Glucocorticoids as Entraining Signals for Peripheral Circadian Oscillators

Pezük, Pınar; Mohawk, Jennifer A.; Wang, Laura A; Menaker, Michael

doi:10.1210/en.2012-1486

Cited by 165 publications

(146 citation statements)

References 56 publications

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“…The observed phase advances of the liver and adrenal rhythms are comparable to those observed in animals fed during the light phase (e.g., 29), suggesting the feeding rhythm as a possible mechanism behind the phase advance of the peripheral rhythms. The correspondence between the timing of behavior and corticosterone secretion is consistent with a role for the adrenal glands in circadian organization (30).…”

Section: Discussionsupporting

confidence: 68%

Cold and hunger induce diurnality in a nocturnal mammal

Vinne

Riede

Gorter

et al. 2014

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

Self Cite

131

116

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The mammalian circadian system synchronizes daily timing of activity and rest with the environmental light-dark cycle. Although the underlying molecular oscillatory mechanism is well studied, factors that influence phenotypic plasticity in daily activity patterns (temporal niche switching, chronotype) are presently unknown. Molecular evidence suggests that metabolism may influence the circadian molecular clock, but evidence at the level of the organism is lacking. Here we show that a metabolic challenge by cold and hunger induces diurnality in otherwise nocturnal mice. Lowering ambient temperature changes the phase of circadian light-dark entrainment in mice by increasing daytime and decreasing nighttime activity. This effect is further enhanced by simulated food shortage, which identifies metabolic balance as the underlying common factor influencing circadian organization. Clock gene expression analysis shows that the underlying neuronal mechanism is downstream from or parallel to the main circadian pacemaker (the hypothalamic suprachiasmatic nucleus) and that the behavioral phenotype is accompanied by phase adjustment of peripheral tissues. These findings indicate that nocturnal mammals can display considerable plasticity in circadian organization and may adopt a diurnal phenotype when energetically challenged. Our previously defined circadian thermoenergetics hypothesis proposes that such circadian plasticity, which naturally occurs in nocturnal mammals, reflects adaptive maintenance of energy balance. Quantification of energy expenditure shows that diurnality under natural conditions reduces thermoregulatory costs in small burrowing mammals like mice. Metabolic feedback on circadian organization thus provides functional benefits by reducing energy expenditure. Our findings may help to clarify relationships between sleep-wake patterns and metabolic phenotypes in humans.circadian rhythms | behavioral neurobiology | behavioral plasticity | chronotype ecology E nvironmental differences between day and night have resulted in daily (circadian) rhythms in physiology and behavior of most organisms. Many mammals are night active (nocturnal), which most likely reduces predation risk (1). Being active at night is however likely to be energetically costly because nocturnal mammals cannot escape the low temperatures at night by sleeping in sheltered places. Nocturnal mammals that are energetically challenged therefore may become day active (diurnal) to reduce energy expenditure (2). Nocturnal and diurnal activity patterns are indeed subject to phenotypic plasticity (temporal niche switching) under natural conditions (2).The central circadian pacemaker in mammals is located in the suprachiasmatic nucleus (SCN) and coordinates tissue specific circadian rhythms throughout the body (3). In most cells, circadian rhythms originate from molecular feedback loops involving gene transcription (4-6) or a putative metabolic oscillator (7-10). At the molecular and systemic level regulatory loops interact to control circadian and meta...

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Section: Discussionsupporting

confidence: 68%

Cold and hunger induce diurnality in a nocturnal mammal

Vinne

Riede

Gorter

et al. 2014

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

Self Cite

131

116

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“…However, further details of the mechanisms underlying this process are poorly defined. Glucocorticoids [41], melatonin [42,43] and direct autonomic innervation [44,45] are endogenous signalling mechanisms by which the SCN maintains alignment of central and peripheral oscillators. Among these, melatonin is the most well studied humoral factor that affects the SCN, whilst also being affected by this region of the brain.…”

Section: The Internal Timing System and Metabolic Dysfunctionmentioning

confidence: 99%

Chronomedicine and type 2 diabetes: shining some light on melatonin

et al. 2016

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In mammals, the circadian timing system drives rhythms of physiology and behaviour, including the daily rhythms of feeding and activity. The timing system coordinates temporal variation in the biochemical landscape with changes in nutrient intake in order to optimise energy balance and maintain metabolic homeostasis. Circadian disruption (e.g. as a result of shift work or jet lag) can disturb this continuity and increase the risk of cardiometabolic disease. Obesity and metabolic disease can also disturb the timing and amplitude of the clock in multiple organ systems, further exacerbating disease progression. As our understanding of the synergy between the timing system and metabolism has grown, an interest has emerged in the development of novel clock-targeting pharmaceuticals or nutraceuticals for the treatment of metabolic dysfunction. Recently, the pineal hormone melatonin has received some attention as a potential chronotherapeutic drug for metabolic disease. Melatonin is well known for its sleep-promoting effects and putative activity as a chronobiotic drug, stimulating coordination of biochemical oscillations through targeting the internal timing system. Melatonin affects the insulin secretory activity of the pancreatic beta cell, hepatic glucose metabolism and insulin sensitivity. Individuals with type 2 diabetes mellitus have lower night-time serum melatonin levels and increased risk of comorbid sleep disturbances compared with healthy individuals. Further, reduced melatonin levels, and mutations and/or genetic polymorphisms of the melatonin receptors are associated with an increased risk of developing type 2 diabetes. Herein we review our understanding of molecular clock control of glucose homeostasis, detail the influence of circadian disruption on glucose metabolism in critical peripheral tissues, explore the contribution of melatonin signalling to the aetiology of type 2 diabetes, and discuss the pros and cons of melatonin chronopharmacotherapy in disease management.

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“…7F). Transcripts within that category were associated with GO terms that include response to corticosteroid stimulus and hormone activity, and it is possible that the expression of these transcripts could be driven by cortisol (45). It is important to emphasize that effects of these endocrine signals on the transcriptome can also interact with the effects of the sleep-wake cycle.…”

Section: Mechanisms Underlying the Temporal Disruption Of Gene Expresmentioning

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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Glucocorticoids as Entraining Signals for Peripheral Circadian Oscillators

Cited by 165 publications

References 56 publications

Cold and hunger induce diurnality in a nocturnal mammal

Cold and hunger induce diurnality in a nocturnal mammal

Chronomedicine and type 2 diabetes: shining some light on melatonin

Mistimed sleep disrupts circadian regulation of the human transcriptome

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