The Circadian Clock Maintains Cardiac Function by Regulating Mitochondrial Metabolism in Mice

Kohsaka, Akira; Das, Partha; Hashimoto, Izumi; Nakao, Tomomi; Deguchi, Yoko; Gouraud, Sabine S.; Waki, Hidefumi; Muragaki, Yasuteru; Maeda, Masanobu

doi:10.1371/journal.pone.0112811

Cited by 96 publications

(90 citation statements)

References 53 publications

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“…Dependency of mitochondrial morphology on clock genes was also reported in mouse skeletal muscle (28) and heart (17) and is linked to impaired mitochondrial function in these organs. Mitochondria in macrophages exhibit daily morphological changes in vitro as well (29).…”

Section: Circadian Rhythms In Mitochondrial Morphologymentioning

confidence: 80%

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The Circadian Nature of Mitochondrial Biology

Manella

Asher

2016

Front. Endocrinol.

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Circadian clocks orchestrate the daily changes in physiology and behavior of light-sensitive organisms. These clocks measure about 24 h and tick in a self-sustained and cell-autonomous manner. Mounting evidence points toward a tight intertwining between circadian clocks and metabolism. Although various aspects of circadian control of metabolic functions have been extensively studied, our knowledge regarding circadian mitochondrial function is rudimentary. In this review, we will survey the current literature related to the circadian nature of mitochondrial biology: from mitochondrial omics studies (e.g., proteome, acetylome, and lipidome), through dissection of mitochondrial morphology, to analyses of mitochondrial processes such as nutrient utilization and respiration. We will describe potential mechanisms that are implicated in circadian regulation of mitochondrial functions in mammals and discuss the possibility of a mitochondrial-autonomous oscillator.

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Section: Circadian Rhythms In Mitochondrial Morphologymentioning

confidence: 80%

“…Indeed, the transcript levels of several nuclear-encoded mitochondrial proteins are altered in clock genes mutant mice (17, 18). Moreover, BMAL1 was shown to bind their promoters by ChIP (19, 20).…”

Section: Circadian Rhythms In Mitochondrial Compositionmentioning

confidence: 99%

The Circadian Nature of Mitochondrial Biology

Manella

Asher

2016

Front. Endocrinol.

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“…Remarkably, the TORC1 pathway was also shown to regulate translation of nucleus-encoded mitochondrial genes and mitochondrial activity (61). Incidentally, mitochondrial oxidative activity is rhythmic and under the control of the circadian clock (62)(63)(64), and this rhythmic activity is attributed in part to the clockdependent regulation of NAD+ synthesis through the transcriptional regulation of the Nampt gene (65,66). To what extend the rhythmic synthesis of mitochondrial proteins modulated by the circadian clock also contributes to this phenomenon remains to be demonstrated.…”

Section: Translation Efficiency Is Regulated During the Diurnal Cyclementioning

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.

217

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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“…The inactivation of the adipocyte clock compromised a time-dependent feedback from adipose to the brain that appears to be necessary for the timing of feeding behavior [30]. The importance of the circadian clock in metabolic fitness has been demonstrated in liver and heart, where loss of circadian rhythmicity in mitochondrial function leads in reduced respiratory output, increased oxidative damage, and abnormal mitochondrial morphology [14, 49]. Similarly, deletion of the transcriptional activators of the circadian clock in neurons of the central nervous system results in increased oxidative damage in the brain [50].…”

Section: Circadian Organization Of Metabolism At the Level Of The Orgmentioning

confidence: 99%

Circadian Clocks and Metabolism: Implications for Microbiome and Aging

Paschos

FitzGerald

2017

Trends in Genetics

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The circadian clock directs many aspects of metabolism to separate in time opposing metabolic pathways and optimize metabolic efficiency. The master circadian clock of the suprachiasmatic nucleus synchronizes to light, while environmental cues such as temperature and feeding out of phase to the light schedule may synchronize peripheral clocks. This misalignment of central and peripheral clocks may be involved in the development of disease and the acceleration of aging, possibly in a gender specific manner. Here we discuss the interplay between the circadian clock and metabolism, the importance of the microbiome and how they relate to aging.

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The Circadian Clock Maintains Cardiac Function by Regulating Mitochondrial Metabolism in Mice

Cited by 96 publications

References 53 publications

The Circadian Nature of Mitochondrial Biology

The Circadian Nature of Mitochondrial Biology

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

Circadian Clocks and Metabolism: Implications for Microbiome and Aging

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