Temperature-amplitude coupling for stable biological rhythms at different temperatures.
Temperature-amplitude coupling for stable biological rhythms at different temperatures.
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DOI:
10.1371/journal.pcbi.1005501
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发表时间:
2017-06
影响因子:
4.3
通讯作者:
Shigeyoshi Y
中科院分区:
文献类型:
--
作者:
Kurosawa G;Fujioka A;Koinuma S;Mochizuki A;Shigeyoshi Y
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. Circadian rhythms govern the timing of many physiological events. Mysteriously, the period of the rhythm is robust to temperature although the underlying biochemical reactions usually accelerate with temperature, a paradox that has remained unsolved for more than 60 years. Experiments conducted over the last few decades in insects, mammals, and plants have demonstrated that biological rhythms are governed by cyclical changes in gene expression. However, the topologies of the regulatory network structures for these rhythms differ between species, suggesting that the mechanisms for period stability with temperature are not conserved. But is it true? We examined the mechanisms for period stability with temperature by combining computational models with distinct network structures and experimental observations from mammalian cell cultures. Unexpectedly, we found that temperature-sensitive amplitude of gene expression, which we call "temperature–amplitude coupling," can stabilize the period with temperature in all models studied, despite differences in regulatory network structures. Thus, the mechanisms for circadian period stability may be shared across species.