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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Main Authors: Gen Kurosawa, Atsuko Fujioka, Satoshi Koinuma, Atsushi Mochizuki, Yasufumi Shigeyoshi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-06-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC5464531?pdf=render
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spelling doaj-e8c33782832e4c7eb22ea0572547bb952020-11-25T02:20:15ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582017-06-01136e100550110.1371/journal.pcbi.1005501Temperature-amplitude coupling for stable biological rhythms at different temperatures.Gen KurosawaAtsuko FujiokaSatoshi KoinumaAtsushi MochizukiYasufumi ShigeyoshiMost 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.http://europepmc.org/articles/PMC5464531?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Gen Kurosawa
Atsuko Fujioka
Satoshi Koinuma
Atsushi Mochizuki
Yasufumi Shigeyoshi
spellingShingle Gen Kurosawa
Atsuko Fujioka
Satoshi Koinuma
Atsushi Mochizuki
Yasufumi Shigeyoshi
Temperature-amplitude coupling for stable biological rhythms at different temperatures.
PLoS Computational Biology
author_facet Gen Kurosawa
Atsuko Fujioka
Satoshi Koinuma
Atsushi Mochizuki
Yasufumi Shigeyoshi
author_sort Gen Kurosawa
title Temperature-amplitude coupling for stable biological rhythms at different temperatures.
title_short 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_sort temperature-amplitude coupling for stable biological rhythms at different temperatures.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2017-06-01
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.
url http://europepmc.org/articles/PMC5464531?pdf=render
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AT satoshikoinuma temperatureamplitudecouplingforstablebiologicalrhythmsatdifferenttemperatures
AT atsushimochizuki temperatureamplitudecouplingforstablebiologicalrhythmsatdifferenttemperatures
AT yasufumishigeyoshi temperatureamplitudecouplingforstablebiologicalrhythmsatdifferenttemperatures
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