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
Shigeyoshi Y
中科院分区:
生物学2区
文献类型:
--
作者:
Kurosawa G;Fujioka A;Koinuma S;Mochizuki A;Shigeyoshi Y

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大多数生物过程都会随着温度而加速,例如细胞分裂。相反,昼夜节律周期对温度波动具有鲁棒性,称为温度补偿。温度补偿很特殊,因为系统级属性(即昼夜节律)在变化的温度下是稳定的,而系统的各个组件(即生化反应)通常对温度敏感。为了了解周期稳定性的机制,我们测量了培养的 C6 神经胶质瘤细胞中生物钟转录物的时间序列。 Cry1 和 Dbp 昼夜节律表达的幅度随温度显着增加。相比之下,其他时钟转录本的振幅没有显着变化。为了理解这些实验结果,我们分析了具有不同网络拓扑的数学模型。研究发现,对于所有研究的模型,随着温度和反应速度的增加,基因表达的几何平均幅度必须增加才能维持稳定期。为了研究这种温度-振幅耦合机制对周期稳定性的普遍性,我们重新审视了酵母代谢周期(YMC)周期的数据,该周期在温度变化下也是稳定的。我们证实 YMC 振幅在较高温度下增加,表明温度-振幅耦合是昼夜节律和 4 小时代谢节律所共有的共同机制。昼夜节律控制着许多生理事件的发生时间。神秘的是,尽管潜在的生化反应通常会随着温度的升高而加速,但节律的周期对温度却很稳定,这一悖论在 60 多年来一直没有得到解决。过去几十年在昆虫、哺乳动物和植物中进行的实验表明,生物节律是由基因表达的周期性变化控制的。然而,这些节律的调节网络结构的拓扑因物种而异,这表明随温度变化的周期稳定性机制并不保守。但这是真的吗?我们通过将计算模型与不同的网络结构和哺乳动物细胞培养物的实验观察相结合,研究了温度周期稳定性的机制。出乎意料的是,我们发现基因表达的温度敏感幅度(我们称之为“温度-幅度耦合”)可以在所有研究的模型中稳定温度周期,尽管调节网络结构存在差异。因此,昼夜节律稳定性的机制可能是跨物种共享的。
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.