Circadian Clock

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This entry is adapted from the peer-reviewed paper 10.3390/pharmaceutics14071424

Most living organisms in both the plant and animal kingdoms have evolved processes to stay in tune with the alternation of day and night, and to optimize their physiology as a function of light supply. In mammals, a circadian clock relying on feedback loops between key transcription factors will thus control the temporally regulated pattern of expression of most genes. Modern ways of life have highly altered the synchronization of human activities with their circadian clocks. The circadian clock orchestrates most physiological events in living organisms and its deregulation in association with modern ways of life correlates with the rise of multiple pathologies in humans.

circadian clock pathologies metabolic disorders

1. A Brief History of Circadian Rhythm Knowledge

Circadian rhythms in nature were observed for a long time, but their importance in physiology has come back into the spotlight recently. The circadian clock has gained much notoriety with the Nobel Prize in Physiology or Medicine awarded to Jeffrey Hall, Michael Rosbash, and Michael Young for their studies on the molecular mechanisms controlling the circadian rhythms ^[1]^[2]^[3].

In the plant kingdom, Androsthenes made the first report on circadian rhythmicity in the 4th century BC with the sleep movements of Tamaricus indicus’ leaves. Some two millennia occurred before some experimental work reinforced this concept of the plant circadian clock. In 1729, Jean-Jacques d’Ortous de Mairan actually noticed that the Mimosa leaves moved with a 24 h periodicity, even when he put the plant in a light-deprived environment ^[4]. This proved that an endogenous clock was able to impose a rhythm to processes, which could be discriminated from simple responses to daily stimuli.

Circadian rhythmicity is also obviously present in the behavioral patterns of animals (sleeping and feeding notably) and leads to the classification between diurnal and nocturnal animals. Besides, many biological processes including body temperature, hormone release, immune response, …, are now recognized to follow circadian evolutions.

Since almost all living organisms display circadian rhythms, this probably implies that evolution has selected the preservation of such rhythms. By allowing organisms to anticipate and prepare for circadian environmental changes, they would provide a selective advantage to living beings to optimize the light and food resources.

The molecular mechanisms responsible for these circadian rhythms remained elusive until the development of mutation screenings in the genome of the fruit fly a few decades ago. At that time, a seminal work highlighted the period (per) gene as critical for the periodicity of the fly activity ^[5]. Since then, researchers identified several other genes as core clock genes, driving circadian rhythms. This clock is based on an intricate network of intertwined transcriptional feedback loops acting as endogenous oscillators ^[6] (Figure 1).

Figure 1. Core clock genes and their intertwined feedback loops.

The molecular core clock relies on the inter-regulation of several genes, including the couple Bmal1/Clock and their transcriptional targets Per, Cry, Ror, and Rev-Erb. When Bmal1 and Clock proteins dimerize, they bind to E-box-containing promoters and activate the transcription of their targets. Among these, PER and CRY proteins dimerize and repress the binding of BMAL1/CLOCK to E-boxes. The expression of REV-ERB will repress the transcription of the bmal1 gene, whereas ROR will stimulate this transcription, via their action on RRE (ROR Response Element) in the bmal1 gene promoter. These intertwined negative and positive feedback loops ensure proper circadian oscillations in the levels of these gene products, with a peak in BMAL1/CLOCK activity at the onset of the active phase, and a more or less delayed expression of its targets/regulators.

Nowadays, researchers evaluate that more than 40% of protein-coding genes display 24 h rhythmicity in mammals ^[7]. Moreover, it seems that beyond transcription, circadian rhythms of oxidation and reduction occur, as evidenced in red blood cells ^[8]. A link between these two kinds of regulation may be the Pentose Phosphate Pathway, with NADPH production regulating core clock transcriptional circuits ^[9].

2. Alterations in Day–Night Lifestyle Influence on Human Health

The central circadian clock in humans is localized in the SCN (suprachiasmatic nucleus), which receives light-driven inputs from specific retinal photoreceptors. This central clock then coordinates the whole-body activities, notably by releasing hormones such as melatonin and glucocorticoids and via neurotransmitters, thus entraining peripheral clocks in the various tissues of the body ^[10] (Figure 2). The SCN thus regulates food intake, and can as well impact metabolism independently of feeding ^[11]^[12]. In parallel, peripheral tissues are also entrained by food intake, and restricted feeding can uncouple peripheral oscillators from the SCN pacemaker ^[13]. In rare conditions, peripheral clocks can even modulate the central clock to a certain extent ^[14].

Figure 2. Circadian clock entrainment.

The circadian central and peripheral clocks are entrained by two distinct main cues: light and food intake, respectively. The suprachiasmatic nucleus (SCN) is sensitive to light and synchronizes the central clock upon light exposure. This central clock transmits information to peripheral organs via the neuronal and endocrine systems and will regulate food intake and metabolism. In parallel, these peripheral organs also rely on food intake to entrain their clocks.

Proper synchronization of these biological oscillators, especially ensured by the absence of food intake in the normal rest phase of the organism, allows for optimized energy expenditure in most cellular and tissular processes. Inversely, clock misalignments generate troubles in metabolic functions, which can result in several pathologies.

For millennia, human beings have kept their activities rather aligned with cues from their environments (so-called zeitgebers) and their circadian clock. The invention of electricity and modern ways of life have shifted this principle in the last decades. Watching TV or computer screens at night has become increasingly common, and disturbs the integration of light cycles by our brain. At the same time, food intake tends to be less and less restricted to our active phase. Moreover, coffee consumption in the evening is becoming quite common and was shown to delay melatonin production and circadian rhythm, beyond its sleep disruptive effects ^[15]^[16].

Since circadian rhythmicity orchestrates most processes, misaligned rhythms are detrimental to one’s fitness. The circadian misalignment is especially exacerbated for some categories of people, either for deliberate leisure purposes or for imposed work reasons. Shifted workers thus represent a category of people regularly submitted to strong circadian misalignments and the impact of such practices on human health is illustrated by their increased propensity to develop several pathologies such as depression, metabolic syndrome, cardiovascular diseases, and cancers (for review, see ^[17]).

A clear experimental demonstration of a link between recurrent circadian clock shifts and pathologies came from a study in which mice were subjected to chronic jet lags. This led to a desynchronization of their SCN central clock, chronic inflammation, the development of hepatosteatosis, and a reduced lifespan ^[18].

Individual variations occur within the human population about the circadian clock. Some people naturally wake up early in the morning and are called “larks” or “early birds” whereas others are dubbed “night owls”. To quantify such phenotypes, researchers used the MSF (Midpoint Sleep on Free days) and showed that the chronotype evolved with age. Indeed, this MSF progressively delays reaching its maximal lateness around 20 years old, before decreasing regularly when becoming older ^[19]. Although this was considered mainly a question of education and choice in the way of life, recent studies suggest that this phenomenon may rely on genetic circuits, which are slightly shifting the body clock ^[20].

This state of things has consequences on people’s alertness, efficiency, and mood ^[21]. A very recent study has investigated the consequences of the shift between the late chronotype of most teenagers and the fact that they are attending school early in the morning. Of note, they show that school performance is improved when learning time is adjusted to the student/t’s chronotype ^[22]. This means that the performance assessment is somehow biased by one’s chronotype and possibly contributes to the fact that in our societies, the early bird catches the worm.

People who display a strong shift in their chronotype suffer from a so-called “social jetlag” ^[23]. Strikingly, this social jetlag is associated with depressive symptoms but also with cardiovascular dysfunctions ^[24]. Notably, later chronotypes correlate with increased psychological disorders, diabetes, poorer cardiovascular health ^[25], and an enhanced risk of mortality ^[26].

Another important circadian misalignment occurring in our modern societies is associated with the aging population. Older people tend to display dampened oscillations in several circadian traits, including the release of melatonin and cortisol hormones, which could be linked to some age-related pathologies (for review, see ^[27]^[28]).

3. The Molecular Links between the Circadian Clock and Metabolism: The Food Connection

The energetic demands of our tissues drastically vary night and day, and metabolic activities are accordingly fluctuating in a circadian manner. It is therefore not surprising that food intake represents a critical zeitgeber for peripheral clocks involved in metabolism regulation.

A clear proof of evidence of the link between circadian clock and metabolism came from studies showing that genetically disrupting either Clock or Bmal1 in mice induced the apparition of several traits associated with metabolic syndrome ^[29]^[30].

Some nuclear receptors such as REV-ERB, ROR, and peroxisome proliferation-activated receptors (PPARs) both regulate cellular metabolism and are components of the molecular core clock machinery. This presence at the crossroad of metabolism and circadian clock makes them good candidates to control metabolic storage and energetic consumption accordingly to circadian activities ^[31]. Hence, REV-ERB agonists, such as SR9009, represent interesting pharmacological compounds due to their pleiotropic activities in the regulation of the circadian clock and lipid metabolism ^[32]. The key role of REV-ERB in the integration of clock and food inputs was recently reinforced by the demonstration that REV-ERBα cyclically modifies the activity of OGT (O-GlcNAc transferase), a nutrient sensor, which regulates among others the expression of SREBP1c, a critical protein in lipogenesis ^[33]. REV-ERBα also controls mTOR ^[34], another protein well known for integrating nutrient and energy status in the cells and recently shown to affect the circadian clock ^[35].

To come back to the connection between metabolism and the clock, metabolite levels can as well modulate the clock and be controlled by it, as illustrated by the NAD⁺ (Nicotinamide Adenine Dinucleotide) example. NAD⁺ is a cofactor for SIRT1 deacetylase, which inhibits BMAL1 activity, and BMAL1/CLOCK conversely controls NAD⁺ level oscillations by controlling the NAD⁺ salvage pathway via NAMPT (nicotinamide phosphoribosyltransferase) expression control ^[36]^[37]. Moreover, SIRT1 deacetylates not only BMAL1 but also PGC1α, a transcriptional coactivator regulating energy homeostasis and the expression of core clock genes ^[38]. Since PGC1α activation depends on AMPK action before its subsequent deacetylation by SIRT1 ^[39], PGC1α stands as an integrator of both NAD⁺ and AMP energy-sensing inputs to control both circadian clock and metabolism.

It is noteworthy that circadian fluctuations in metabolites are coordinated between the different tissues of an organism, reflecting a coherence among clocks ^[40]. Furthermore, meal timing was shown to play a role in peripheral clock synchronization in humans ^[41]. Given this tight link between metabolism and the circadian clock, it is not surprising to notice that clock alterations result in metabolic pathologies. In the Gremlins movie, Gizmo’s seller tells the hero not to give him food after midnight. Human beings should also pay more attention to the recommendation not to eat during their resting phase. Actually, it seems that many disorders occurring following the mishandled circadian clock may rely on improper food intake timing, resulting in physiopathological situations. Experimental studies with mice demonstrated that shifting their feeding time to their circadian rest phase induced metabolic syndrome in these mice ^[42]. Changing one’s diet can reciprocally affect the circadian clock ^[43]. Indeed, mice that are given a high-fat diet shift their locomotor activities ^[44]. Moreover, the nature of food can also alter the circadian clock, as illustrated by BMAL1 inhibition triggered by the saturated fatty acid palmitate ^[45].

When modern ways of life disrespect both food intake and the circadian clock, several metabolic pathologies arise.

4. A Healthy Way of Life: Get Synchronized with Your Circadian Clock

After having shown that the timing of feeding can trigger great metabolic repercussions, mice models also demonstrated that good feeding habits could restore a healthy situation. Time-restricted feeding actually proved to prevent the onset of metabolic alterations in mice given a high-fat diet, for an equivalent caloric intake ^[46]. This method was efficient as well to counteract the metabolic diseases of clock-deficient mice ^[47].

With this in mind, and although evidence is still scarce for food as a bona fide zeitgeber in humans ^[48], several strategies of chronological diet are nowadays proposed to improve human metabolism and health. These include fasting periods of 12H or more, caloric restriction, or fasting-mimicking diets based on high fat and low carbohydrate contents ^[49]^[50]. Such strategies display the advantage to improve weight maintenance without requiring pharmacological drugs, yet the importance of each intervention remains debated since they are often combined in the dietary protocols. The use of natural bioactive compounds as diet supplements also drove promising results ^[51]. Notably, Epigallocatechin-3-gallate (EGCG) can restore a proper clock and metabolism in mice fed with a high-fat and high fructose diet, when administered at specific times ^[52].

Circadian clock misalignments are highly associated with negative health impacts on shift workers, who represent a large population in our modern societies. Rotating night shift work was especially shown to increase the risk of developing type 2 diabetes when it was combined with several unhealthy lifestyles ^[53]. Several research groups are trying to identify strategies aimed at alleviating the health problems met by this category of workers. A study performed with a small cohort of 11 individuals simulating the night shift suggested that the absence of eating at night may be helpful to impair the metabolic disruption in shift workers ^[54]. Although measuring metabolic traits requires complicated logistics in such studies, sleep improvements represent useful hints to evidence reduced misalignments in shifted workers. A chronotype-adjusted shift schedule was implemented in a factory, by removing the highest shifts for extreme chronotypes, which led to an increase in sleep duration and quality ^[55]. While it may be difficult to apply in most factories or hospitals, another approach could be implemented more easily on a large scale, which relies on light-based interventions and was also successful in improving sleep, as well as reducing fatigue and working errors ^[56].

Exposure to artificial light at night reduces melatonin secretion and alters sleep and circadian rhythms ^[57]. An easy tip for most people would therefore be to reduce this exposure as much as possible, by limiting the use of computer screens late at night. When not possible due to work duties, softwares exist which modify the spectrum of screen light day and night, and especially decrease the emission of blue light at night, with the intent to preserve the circadian clock. The pharmacological use of melatonin to counteract its reduced secretion could represent another solution ^[58].

More globally, the impact of the visual and non-visual effects of light on human activity is gaining importance nowadays, giving rise to the human-centric lighting concept ^[59] and recommendations such as adapting light environments throughout the day ^[60].

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