Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators

Saini, Camille; Morf, Jörg; Stratmann, Markus; Gos, Pascal; Schibler, Ueli

doi:10.1101/gad.183251.111

Cited by 217 publications

(195 citation statements)

References 55 publications

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“…This regulatory signature was of particular interest given studies in mouse liver which proposed that mouse HSF1 acts as a mediator of daily gene expression rhythms in response to body temperature cycles [9,13]. Moreover, in parallel with its regulation of Hsp genes, HSF1 also controlled the master clock gene mPer2, thus providing a mechanism for temperature entrainment of the molecular circadian oscillator [9,14,15]. The possible existence of a similar temperature entrainment pathway in flies was addressed by behavioural phenotyping of genetic mutations affecting the Drosophila HSF1/HSP90 pathway.…”

Section: Resultsmentioning

confidence: 99%

Temperature-dependent resetting of the molecular circadian oscillator inDrosophila

2014

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Circadian clocks responsible for daily time keeping in a wide range of organisms synchronize to daily temperature cycles via pathways that remain poorly understood. To address this problem from the perspective of the molecular oscillator, we monitored temperature-dependent resetting of four of its core components in the fruitfly Drosophila melanogaster: the transcripts and proteins for the clock genes period ( per) and timeless (tim). The molecular circadian cycle in adult heads exhibited parallel responses to temperature-mediated resetting at the levels of per transcript, tim transcript and TIM protein. Early phase adjustment specific to per transcript rhythms was explained by clockindependent temperature-driven transcription of per. The cold-induced expression of Drosophila per contrasts with the previously reported heatinduced regulation of mammalian Period 2. An altered and more readily reentrainable temperature-synchronized circadian oscillator that featured temperature-driven per transcript rhythms and phase-shifted TIM and PER protein rhythms was found for flies of the 'Tim 4' genotype, which lacked daily tim transcript oscillations but maintained post-transcriptional temperature entrainment of tim expression. The accelerated molecular and behavioural temperature entrainment observed for Tim 4 flies indicates that clock-controlled tim expression constrains the rate of temperature cycle-mediated circadian resetting.

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Section: Resultsmentioning

confidence: 99%

Temperature-dependent resetting of the molecular circadian oscillator inDrosophila

2014

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“…Such (28). Other transcripts were enhanced by sleep and circadian rhythmicity during the biological night (Fig.…”

Section: Forced Desynchrony and The Transcriptome: Alterations In Expmentioning

confidence: 99%

Mistimed sleep disrupts circadian regulation of the human transcriptome

Archer

Laing

Möller-Levet

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

314

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Circadian organization of the mammalian transcriptome is achieved by rhythmic recruitment of key modifiers of chromatin structure and transcriptional and translational processes. These rhythmic processes, together with posttranslational modification, constitute circadian oscillators in the brain and peripheral tissues, which drive rhythms in physiology and behavior, including the sleep-wake cycle. In humans, sleep is normally timed to occur during the biological night, when body temperature is low and melatonin is synthesized. Desynchrony of sleep-wake timing and other circadian rhythms, such as occurs in shift work and jet lag, is associated with disruption of rhythmicity in physiology and endocrinology. However, to what extent mistimed sleep affects the molecular regulators of circadian rhythmicity remains to be established. Here, we show that mistimed sleep leads to a reduction of rhythmic transcripts in the human blood transcriptome from 6.4% at baseline to 1.0% during forced desynchrony of sleep and centrally driven circadian rhythms. Transcripts affected are key regulators of gene expression, including those associated with chromatin modification (methylases and acetylases), transcription (RNA polymerase II), translation (ribosomal proteins, initiation, and elongation factors), temperature-regulated transcription (cold inducible RNA-binding proteins), and core clock genes including CLOCK and ARNTL (BMAL1). We also estimated the separate contribution of sleep and circadian rhythmicity and found that the sleep-wake cycle coordinates the timing of transcription and translation in particular. The data show that mistimed sleep affects molecular processes at the core of circadian rhythm generation and imply that appropriate timing of sleep contributes significantly to the overall temporal organization of the human transcriptome.bloodomics | chronobiology | microarray | genomics | biological rhythms T wenty-four-hour rhythms in physiology and behavior are generated through interaction between environmental cycles and endogenous self-sustained circadian oscillators (1). In mammals, circadian oscillators are present in the brain and most peripheral tissues (2). Circadian rhythmicity within cells in these tissues is generated by a molecular oscillator, which is composed of core transcriptional-translational feedback loops that can also interact with metabolic oscillators (3).The circadian regulation of the mammalian transcriptome includes circadian transcriptional and translational regulation by proteins such as the positive transcription factors CLOCK and ARNTL (BMAL1), and the repressors PERIOD (PER) and CRYPTOCHROME (CRY) (4), chromatin modification by factors such as E1A binding protein P300 (EP300) and the methyltransferase MLL3 (4-6), RNA polymerase activity (4, 7), and posttranscriptional events such as the regulation of ribosome biogenesis and translation (8, 9). Furthermore, physiological factors such as body temperature (10) and endocrine rhythms such as cortisol (11) can modify and reinforce these regulat...

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“…Most animal species exhibit circadian rhythms at many functional levels including gene expression (Vollmers et al 2009), hormonal activity (Kino 2012), body temperature changes (Saini et al 2012), individual behavioral activity (Allada and Chung 2010) and population dynamics (Clairambault et al 2011). neurophysiological correlates of these cycles have also been identified.…”

Section: Comparison Of Circadian Rhythms Between Amphibians and Othermentioning

confidence: 99%

Electroencephalographic signals synchronize with behaviors and are sexually dimorphic during the light–dark cycle in reproductive frogs

et al. 2013

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Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators

Cited by 217 publications

References 55 publications

Temperature-dependent resetting of the molecular circadian oscillator inDrosophila

Temperature-dependent resetting of the molecular circadian oscillator inDrosophila

Mistimed sleep disrupts circadian regulation of the human transcriptome

Electroencephalographic signals synchronize with behaviors and are sexually dimorphic during the light–dark cycle in reproductive frogs

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