The Circadian Clock Coordinates Ribosome Biogenesis

Jouffe, Céline; Cretenet, Gaspard; Symul, Laura; Martín, Eva; Atger, Florian; Naef, Félix; Gachon, Frédéric

doi:10.1371/journal.pbio.1001455

Cited by 262 publications

(331 citation statements)

References 94 publications

(109 reference statements)

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“…As anticipated, circadian clock genes show rhythms at all stages, from their respective pre-mRNAs to the accumulation of the mRNA and downstream mRNA translation (Fig. 2B), confirming that translational regulation has a minor impact upon clock gene expression (12). To assess and quantify rhythmic regulations at the different steps, we developed computational models and classified genes depending on the rhythmic or constant behavior at each measured level (pre-mRNA, mRNA, and ribosome footprints) (Dataset S1).…”

Section: Resultssupporting

confidence: 81%

“…During the last decades, efforts have been made to produce a comprehensive knowledge of the transcriptional regulation orchestrated by the circadian clock (7)(8)(9) and feeding rhythms (10,11). More recently, additional layers of regulation at the translational (12,13) and posttranslational (14) levels have been described, increasing the complexity of the phenomenon involved in the establishment of the rhythmic mRNA expression and protein synthesis landscapes.…”

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confidence: 99%

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Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

Atger

Gobet

Marquis

et al. 2015

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

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212

287

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Diurnal oscillations of gene expression are a hallmark of rhythmic physiology across most living organisms. Such oscillations are controlled by the interplay between the circadian clock and feeding rhythms. Although rhythmic mRNA accumulation has been extensively studied, comparatively less is known about their transcription and translation. Here, we quantified simultaneously temporal transcription, accumulation, and translation of mouse liver mRNAs under physiological light-dark conditions and ad libitum or night-restricted feeding in WT and brain and muscle Arnt-like 1 (Bmal1)-deficient animals. We found that rhythmic transcription predominantly drives rhythmic mRNA accumulation and translation for a majority of genes. Comparison of wild-type and Bmal1 KO mice shows that circadian clock and feeding rhythms have broad impact on rhythmic gene expression, Bmal1 deletion affecting surprisingly both transcriptional and posttranscriptional levels. Translation efficiency is differentially regulated during the diurnal cycle for genes with 5′-Terminal Oligo Pyrimidine tract (5′-TOP) sequences and for genes involved in mitochondrial activity, many harboring a Translation Initiator of Short 5′-UTR (TISU) motif. The increased translation efficiency of 5′-TOP and TISU genes is mainly driven by feeding rhythms but Bmal1 deletion also affects amplitude and phase of translation, including TISU genes. Together this study emphasizes the complex interconnections between circadian and feeding rhythms at several steps ultimately determining rhythmic gene expression and translation.circadian rhythms | ribosome profiling | mRNA translation | 5′-TOP sequences | TISU motifs L iving organisms on Earth are subjected to light-dark cycles caused by rotation of the Earth around the sun. To anticipate these changes, virtually all organisms have acquired a circadian timing system during evolution that allows a better adaptation to their environment. As a consequence, most aspects of their physiology are orchestrated in a rhythmic way by the circadian clock (from the Latin circa diem, meaning "about a day"), an endogenous and autonomous oscillator with a period of around 24 h (1, 2). Not surprisingly, perturbations of this clock in mammals lead to pathologies including psychiatric, metabolic, and vascular disorders (1,3,4). At the organismal scale, the oscillatory clockwork is organized in a hierarchal manner. Within the suprachiasmatic nuclei (SCN) of the hypothalamus, the "master clock" receives light input via the retina and communicates timing signals to "enslave" oscillators in peripheral organs (1, 2). The molecular oscillator consists of interconnected transcriptional and translational feedback loops, in which multiple layers of control, including temporal posttranscriptional and posttranslational regulation, play important roles (5). These additional layers of regulation are largely coordinated by systemic cues originating from circadian clock and/or feeding-coordinated rhythmic metabolism, allowing the adjustment of the molecular clo...

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Section: Resultssupporting

confidence: 81%

mentioning

confidence: 99%

Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

Atger

Gobet

Marquis

et al. 2015

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

Self Cite

212

287

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“…Although the central circadian clock, as indexed by melatonin, remained largely unaffected, the temporal organization of expression of clock genes considered to be central to circadian rhythm generation was affected in the blood transcriptome, with only NR1D2 and CSNK1E remaining rhythmic when sleeping out of phase. Histone modification, and the control of transcription and translation (4)(5)(6)(7)(8)(9), is also considered central to circadian organization of the transcriptome and the time courses of transcripts associated with all of these processes were affected in this study (Fig. 3).…”

Section: Transcripts and Associated Molecular Processes Affected By Dmentioning

confidence: 72%

“…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 regulatory processes.…”

mentioning

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.

327

317

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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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“…15 The gene for prolactin, for example, was reported to display dynamic expression and pulsating transcription with implications for cellular differentiation. 16 Jouffe et al 17 observed rhythmic diurnal expression of many of the components required for translation initiation, indicating that the circadian clock coordinates the regulation of the biogenesis of ribosomes. The characterization of gene regulation revealed an unexpected nonlinear transcriptional program and indicates that the function of regulatory elements is complex on many time scales ranging from milliseconds to hours.…”

Section: Dynamism In Gene Expressionmentioning

confidence: 99%

It is time to take timing seriously in clinical genetics

Kosztolányi

2014

Eur J Hum Genet

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Observations made by molecular techniques on the genome along the individuals' lifetime indicate that the genome in somatic cells displays changes at molecular, cellular, and organismal levels. Timing of genetic events leading to somatic mosaicism and gene expression dynamism results in a highly important variable for comprehending the role of genetics in health and disease. Consideration of time in clinical genetics should be enthusiastically invested into research strategy, interpretation of the results, diagnostic routine, and particularly in ethical discussions.

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The Circadian Clock Coordinates Ribosome Biogenesis

Abstract: The authors identify a new role of the circadian clock in coordinating mRNA translation during ribosome biogenesis, a key process for cell metabolism.

Cited by 262 publications

References 94 publications

Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

Mistimed sleep disrupts circadian regulation of the human transcriptome

It is time to take timing seriously in clinical genetics

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