Phase-dependent resetting of the adrenal clock by ACTH in vitro

Yoder, J. Marina; Brandeland, Megan; Engeland, William C.

doi:10.1152/ajpregu.00519.2013

Cited by 29 publications

(28 citation statements)

References 53 publications

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“…We have shown that the adrenal clock is phase shifted by ACTH in vitro and that the phase shift is phase dependent (47). However, our in vitro experiments showed that ACTH produced a phase delay in the adrenal PER2Luc rhythm when administered at a circadian time analogous to the active phase of the rhythm, but no phase advance at the circadian time representing the inactive phase.…”

Section: Discussionmentioning

confidence: 58%

“…Adrenals and anterior pituitaries were rapidly excised and placed in cold Hank's Balanced Salt Solution. Cleaned and hemisected adrenals or whole pituitaries were cultured on Millicell organotypic inserts in a 35-mm Petri dish with 1.5 ml of warmed culture media (Dulbecco's Modified Eagle Media without phenol red) supplemented with luciferin and penicillinstreptomycin as described previously (47,48). Dishes were sealed with circular glass coverslips and silicon grease.…”

Section: Methodsmentioning

confidence: 99%

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Chronic subordination stress phase advances adrenal and anterior pituitary clock gene rhythms

Razzoli¹,

Karsten

Yoder

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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Circadian rhythms in glucocorticoids are the product of interactions between the hypothalamic-pituitary-adrenal (HPA) axis and the mammalian clock gene system. The adrenal clock can generate the glucocorticoid rhythm that in turn synchronizes other peripheral clocks to maintain homeostasis. Stress acutely activates and chronically upregulates the HPA axis, suggesting that the adrenal clock could be modulated by stress. However, there is no direct evidence that stress affects the adrenal clock rhythm. We tested the hypothesis that a model of chronic subordination stress (CSS) that has a major impact on HPA axis regulation, metabolism, and emotional behavior alters adrenal and pituitary clock gene rhythms. Clock gene rhythms were assessed using mPER2::Luciferase (PER2Luc) knockin mice in which in vitro bioluminescence rhythms reflect the Per2 clock gene expression. PER2Luc mice that experienced CSS for 2 wk showed positive energy balance reflected by increased body weight and food intake. Additionally, CSS phase advanced the adrenal (∼2 h) and the pituitary (∼1 h) PER2Luc rhythm compared with control mice. The activity rhythm was not affected. The adrenal clock phase shift was associated with increased feed conversion efficiency, suggesting that the metabolic phenotype in CSS mice may be related to altered adrenal clock rhythmicity. Interestingly, a single subordination experience followed by 8 h sensory housing also phase advanced the adrenal, but not the pituitary, PER2Luc rhythm. Overall, these data demonstrate a stress-induced phase shift in a peripheral clock gene rhythm and differential stress sensitivity of two peripheral clocks within the HPA axis, suggesting a link between clock desynchrony and individual vulnerability to stress.

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Section: Discussionmentioning

confidence: 58%

Section: Methodsmentioning

confidence: 99%

Chronic subordination stress phase advances adrenal and anterior pituitary clock gene rhythms

Razzoli¹,

Karsten

Yoder

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Peripheral tissues (adrenal gland, cornea, lung, liver, spleen and anterior pituitary) were rapidly dissected and placed in ice-cold Hank's solution. Each tissue explant was placed on a membrane (0.4μm, 30 mm in diameter, Millicell cell culture inserts; Millipore, Billerica, MA, USA) in a 35 mm Petri dish, sealed with vacuum grease, and cultured in 1.1 ml DMEM containing 10 mM HEPES, 0.1 mM Luciferin (Promega, Madison, WI), 25 units/ml penicillin, 25 μg/ml streptomycin (Gibco, Grand island, NY), and 2% B27 (Gibco) as described previously [19]. Cultures were incubated at 37°C, and bioluminescence was monitored for 1 min at 7.5-min intervals using a LumiCycle luminometer (Actimetrics, Evanston, IL).…”

Section: Methodsmentioning

confidence: 99%

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

et al. 2016

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Light is a powerful entrainer of circadian clocks in almost all eukaryotic organisms promoting synchronization of internal circadian rhythms with external environmental light-dark (LD) cycles. In mammals, the circadian system is organized in a hierarchical manner, in which a central pacemaker in the suprachiasmatic nucleus (SCN) synchronizes oscillators in peripheral tissues. Recent evidence demonstrates that photoentrainment of the SCN proceeds via signaling from a subpopulation of retinal ganglion cells (RGCs) which are melanopsin-expressing and intrinsically photosensitive (ipRGCs). However, it is still unclear whether photoentrainment of peripheral clocks is mediated exclusively by the ipRGC system or if signaling from RGCs that do not express melanopsin also plays a role. Here we have used genetic “silencing” of ipRGC neurotransmission in mice to investigate whether this photoreceptive system is obligatory for the photoentrainment of peripheral circadian clocks. Genetic silencing of ipRGC neurotransmission in mice was achieved by expression of tetanus toxin light chain in melanopsin-expressing cells (Opn4::TeNT mouse line). Rhythms of the clock gene Period 2 in various peripheral tissues were measured by crossbreeding Opn4::TeNT mice with PER2 luciferase knock-in mice (mPER2Luc). We found that in Opn4::TeNT mice the pupillary light reflex, light modulation of activity, and circadian photoentrainment of locomotor activity were severely impaired. Furthermore, ex vivo cultures from Opn4::TeNT, mPER2Luc mice of the adrenal gland, cornea, lung, liver, pituitary and spleen exhibited robust circadian rhythms of PER2::LUC bioluminescence. However, their peak bioluminescence rhythms were not aligned to the projected LD cycles indicating their lack of photic entrainment in vivo. Finally, we found that the circadian rhythm in adrenal corticosterone in Opn4::TeNT mice, as monitored by in vivo subcutaneous microdialysis, was desynchronized from environmental LD cycles. Our findings reveal a non-redundant role of ipRGCs for photic entrainment of peripheral tissues, highlighting the importance of this photoreceptive system for the organismal adaptation to daily environmental LD cycles.

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“…The light pulse data discussed above suggest that adrenal clocks are entrained by neuronal mechanisms (Buijs et al 1999, Ishida et al 2005. However, Yoder and coworkers recently found that ACTH itself can also shift the phase of the adrenal Per2 rhythm (Yoder et al 2014). One might speculate that, in this way, stress-induced HPA axis activation can reset adrenal clocks, thus affecting circadian GC release.…”

Section: Circadian Regulation Of the Hpa Axismentioning

confidence: 97%

Endocrine regulation of circadian physiology

Tsang

Astiz

Friedrichs

et al. 2016

Journal of Endocrinology

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Endogenous circadian clocks regulate 24-h rhythms of behavior and physiology to align with external time. The endocrine system serves as a major clock output to regulate various biological processes. Recent findings suggest that some of the rhythmic hormones can also provide feedback to the circadian system at various levels, thus contributing to maintaining the robustness of endogenous rhythmicity. This delicate balance of clock-hormone interaction is vulnerable to modern lifestyle factors such as shiftwork or high-calorie diets, altering physiological set points. In this review, we summarize the current knowledge on the communication between the circadian timing and endocrine systems, with a focus on adrenal glucocorticoids and metabolic peptide hormones. We explore the potential role of hormones as systemic feedback signals to adjust clock function and their relevance for the maintenance of physiological and metabolic circadian homeostasis.

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Phase-dependent resetting of the adrenal clock by ACTH in vitro

Cited by 29 publications

References 53 publications

Chronic subordination stress phase advances adrenal and anterior pituitary clock gene rhythms

Chronic subordination stress phase advances adrenal and anterior pituitary clock gene rhythms

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

Endocrine regulation of circadian physiology

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