Reciprocal Interactions between Circadian Clocks, Food Intake, and Energy Metabolism

Abstract

Like other biological functions, food intake and energy metabolism display daily rhythms controlled by the circadian timing system that comprises a main circadian clock and numerous secondary clocks in the brain and peripheral tissues. Each secondary circadian clock delivers local temporal cues based on intracellular transcriptional and translational feedback loops that are tightly interconnected to intracellular nutrient-sensing pathways. Genetic impairment of molecular clocks and alteration in the rhythmic synchronizing cues, such as ambient light at night or mistimed meals, lead to circadian disruption that, in turn, negatively impacts metabolic health. Not all circadian clocks are sensitive to the same synchronizing signals. The master clock in the suprachiasmatic nuclei of the hypothalamus is mostly synchronized by ambient light and, to a lesser extent, by behavioral cues coupled to arousal and exercise. Secondary clocks are generally phase-shifted by timed metabolic cues associated with feeding, exercise, and changes in temperature. Furthermore, both the master and secondary clocks are modulated by calorie restriction and high-fat feeding. Taking into account the regularity of daily meals, the duration of eating periods, chronotype, and sex, chrononutritional strategies may be useful for improving the robustness of daily rhythmicity and maintaining or even restoring the appropriate energy balance.

Dynamic encoding of temperature in the central circadian circuit coordinates physiological activities

“…In nature, organisms have developed a sophisticated neuronal mechanism that allows them to finely adjust their metabolism and behavior in response to fluctuations in environmental temperature, occurring either daily or seasonally 2 , 35 . In order to unravel the intricate encoding and regulation of temperature-dependent physiological activity changes in the central brain, we engineered a highly precise temperature-controlled Peltier device that was seamlessly integrated with an in vivo two-photon calcium imaging system.…”

Treat time matters: Untimely sugar consumption implicated in long‐term energy imbalance

“…Though light is a primary entrainment cue for the master pacemaker of the brain, the suprachiasmatic nucleus (SCN) of the hypothalamus, food is an important Zeitgeber (or “time‐giver”) for many peripheral organs, 1 where the circadian phase can adapt to the timing of energy intake, as opposed to adhering to the circadian organization provided by the SCN's entrainment to the light/dark cycle. Interestingly, a “misalignment” of the circadian clock across peripheral organs and the SCN is thought to be induced by mistimed energy intake patterns, 1 and is deleterious for metabolic health in humans and other organisms 2 . Both the timing of food intake and the quality of nutrient intake are important for maintaining temporal organization within the body and for driving normal patterns of circadian gene expression 3 …”

“…Interestingly, a "misalignment" of the circadian clock across peripheral organs and the SCN is thought to be induced by mistimed energy intake patterns, 1 and is deleterious for metabolic health in humans and other organisms. 2 Both the timing of food intake and the quality of nutrient intake are important for maintaining temporal organization within the body and for driving normal patterns of circadian gene expression. 3 In this issue, Muguerza et al use nocturnal rats to test several metabolic and circadian effects of elevated sugar consumption ("sweet treats") administered at activity onset (8 p.m., or Zeitgeber time ZT12) versus the onset of the rest phase (8 a.m, ZT0).…”

Melatonin in energy control: Circadian time‐giver and homeostatic monitor

“…This is because such erroneous signals induce circadian disturbances, which in turn will trigger or promote adverse effects on metabolic health. 22,23 Chronic low-grade inflammation is a pervasive characteristic of obesity, diabetes, and aging. White adipose tissue that secretes adipokines and inflammatory cytokines contributes directly to systemic inflammation.…”

“…Shiftwork involves not only prolonged exposure to light at night, coupled with nocturnal or irregular meals, but also implies daytime sleep, which is often too short and of insufficient quality. 22,29,30 Of note, in addition to its shifting effects on the master clock, exposure to light at night also inhibits directly the synthesis and release of melatonin by the pineal gland (Figure 1). 6 As we shall see in the brief overview below, melatonin participates in energy control, not only by acting on temporal organization via resetting and enhancing the amplitude of circadian clocks, but also by modulating homeostasis of metabolic processes and intracellular oxidative stress.…”