Food‐entrainable circadian oscillators in the brain

Verwey, Michael; Amir, Shimon

doi:10.1111/j.1460-9568.2009.06960.x

Cited by 102 publications

(87 citation statements)

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“…Results were not caused by lesion of the SCN. It has been shown previously that entrainment of both activity and temperature rhythms to a restricted feeding schedule persists in SCN-lesioned rats (54,6,57,34). In addition, examination of the SCN histology in this experiment indicates that the SCN was not damaged by the Arc Lep-SAP injections, as also shown previously in experiments using the same Lep-SAP injection parameters (28).…”

Section: Discussionsupporting

confidence: 66%

Leptin-sensitive neurons in the arcuate nucleus integrate activity and temperature circadian rhythms and anticipatory responses to food restriction

Wiater

Dinh

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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Wiater MF, Li A-J, Dinh TT, Jansen HT, Ritter S. Leptin-sensitive neurons in the arcuate nucleus integrate activity and temperature circadian rhythms and anticipatory responses to food restriction. Am J Physiol Regul Integr Comp Physiol 305: R949 -R960, 2013. First published August 28, 2013 doi:10.1152/ajpregu.00032.2013.-Previously, we investigated the role of neuropeptide Y and leptin-sensitive networks in the mediobasal hypothalamus in sleep and feeding and found profound homeostatic and circadian deficits with an intact suprachiasmatic nucleus. We propose that the arcuate nuclei (Arc) are required for the integration of homeostatic circadian systems, including temperature and activity. We tested this hypothesis using saporin toxin conjugated to leptin (Lep-SAP) injected into Arc in rats. Lep-SAP rats became obese and hyperphagic and progressed through a dynamic phase to a static phase of growth. Circadian rhythms were examined over 49 days during the static phase. Rats were maintained on a 12:12-h light-dark (LD) schedule for 13 days and, thereafter, maintained in continuous dark (DD). After the first 13 days of DD, food was restricted to 4 h/day for 10 days. We found that the activity of Lep-SAP rats was arrhythmic in DD, but that food anticipatory activity was, nevertheless, entrainable to the restricted feeding schedule, and the entrained rhythm persisted during the subsequent 3-day fast in DD. Thus, for activity, the circuitry for the light-entrainable oscillator, but not for the food-entrainable oscillator, was disabled by the Arc lesion. In contrast, temperature remained rhythmic in DD in the Lep-SAP rats and did not entrain to restricted feeding. We conclude that the leptin-sensitive network that includes the Arc is required for entrainment of activity by photic cues and entrainment of temperature by food, but is not required for entrainment of activity by food or temperature by photic cues.feeding; obesity; hypothalamus; saporin; BMAL-1; glucose THE ARCUATE NUCLEUS (ARC) of the hypothalamus is a key site for the regulation of feeding, adiposity, and metabolism, which is dependent on the adipose tissue-derived hormone leptin (19,56). Receptors for leptin occur densely in the Arc and are often coexpressed with neuropeptide Y (NPY) (3, 52). The mediobasal hypothalamus, including the Arc, contributes to the hypothalamic control of circadian rhythms, including feeding and rest/activity (22,49,59,28). Obese Zucker rats lacking leptin receptors maintain modified light-entrained temperature and locomotor rhythms and enhanced food anticipatory activity (41, 37). Diet-induced obesity decreases food anticipatory activity (43), suggesting that the Arc leptin/NPY circuits are critical to the anticipation of scheduled food availability, inhibiting activity when leptin levels are enhanced by obesity and facilitating activity when leptin signaling is absent (38). Similar observations in obese lesioned rats for core body temperature (Tb), activity, and food anticipation have been reported for rats with electrolytic...

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Section: Discussionsupporting

confidence: 66%

Leptin-sensitive neurons in the arcuate nucleus integrate activity and temperature circadian rhythms and anticipatory responses to food restriction

Wiater

Dinh

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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“…These food-entrained rhythms are accompanied by phase resetting of the molecular clock in the brain (4,5) and various peripheral tissues (6), but not in the light-entrainable pacemaker, the suprachiasmatic nucleus (SCN) (4,5). In the brain, a network of structures such as the cerebral cortex, hippocampus, dorsal medial hypothalamic nucleus, and cerebellum are entrained by food and may participate in regulating RF-dependent biological rhythms (4,7,8).…”

mentioning

confidence: 99%

“…PKCα also mediates light entrainment by stabilizing PER2 in the SCN (11), whereas both PKCα and PKCγ may phosphorylate and activate CLOCK in response to serum stimulation (12). Unlike PKCα, PKCγ is neuronspecific, with the most abundant expression in the cerebral cortex, hippocampus, and cerebellum (16), all of which are regions that can be entrained by food (4,7,8), whereas there is little or no expression in the SCN (14). Here we set out to investigate whether PKCγ plays a role in food entrainment to further reveal the molecular mechanism regarding the resetting of the circadian clock by RF.…”

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confidence: 99%

PKCγ participates in food entrainment by regulating BMAL1

Zhang¹,

Abraham

Lin³

et al. 2012

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

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Temporally restricted feeding (RF) can phase reset the circadian clocks in numerous tissues in mammals, contributing to altered timing of behavioral and physiological rhythms. However, little is known regarding the underlying molecular mechanism. Here we demonstrate a role for the gamma isotype of protein kinase C (PKCγ) in food-mediated entrainment of behavior and the molecular clock. We found that daytime RF reduced late-night activity in wild-type mice but not mice homozygous for a null mutation of PKCγ (PKCγ). Molecular analysis revealed that PKCγ exhibited RF-induced changes in activation patterns in the cerebral cortex and that RF failed to substantially phase shift the oscillation of clock gene transcripts in the absence of PKCγ. PKCγ exerts effects on the clock, at least in part, by stabilizing the core clock component brain and muscle aryl hydrocarbon receptor nuclear translocator like 1 (BMAL1) and reducing its ubiquitylation in a deubiquitination-dependent manner. Taken together, these results suggest that PKCγ plays a role in food entrainment by regulating BMAL1 stability.

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“…Recent molecular tools and genetic manipulations in rodents have allowed the search and identification of food-entrained clocks in the whole body including the central nervous system and peripheral tissues (e.g., liver, stomach, and intestines; Stokkan, Yamazaki, Tei, Sakaki, & Menaker, 2001;Davidson, Poole, Yamazaki, & Menaker, 2003;Verwey & Amir, 2009;Mendoza, Pévet, Felder-Schmittbuhl, Bailly, & Challet, 2010). The discovery of these food-entrained clocks in the whole body has led to propositions that food anticipatory rhythms are controlled by interactions between peripheral and central food-entrained clocks (Escobar, Cailotto, Angeles-Castellanos, Delgado, & Buijs, 2009).…”

Section: Introductionmentioning

confidence: 99%

Daily anticipatory rhythms of behavior and body temperature in response to glucose availability in rats.

Carneiro

Fernandes

Medeiros

et al. 2012

Psychology & Neuroscience

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When food is available recurrently at a particular time of day, several species increase their locomotion in the hours that precede food delivery, a phenomenon called food anticipatory activity (FAA). In mammals, many studies have shown that FAA is driven by a food-entrained circadian oscillator (FEO) that is distinct from the light-entrained pacemaker in the suprachiasmatic nucleus of the hypothalamus. Few studies have investigated the effect of sugar ingestion on food anticipatory rhythms and the FEO. We aimed to extend the understanding of the role of glucose on the emergence of food anticipatory rhythms by investigating whether glucose ingestion is sufficient to produce daily food anticipation, reflected by motor activity and core body temperature rhythms. Under a 12 h/12 h light/dark cycle, chow-deprived rats had glucose solution available between Zeitgeber Time (ZT) 6 and ZT 9 for 10 days (glucose restriction group), whereas control animals had chow available within the same time window (chow restriction group). Animals in both groups exhibited anticipatory motor activity and body temperature around the fourth day of the scheduled food restriction. Glucose-fed rats ingested ~15 kcal on the days immediately before FAA emergence and reached an intake of ~20 kcal/day, whereas chow-fed rats ingested ~40 kcal/day. The glucose restriction group exhibited a pattern of food anticipation (activity and temperature) that was extremely similar to that observed in the chow restriction group. We conclude that glucose ingestion is a sufficient temporal cue to produce recurrent food anticipation, reflected by activity and temperature rhythms, in rats.

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Food‐entrainable circadian oscillators in the brain

Cited by 102 publications

References 104 publications

Leptin-sensitive neurons in the arcuate nucleus integrate activity and temperature circadian rhythms and anticipatory responses to food restriction

Leptin-sensitive neurons in the arcuate nucleus integrate activity and temperature circadian rhythms and anticipatory responses to food restriction

PKCγ participates in food entrainment by regulating BMAL1

Daily anticipatory rhythms of behavior and body temperature in response to glucose availability in rats.

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