Circadian rhythms in glucose and lipid metabolism in nocturnal and diurnal mammals

Abstract

a b s t r a c tMost aspects of energy metabolism display clear variations during day and night. This daily rhythmicity of metabolic functions, including hormone release, is governed by a circadian system that consists of the master clock in the suprachiasmatic nuclei of the hypothalamus (SCN) and many secondary clocks in the brain and peripheral organs. The SCN control peripheral timing via the autonomic and neuroendocrine system, as well as via behavioral outputs. The sleepewake cycle, the feeding/fasting rhythm and most hormonal rhythms, including that of leptin, ghrelin and glucocorticoids, usually show an opposite phase (relative to the lightedark cycle) in diurnal and nocturnal species. By contrast, the SCN clock is most active at the same astronomical times in these two categories of mammals. Moreover, in both species, pineal melatonin is secreted only at night. In this review we describe the current knowledge on the regulation of glucose and lipid metabolism by central and peripheral clock mechanisms. Most experimental knowledge comes from studies in nocturnal laboratory rodents. Nevertheless, we will also mention some relevant findings in diurnal mammals, including humans. It will become clear that as a consequence of the tight connections between the circadian clock system and energy metabolism, circadian clock impairments (e.g., mutations or knock-out of clock genes) and circadian clock misalignments (such as during shift work and chronic jet-lag) have an adverse effect on energy metabolism, that may trigger or enhancing obese and diabetic symptoms.

Interplay between the endocrine and circadian systems in fishes

“…These hepatic leptin-a rhythms also did not shift according to the feeding time in zebrafish under an LD cycle, indicating that light is probably the dominant synchroniser (Paredes et al 2015). In addition, these daily leptin rhythms may also be regulated by rhythmic endogenous factors (hormones and foodderived metabolites), as described in mammals (Challet 2015, Kumar et al 2015. In particular, the leptin rhythm in the goldfish liver is related to plasma glucose levels (Tinoco et al 2014), with a postprandial glucose peak preceding the leptin peak, supporting the notion that leptin is induced by glucose in the hepatocytes of grass carp (Ctenopharyngodon idella; Lu et al 2015).…”

“…Leptin is predominantly expressed in the fish liver, which is an important energy-storing tissue, rather than in adipose tissue as in mammals (Gorissen & Flik 2014, Londraville et al 2014. Given its general role as an anorexigenic hormone, leptin expression is expected to increase after feeding and decrease after fasting, as reported in mammals, where plasma levels of this adipokine oscillate in a diurnal fashion, with increased values after food ingestion (Challet 2015, Kumar et al 2015. In fishes, leptin expression also exhibits an acute and transient postprandial increase in the liver, with hepatic leptin-a expression generally increasing 6 h and 9 h after feeding in teleosts such as common carp (Cyprinus carpio; Huising et al 2006), goldfish , Atlantic salmon (Moen & Finn 2013), orange-spotted grouper (Zhang et al 2013) and Mandarin fish (Siniperca chuatsi; Yuan et al 2016).…”

“…Thus, these species would be expected to experience an increase in blood leptin during the night, as this coincides with low nocturnal activity in goldfish and zebrafish. In mammals, the daily peak in circulating leptin also occurs during the fasting/sleeping period, with levels then declining before waking (reviewed in Patton & Mistlberger 2013, Challet 2015, Kumar et al 2015. All findings to date indicate that leptin facilitates a decreased appetite state during the inactive phase in animals, inhibiting the appearance of FAA.…”

Effect of Circadian Rhythm on Metabolic Processes and the Regulation of Energy Balance

“…The energy produced and stored in metabolism is used to maintain metabolic activities such as basal metabolic rate, physical activity, and thermal effect of foods [48]. Francis G Benedict first described the circadian changes in energy metabolism in 1915 [49].…”

“…One of the most important factors affecting the basal metabolic rate is the sleep pattern. Sleep and circadian rhythm are the main components of energy metabolism regulation [48,51]. There are 2 phases of sleep: rapid eye movement (REM) and non-REM [52].…”