Signalling entrains the peripheral circadian clock

doi:10.1016/j.cellsig.2019.109433

Cellular Signalling

Volume 69, May 2020, 109433

https://doi.org/10.1016/j.cellsig.2019.109433 Get rights and content

Highlights

•
Peripheral clock can regulate synchronization independent of superchiasmatic nucleus (SCN).
•
We discuss how different signals entrain peripheral circadian clocks in peripheral tissues.
•
Organ-to-organ communications are involved in entrainment of peripheral circadian clocks.

Abstract

In mammals, 24-h rhythms of behaviour and physiology are regulated by the circadian clock. The circadian clock is controlled by a central clock in the brain's suprachiasmatic nucleus (SCN) that synchronizes peripheral clocks in peripheral tissues. Clock genes in the SCN are primarily entrained by light. Increasing evidence has shown that peripheral clocks are also regulated by light and hormones independent of the SCN. How the peripheral clocks deal with internal signals is dependent on the relevance of a specific cue to a specific tissue. In different tissues, most genes that are under circadian control are not overlapping, revealing the tissue-specific control of peripheral clocks. We will discuss how different signals control the peripheral clocks in different peripheral tissues, such as the liver, gastrointestinal tract, and pancreas, and discuss the organ-to-organ communication between the peripheral clocks at the molecular level.

Introduction

In mammals, biorhythms are essential for maintaining whole-body homeostasis, while disruption of biorhythms may lead to deregulation of homeostasis and development of diseases [1,2]. An internal timing system has evolved to measure time, anticipate environmental daily changes, and tune physiology and behaviour to these variations. This anticipatory internal timing system was named the “circadian clock”, providing a good example of how changes in the environment influence behaviour and physiology [3].

Circadian clocks are composed of central and peripheral clocks, which are both coordinated to produce daily rhythms in physiology and behaviour [4]. In mammals, circadian clocks are found in nearly all cells and tissues. The central clock is located in the superchiasmatic nucleus (SCN) of the hypothalamus, which is a dominant circadian pacemaker [5]. It can receive direct photic input from the retina via the intrinsically photoreceptive retinal ganglion cell (ipRGC), a type of photoreceptive cell, and produces robust biorhythms [6]. In turn, the central clock uses diverse and not entirely known pathways to reset the phase of peripheral clocks. SCN transmits signals to the periphery of the body by directly interacting with other brain regions, through the production of signalling molecules, or by indirectly determining rest-activity periods that in turn regulate feeding-fasting rhythms [7,8].

Mammalian SCN is resistant to most non-photic zeitgebers, while the peripheral clocks respond to ambient influences such as temperature, which allows the maintenance of SCN circadian properties despite external changes [9]. The synchronization mechanisms are different among different tissues. Circadian rhythms in peripheral organs are controlled by the interaction of local tissue clocks and SCN-generated rhythms in physiology and behaviours. Nevertheless, under some conditions, the peripheral clock could be independent of the central clock. In response to advances and delays of the environmental light cycle, when isolated in cell culture, the central clock maintains its own rhythmicity, while the peripheral clock loses its rhythm in a few days, as seen in a transgenic rat line in which luciferase is rhythmically expressed under the control of the mouse Period (Per1) promoter [10].

Most mammalian cell types seem to contain all the molecular ingredients required to achieve circadian gene expression. Analysis of clock gene expression in mammals revealed that most of their corresponding mRNA products accumulated in a circadian manner not only in the SCN but also in a variety of peripheral tissues, including liver, muscle, kidney and lung [[11], [12], [13], [14]]. The expression of circadian clock genes was also found in other cells, such as mononuclear leukocytes and vascular smooth muscle cells [[15], [16], [17]]. However, the phase of the rhythmic expression of clock genes in the periphery is opposite or phase-delayed to the rhythm of the same clock genes expressed in the SCN.

Many reviews have focused on the function of the central circadian clock. Accumulating evidence has revealed that peripheral clocks are different from SCN clocks and can regulate synchronization independent of SCN. In this review, we discuss the signals that control peripheral clocks in individual organs and tissues, such as the liver, gastrointestinal tract (GIT), pancreas, lung, breast, skin, skeletal muscle, adipose tissues and cardiovascular system (See Table 1). Furthermore, we review work on how peripheral clocks in different organs communicate.

Section snippets

Peripheral clock in the liver

The liver is one of the most important organs involved in glucose and lipid metabolism and is finely regulated by coordination between the central clock and the peripheral clock in the liver. The circadian clock plays key roles in liver function in both health and disease [[18], [19], [20], [21]]. Accumulating data reveal that the peripheral clock in the liver is entrained by many factors, including feeding cues, insulin, glucocorticoid, ghrelin, mammalian/mechanistic target of rapamycin (mTOR)

Peripheral clock in the GIT

The GIT is subject to various 24-h rhythmic processes, which are under circadian clock gene control. The GIT exhibits diurnal rhythms in many physiologic functions, such as colonic motor activity, gastric acid secretion, mucosal transporters, mucosal enzyme activities, proliferation rates, etc. Clock genes, which are present within colonic epithelial cells and neurons of the myenteric plexus, coordinate rhythmic physiological functions such as motility, cell proliferation, and migration [42,43].

Peripheral clock in the pancreas

Circadian clock is critical for maintaining glucose homeostasis. The pancreas is one of the most important endocrine and exocrine organs and plays an essential role in body metabolism. The peripheral clock in the pancreas is required for achieving its function, such as insulin release. Peripheral circadian clocks in the pancreas have been identified in rats [54] and mice [55]. The expression of the major clock genes Per1, Per2, Bmal1, Cry1, timeless (Tim) and Clock, as well as of the output

Peripheral clock in the lung

Chronic lung diseases are often characterized by disrupted daily or circadian rhythms of lung function and inflammatory responses [60]. The molecular clock and redox signalling in the lung play a critical role in regulating inflammation, oxidative stress, and DNA damage responses in the pathophysiology of chronic airway diseases and their exacerbations, providing a potential for the molecular clock genes to be used as novel biomarkers for lung disease severity and as therapeutic targets for

Peripheral clock in the breast

Circadian clocks and breast biology are tightly connected, and the rhythmic expression of numerous genes is regulated by the circadian clock in the breast [65,66]. The disruption of circadian genes can change breast biology and may further contribute to breast cancer. Studies have shown that breast cancer is associated with the upregulation of TIMELESS and the downregulation of PER, CRY, and CLOCK, which might be related to the methylation of those genes in the tumour tissue [67,68]. In

Peripheral clock in the cardiovascular system

The circadian rhythms and the molecular clock have important functions in cardiovascular physiology and disease [71]. The clock machinery is found in the cells in the vascular system, such as endothelial cells, smooth muscle cells, fibroblasts, and stem cells. Daily vascular function and its disturbance are modulated by this machinery, which plays a critical role in the dysfunction of the vascular system [72]. The link between the peripheral circadian clock and hypoxia signalling in the

Peripheral clock in skeletal muscle

The functions of skeletal muscle are under the control of a circadian clock, especially myogenesis and skeletal muscle metabolism, which have been summarized in many reviews [[77], [78], [79]]. Therefore, we will only review the signalling involved in the entrainment of the peripheral circadian clock in skeletal muscle (Fig. 3).

Exercise plays an important role in regulating core clock gene expression in skeletal muscle. Dyar et al. examined circadian gene expression in fast- and slow-twitch

Peripheral clock in the skin

The skin is the largest organ in the human body and the interface between the organism and the external environment. Therefore, the peripheral circadian clock in the skin is entrained by multiple ambient and endogenous stimuli, such as UV and infrared radiation, visible light, temperature, hormones, reactive oxygen species, etc. These stimuli can affect the molecular clock in the skin, contributing to skin-related biological processes. Skin is widely used as a model to study the regulation of

Peripheral clock in the adipose tissues

Adipose tissues (white, brown and beige adipose) play important roles in the regulation of whole-body metabolism, thermogenesis and energy homeostasis. The interaction between circadian clocks and diet or exercise might have an impact on adipose tissue physiology and metabolism and therefore impact the whole-body phenotype and energy homeostasis, especially in brown adipose tissue, which plays more important roles in whole-body metabolic homeostasis [[92], [93], [94]]. The clock proteins and

Organ-to-organ communications entrain peripheral circadian clocks

Interestingly, an increasing number of studies have revealed that different tissues that achieve circadian rhythm have to interact with each other in a way that is not independent of environmental signals. Known organ-organ communications in the peripheral circadian clock are shown in Fig. 4. The loss or disruption of the clock in one peripheral tissue can affect the clock in another tissue. Paschos et al. demonstrated that the specific deletion of Bmal1, which encodes a core molecular clock

Perspectives

Here, we reviewed the peripheral clock in different organs. Every organ has its own circadian rhythm, which is synchronized by the integration of multiple signals. One signal molecule, such as insulin, could also affect the peripheral clock in multiple organs. It would be interesting to understand how one signal molecule acts on different peripheral circadian clocks and coordinates their functions. Although there are increasing data on the regulation of peripheral circadian clocks, the

Declaration of Competing Interest

The authors declare no conflict of interest.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (No. 81672358, No. 81701945, No. 81802890), the Natural Science Foundation of Shanghai (No. 18ZR1436900), and Shanghai Municipal Health Bureau (No. 2018BR32) and the Shanghai Municipal Education Commission-Gaofeng Clinical Medicine Grant Support (No. 20181708).

References (108)

E.M. Gibson et al.
Aging in the circadian system: considerations for health, disease prevention and longevity
Exp. Gerontol.
(2009)
A. Balsalobre et al.
A serum shock induces circadian gene expression in mammalian tissue culture cells
Cell
(1998)
M.J. Zylka et al.
Molecular analysis of mammalian timeless
Neuron
(1998)
K. Oishi et al.
Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats
Biochem. Biophys. Res. Commun.
(1998)
P. McNamara et al.
Regulation of CLOCK and MOP4 by nuclear hormone receptors in the vasculature: a humoral mechanism to reset a peripheral clock
Cell
(2001)
A. Mukherji et al.
The circadian clock and liver function in health and disease
J. Hepatol.
(2019)
K. Oishi et al.
Feeding cycle-dependent circulating insulin fluctuation is not a dominant Zeitgeber for mouse peripheral clocks except in the liver: differences between endogenous and exogenous insulin effects
Biochem. Biophys. Res. Commun.
(2017)
K. Honma et al.
Loss of circadian rhythm of circulating insulin concentration induced by high-fat diet intake is associated with disrupted rhythmic expression of circadian clock genes in the liver
Metab. Clin. Exp.
(2016)
D. Landgraf et al.
Circadian clock-gastrointestinal peptide interaction in peripheral tissues and the brain
Best Pract. Res. Clin. Endocrinol. Metab.
(2017)
R. Cao et al.
Translational control of entrainment and synchrony of the suprachiasmatic circadian clock by mTOR/4E-BP1 signaling
Neuron
(2013)

E. Marbach-Breitruck et al.

Tick-tock hedgehog-mutual crosstalk with liver circadian clock promotes liver steatosis

J. Hepatol.

(2019)

A.K. Luciano et al.

CLOCK phosphorylation by AKT regulates its nuclear accumulation and circadian gene expression in peripheral tissues

J. Biol. Chem.

(2018)

M. Sladek et al.

Insight into the circadian clock within rat colonic epithelial cells

Gastroenterology

(2007)

W.A. Hoogerwerf et al.

Clock gene expression in the murine gastrointestinal tract: endogenous rhythmicity and effects of a feeding regimen

Gastroenterology

(2007)

N. Aoki et al.

Involvement of 5-HT(3) and 5-HT(4) receptors in the regulation of circadian clock gene expression in mouse small intestine

J. Pharmacol. Sci.

(2014)

C.A. Thaiss et al.

Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis

Cell

(2014)

A. Zarrinpar et al.

Diet and feeding pattern affect the diurnal dynamics of the gut microbiome

Cell Metab.

(2014)

V. Leone et al.

Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism

Cell Host Microbe

(2015)

E. Muhlbauer et al.

Indication of circadian oscillations in the rat pancreas

FEBS Lett.

(2004)

I.K. Sundar et al.

Redox regulation of circadian molecular clock in chronic airway diseases

Free Radic. Biol. Med.

(2018)

E. Reszka et al.

Circadian genes in breast cancer

Adv. Clin. Chem.

(2016)

C.W. Yu et al.

Pro-inflammatory cytokines IL-6 and CCL2 suppress expression of circadian gene Period2 in mammary epithelial cells

Biochim. Biophys. Acta Gene Regul. Mech.

(2018)

S. Crnko et al.

Vasculature on the clock: Circadian rhythm and vascular dysfunction

Vasc. Pharmacol.

(2018)

X. Wu et al.

Regulation of circadian rhythms by NEAT1 mediated TMAO-induced endothelial proliferation: A protective role of asparagus extract

Exp. Cell Res.

(2019)

K.A. Dyar et al.

The calcineurin-NFAT pathway controls activity-dependent circadian gene expression in slow skeletal muscle

Mol. Metab.

(2015)

P.G. Saracino et al.

Hormonal regulation of core clock gene expression in skeletal muscle following acute aerobic exercise

Biochem. Biophys. Res. Commun.

(2019)

D.G. Lassiter et al.

AMPK activation negatively regulates GDAP1, which influences metabolic processes and circadian gene expression in skeletal muscle

Mol. Metab.

(2018)

C.B. Peek et al.

Circadian clock interaction with HIF1alpha mediates oxygenic metabolism and anaerobic glycolysis in skeletal muscle

Cell Metab.

(2017)

D. Lekkas et al.

The circadian clock control of adipose tissue physiology and metabolism

Autonom. Neurosci. Basic Clin.

(2019)

M.N. Moraes et al.

TRPV1 participates in the activation of clock molecular machinery in the brown adipose tissue in response to light-dark cycle

Biochim. Biophys. Acta Mol. Cell Res.

(2017)

M.N. Moraes et al.

Cold-sensing TRPM8 channel participates in circadian control of the brown adipose tissue

Biochim. Biophys. Acta Mol. Cell Res.

(2017)

E.A. Yu et al.

Disrupting the circadian clock: gene-specific effects on aging, cancer, and other phenotypes

Aging

(2011)

C. Saini et al.

Human peripheral clocks: applications for studying circadian phenotypes in physiology and pathophysiology

Front. Neurol.

(2015)

M. Selcho et al.

Central and peripheral clocks are coupled by a neuropeptide pathway in Drosophila

Nat. Commun.

(2017)

J. Husse et al.

Synchronization of the mammalian circadian timing system: light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time

BioEssays: News Rev. Mol. Cell. Dev. Biol.

(2015)

M.T. Clandinin et al.

Impact of dietary fatty acid balance on membrane structure and function of neuronal tissues

Adv. Exp. Med. Biol.

(1992)

K.A. Stokkan et al.

Entrainment of the circadian clock in the liver by feeding

Science (New York, NY)

(2001)

F. Damiola et al.

Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus

Genes Dev.

(2000)

M.H. Vitaterna et al.

The mouse clock mutation reduces circadian pacemaker amplitude and enhances efficacy of resetting stimuli and phase-response curve amplitude

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

(2006)

S. Yamazaki et al.

Resetting central and peripheral circadian oscillators in transgenic rats

Science (New York, NY)

(2000)

R. Allada et al.

Stopping time: the genetics of fly and mouse circadian clocks

Annu. Rev. Neurosci.

(2001)

S.M. Reppert et al.

Molecular analysis of mammalian circadian rhythms

Annu. Rev. Physiol.

(2001)

H. Nonaka et al.

Angiotensin II induces circadian gene expression of clock genes in cultured vascular smooth muscle cells

Circulation

(2001)

D. Shi et al.

Circadian clock genes in the metabolism of non-alcoholic fatty liver disease

Front. Physiol.

(2019)

A. Shetty et al.

Role of the circadian clock in the metabolic syndrome and nonalcoholic fatty liver disease

Dig. Dis. Sci.

(2018)

G. Mazzoccoli et al.

The biological clock: A pivotal hub in non-alcoholic fatty liver disease pathogenesis

Front. Physiol.

(2018)

F. Dang et al.

Insulin post-transcriptionally modulates Bmal1 protein to affect the hepatic circadian clock

Nat. Commun.

(2016)

D. Yamajuku et al.

Real-time monitoring in three-dimensional hepatocytes reveals that insulin acts as a synchronizer for liver clock

Sci. Rep.

(2012)

Q. Wang et al.

Ghrelin restores the disruption of the circadian clock in steatotic liver

Int. J. Mol. Sci.

(2018)

D. Landgraf et al.

Oxyntomodulin regulates resetting of the liver circadian clock by food

eLife

(2015)

Cited by (36)

The Physiological and Pharmacological Significance of the Circadian Timing of the HPA Axis: A Mathematical Modeling Approach
2024, Journal of Pharmaceutical Sciences
As a potent endogenous regulator of homeostasis, the circadian time-keeping system synchronizes internal physiology to periodic changes in the external environment to enhance survival. Adapting endogenous rhythms to the external time is accomplished hierarchically with the central pacemaker located in the suprachiasmatic nucleus (SCN) signaling the hypothalamus-pituitary-adrenal (HPA) axis to release hormones, notably cortisol, which help maintain the body's circadian rhythm. Given the essential role of HPA-releasing hormones in regulating physiological functions, including immune response, cell cycle, and energy metabolism, their daily variation is critical for the proper function of the circadian timing system. In this review, we focus on cortisol and key fundamental properties of the HPA axis and highlight their importance in controlling circadian dynamics. We demonstrate how systems-driven, mathematical modeling of the HPA axis complements experimental findings, enhances our understanding of complex physiological systems, helps predict potential mechanisms of action, and elucidates the consequences of circadian disruption. Finally, we outline the implications of circadian regulation in the context of personalized chronotherapy. Focusing on the chrono-pharmacology of synthetic glucocorticoids, we review the challenges and opportunities associated with moving toward personalized therapies that capitalize on circadian rhythms.
CRY1/2 regulate rhythmic CYP2A5 in mouse liver through repression of E4BP4
2023, Biochemical Pharmacology
CYP2A5, an enzyme responsible for metabolism of diverse drugs, displays circadian rhythms in its expression and activity. However, the underlying mechanisms are not fully established. Here we aimed to investigate a potential role of CRY1/2 (circadian clock modulators) in circadian regulation of hepatic CYP2A5. Regulatory effects of CRY1/2 on CYP2A5 were determined using Cry1-null and Cry2-null mice, and validated using AML-12, Hepa1-6 and HepG2 cells. CYP2A5 activities both in vivo and in vitro were assessed using coumarin 7-hydroxylation as a probe reaction. mRNA and protein levels were detected by qPCR and western blotting, respectively. Regulatory mechanism was studied using a combination of luciferase reporter assays, chromatin immunoprecipitation (ChIP) and co-immunoprecipitation (Co-IP). We found that ablation of Cry1 or Cry2 in mice reduced hepatic CYP2A5 expression (at both mRNA and protein levels) and blunted its diurnal rhythms. Consistently, these knockouts showed decreased CYP2A5 activity (characterised by coumarin 7-hydroxylation) and a loss of its time-dependency, as well as exacerbated coumarin-induced hepatotoxicity. Cell-based assays confirmed that CRY1/2 positively regulated CYP2A5 expression and rhythms. Based on combined luciferase reporter, ChIP and Co-IP assays, we unraveled that CRY1/2 interacted with E4BP4 protein to repress its inhibitory effect on Cyp2a5 transcription and expression. In conclusion, CRY1/2 regulate rhythmic CYP2A5 in mouse liver through repression of E4BP4. These findings advance our understanding of circadian regulation of drug metabolism and pharmacokinetics.
Cartilage-specific deficiency of clock gene Bmal1 accelerated articular cartilage degeneration in osteoarthritis by up-regulation of mTORC1 signaling
2023, International Immunopharmacology
Although a growing body of studies recently demonstrated that circadian clock gene Bmal1 plays an important role in cartilage development and homeostasis, evidence regarding the contribution of Bmal1 in articular cartilage of OA progression is still unclear. In the present study, we investigated the direct role of Bmal1 in articular cartilage homeostasis during OA progression using tamoxifen-induced cartilage-specific knockout mice. We found that the expression of BMAL1 was decreased in OA-damaged and aging cartilage tissues. Cartilage-specific deletion of Bmal1 promoted cartilage degradation and chondrocyte apoptosis, and inhibited chondrocyte anabolism in OA mice, leading to acceleration of articular cartilage degeneration and osteophyte formation during OA progression. Mechanistic study indicated that loss of Bmal1 resulted in hyperactivation of mammalian target of rapamycin complex 1(mTORC1) signaling in OA cartilage, and pharmacological inhibition of mTORC1 signaling pathway by rapamycin alleviated partially Bmal1 ablation-induced cartilage degradation and chondrocyte apoptosis in ex vivo OA model. Therefore, our results provide the evidence of a vital role for Bmal1 in cartilage degradation in post-traumatic OA by partially regulating the mTORC1 signaling.
The role of light pollution in mammalian metabolic homeostasis and its potential interventions: A critical review
2022, Environmental Pollution
Citation Excerpt :
The circadian system involves central oscillators in the SCN of the hypothalamus and peripheral oscillators functioning in the organ (Sinturel et al., 2022). The peripheral clocks are coordinated by the SCN clocks but may also be regulated independently of the SCN by light and hormones (Zhang et al., 2020b). At the molecular level, the circadian clock is composed of positive regulators Circadian Locomotor Output Cycles Kaput (CLOCK) and Brain and Muscle Arnt-like Protein 1 (BMAL1), and negative feedback factors Cryptochrome (CRY1, CRY2), Period (PER1, PER2, PER3), as well as accessory feedback loops, such as the nuclear receptors retinoic acid-related orphan receptors (RORs), nuclear receptors REV-ERBs, and peroxisome proliferator-activated receptors (PPARs) (Fonken and Nelson, 2014; Patke et al., 2020).
Irregular or unnatural artificial light causes severe environmental stress on the survival and health of organisms, which is rapidly becoming a widespread new type of environmental pollution. A series of disruptive behaviors to body homeostasis brought about by light pollution, including metabolic abnormalities, are likely to be the result of circadian rhythm disturbances. Recently, the proposed role of light pollution in metabolic dysregulation has accelerated it into an emerging field. Hence, the regulatory role of light pollution in mammalian metabolic homeostasis is reviewed in this contribution. Light at night is the most widely affected type of light pollution, which disrupts metabolic homeostasis largely due to its disruption of daily food intake patterns, alterations of hormone levels such as melatonin and glucocorticoids, and changes in the rhythm of inflammatory factor production. Besides, light pollution impairs mammalian metabolic processes in an intensity-, photoperiod-, and wavelength-dependent manner, and is also affected by species, gender, and diets. Nevertheless, metabolic disorders triggered by light pollution are not irreversible to some extent. Potential interventions such as melatonin supplementation, recovery to the LD cycle, time-restricted feeding, voluntary exercise, wearing blue light-shied goggles, and bright morning light therapy open a bright avenue to prevent light pollution. This work will help strengthen the relationship between light information and metabolic homeostasis and provide new insights for the better prevention of metabolic disorders and light pollution.
Neurobioloy of sleep and circadian disorders
2022, Neurobiology of Brain Disorders: Biological Basis of Neurological and Psychiatric Disorders, Second Edition
Mammalian sleep has evolved under the influence of the day–night cycle and in response to reproductive needs, food seeking, and predator escape, resulting in circadian (predictive) and homeostatic (reactive) regulation. A molecular clock characterized by transcription/translation feedback loops mediates circadian regulation of sleep. Misalignment with the rhythm of the sun results in circadian rhythm disorders and jet lag. The molecular basis of homeostatic sleep regulation is mostly unknown. A network of mutually inhibitory brain nuclei regulates sleep states and sleep–wake transitions. Abnormalities in these networks create sleep disorders, for example, rapid eye movement sleep behavior disorder, sleep walking, or narcolepsy. Physiological changes associated with sleep can also be imbalanced, resulting in excess movements such as periodic leg movements during sleep or abnormal breathing in obstructive sleep apneas. As every organ in the body is affected by sleep directly or indirectly, sleep and sleep-associated disorders are frequent and only now starting to be understood.
Alterations in Per2, Bcl2 gene expression, and oxidative status in aged rats liver after light pulse at night
2024, Sleep and Biological Rhythms

View all citing articles on Scopus

¹: These authors contributed equally to this work.

View full text

ReviewSignalling entrains the peripheral circadian clock

Highlights

Abstract

Introduction

Section snippets

Peripheral clock in the liver

Peripheral clock in the GIT

Peripheral clock in the pancreas

Peripheral clock in the lung

Peripheral clock in the breast

Peripheral clock in the cardiovascular system

Peripheral clock in skeletal muscle

Peripheral clock in the skin

Peripheral clock in the adipose tissues

Organ-to-organ communications entrain peripheral circadian clocks

Perspectives

Declaration of Competing Interest

Acknowledgements

Exp. Gerontol.

Cell

Neuron

Biochem. Biophys. Res. Commun.

Cell

J. Hepatol.

Biochem. Biophys. Res. Commun.

Metab. Clin. Exp.

Best Pract. Res. Clin. Endocrinol. Metab.

Neuron

J. Hepatol.

J. Biol. Chem.

Gastroenterology

Gastroenterology

J. Pharmacol. Sci.

Cell

Cell Metab.

Cell Host Microbe

FEBS Lett.

Free Radic. Biol. Med.

Adv. Clin. Chem.

Biochim. Biophys. Acta Gene Regul. Mech.

Vasc. Pharmacol.

Exp. Cell Res.

Mol. Metab.

Biochem. Biophys. Res. Commun.

Mol. Metab.

Cell Metab.

Autonom. Neurosci. Basic Clin.

Biochim. Biophys. Acta Mol. Cell Res.

Biochim. Biophys. Acta Mol. Cell Res.

Disrupting the circadian clock: gene-specific effects on aging, cancer, and other phenotypes

Aging

Human peripheral clocks: applications for studying circadian phenotypes in physiology and pathophysiology

Front. Neurol.

Central and peripheral clocks are coupled by a neuropeptide pathway in Drosophila

Nat. Commun.

Synchronization of the mammalian circadian timing system: light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time

BioEssays: News Rev. Mol. Cell. Dev. Biol.

Impact of dietary fatty acid balance on membrane structure and function of neuronal tissues

Adv. Exp. Med. Biol.

Entrainment of the circadian clock in the liver by feeding

Science (New York, NY)

Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus

Genes Dev.

The mouse clock mutation reduces circadian pacemaker amplitude and enhances efficacy of resetting stimuli and phase-response curve amplitude

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

Resetting central and peripheral circadian oscillators in transgenic rats

Science (New York, NY)

Stopping time: the genetics of fly and mouse circadian clocks

Annu. Rev. Neurosci.

Molecular analysis of mammalian circadian rhythms

Annu. Rev. Physiol.

Angiotensin II induces circadian gene expression of clock genes in cultured vascular smooth muscle cells

Circulation

Circadian clock genes in the metabolism of non-alcoholic fatty liver disease

Front. Physiol.

Role of the circadian clock in the metabolic syndrome and nonalcoholic fatty liver disease

Dig. Dis. Sci.

The biological clock: A pivotal hub in non-alcoholic fatty liver disease pathogenesis

Front. Physiol.

Insulin post-transcriptionally modulates Bmal1 protein to affect the hepatic circadian clock

Review
Signalling entrains the peripheral circadian clock