

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Autores principales: Kurosawa, Gen, Fujioka, Atsuko, Koinuma, Satoshi, Mochizuki, Atsushi, Shigeyoshi, Yasufumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5464531/
https://www.ncbi.nlm.nih.gov/pubmed/28594845
http://dx.doi.org/10.1371/journal.pcbi.1005501
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author Kurosawa, Gen
Fujioka, Atsuko
Koinuma, Satoshi
Mochizuki, Atsushi
Shigeyoshi, Yasufumi
author_facet Kurosawa, Gen
Fujioka, Atsuko
Koinuma, Satoshi
Mochizuki, Atsushi
Shigeyoshi, Yasufumi
author_sort Kurosawa, Gen
collection PubMed
description Most biological processes accelerate with temperature, for example cell division. In contrast, the circadian rhythm period is robust to temperature fluctuation, termed temperature compensation. Temperature compensation is peculiar because a system-level property (i.e., the circadian period) is stable under varying temperature while individual components of the system (i.e., biochemical reactions) are usually temperature-sensitive. To understand the mechanism for period stability, we measured the time series of circadian clock transcripts in cultured C6 glioma cells. The amplitudes of Cry1 and Dbp circadian expression increased significantly with temperature. In contrast, other clock transcripts demonstrated no significant change in amplitude. To understand these experimental results, we analyzed mathematical models with different network topologies. It was found that the geometric mean amplitude of gene expression must increase to maintain a stable period with increasing temperatures and reaction speeds for all models studied. To investigate the generality of this temperature–amplitude coupling mechanism for period stability, we revisited data on the yeast metabolic cycle (YMC) period, which is also stable under temperature variation. We confirmed that the YMC amplitude increased at higher temperatures, suggesting temperature-amplitude coupling as a common mechanism shared by circadian and 4 h-metabolic rhythms.
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spelling pubmed-54645312017-06-22 Temperature–amplitude coupling for stable biological rhythms at different temperatures Kurosawa, Gen Fujioka, Atsuko Koinuma, Satoshi Mochizuki, Atsushi Shigeyoshi, Yasufumi PLoS Comput Biol Research Article Most biological processes accelerate with temperature, for example cell division. In contrast, the circadian rhythm period is robust to temperature fluctuation, termed temperature compensation. Temperature compensation is peculiar because a system-level property (i.e., the circadian period) is stable under varying temperature while individual components of the system (i.e., biochemical reactions) are usually temperature-sensitive. To understand the mechanism for period stability, we measured the time series of circadian clock transcripts in cultured C6 glioma cells. The amplitudes of Cry1 and Dbp circadian expression increased significantly with temperature. In contrast, other clock transcripts demonstrated no significant change in amplitude. To understand these experimental results, we analyzed mathematical models with different network topologies. It was found that the geometric mean amplitude of gene expression must increase to maintain a stable period with increasing temperatures and reaction speeds for all models studied. To investigate the generality of this temperature–amplitude coupling mechanism for period stability, we revisited data on the yeast metabolic cycle (YMC) period, which is also stable under temperature variation. We confirmed that the YMC amplitude increased at higher temperatures, suggesting temperature-amplitude coupling as a common mechanism shared by circadian and 4 h-metabolic rhythms. Public Library of Science 2017-06-08 /pmc/articles/PMC5464531/ /pubmed/28594845 http://dx.doi.org/10.1371/journal.pcbi.1005501 Text en © 2017 Kurosawa 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 (http://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
Kurosawa, Gen
Fujioka, Atsuko
Koinuma, Satoshi
Mochizuki, Atsushi
Shigeyoshi, Yasufumi
Temperature–amplitude coupling for stable biological rhythms at different temperatures
title Temperature–amplitude coupling for stable biological rhythms at different temperatures
title_full Temperature–amplitude coupling for stable biological rhythms at different temperatures
title_fullStr Temperature–amplitude coupling for stable biological rhythms at different temperatures
title_full_unstemmed Temperature–amplitude coupling for stable biological rhythms at different temperatures
title_short Temperature–amplitude coupling for stable biological rhythms at different temperatures
title_sort temperature–amplitude coupling for stable biological rhythms at different temperatures
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5464531/
https://www.ncbi.nlm.nih.gov/pubmed/28594845
http://dx.doi.org/10.1371/journal.pcbi.1005501
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