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Circadian Regulation of Hormonal Timing and the Pathophysiology of Circadian Dysregulation

Jacob S. Moeller, Savannah R. Bever, Samantha L. Finn, Chayarndorn Phumsatitpong, Madison F. Browne, Lance J. Kriegsfeld

10.1002/cphy.c220018

Source: Volume 12, Issue 4, October 2022

Published online: September 2022

Full Article on Wiley Online Library



Abstract

Circadian rhythms are endogenously generated, daily patterns of behavior and physiology that are essential for optimal health and disease prevention. Disruptions to circadian timing are associated with a host of maladies, including metabolic disease and obesity, diabetes, heart disease, cancer, and mental health disturbances. The circadian timing system is hierarchically organized, with a master circadian clock located in the suprachiasmatic nucleus (SCN) of the anterior hypothalamus and subordinate clocks throughout the CNS and periphery. The SCN receives light information via a direct retinal pathway, synchronizing the master clock to environmental time. At the cellular level, circadian rhythms are ubiquitous, with rhythms generated by interlocking, autoregulatory transcription‐translation feedback loops. At the level of the SCN, tight cellular coupling maintains rhythms even in the absence of environmental input. The SCN, in turn, communicates timing information via the autonomic nervous system and hormonal signaling. This signaling couples individual cellular oscillators at the tissue level in extra‐SCN brain loci and the periphery and synchronizes subordinate clocks to external time. In the modern world, circadian disruption is widespread due to limited exposure to sunlight during the day, exposure to artificial light at night, and widespread use of light‐emitting electronic devices, likely contributing to an increase in the prevalence, and the progression, of a host of disease states. The present overview focuses on the circadian control of endocrine secretions, the significance of rhythms within key endocrine axes for typical, homeostatic functioning, and implications for health and disease when dysregulated. © 2022 American Physiological Society. Compr Physiol 12: 4185–4214, 2022.

Figure 1. Figure 1. The core molecular clockwork. The core intracellular mechanisms responsible for mammalian circadian rhythm generation. The process begins when CLOCK and BMAL1 proteins dimerize to drive the transcription of the Per and Cry genes. Throughout the day, PER and CRY proteins rise within the cell cytoplasm. When levels of PER and CRY reach a threshold, they form heterodimers, feed back to the cell nucleus, and negatively regulate CLOCK: BMAL1‐mediated transcription of their own genes. Levels of PER are regulated by casein kinase 1 epsilon and delta (CK1ϵ/d) which phosphorylates these proteins and marks them for degradation, thereby appropriately delaying negative feedback. AMP kinase (not pictured) similarly phosphorylates CRY proteins. Whereas Clock is constitutively expressed, a secondary feedback loop drives the transcription of Ror and Rev‐Erbα that, in turn, induce rhythms in Bmal1 transcription through stimulatory and inhibitory actions on ROR response elements (RRE) in the Bmal1 promotor, respectively. Clock‐controlled genes are tissue‐specific genes that are produced rhythmically by the CLOCK:BMAL1 complex but are not part of the clockwork mechanism (i.e., do not feed back onto the clockwork), allowing the cellular clock to broadly regulate rhythms in gene transcription required differentially across systems. Created with BioRender.com.
Figure 2. Figure 2. Circadian control of the preovulatory LH surge in spontaneously ovulating rodents. Model depicting SCN communication of kisspeptin and RFRP‐3 cells in the coordinate and E2 positive and negative feedback required for surge generation. In this model, the SCN communicates to AVPV and ARC kp cells as integration sites for circadian and steroid hormone integration. AVPV Kp cells increase activity in response to E2 and astrocyte‐derived P4. These cells receive AVP (and potentially VIP) stimulation from the SCN that initiates the surge in a time‐dependent manner, presumably due to a subordinate clockwork coordinating daily changes in AVP/VIP receptor expression. ARC Kp reduces activity in response to E2, and AVP communication from the SCN via the CSF may release ARC Kp cells from E2 inhibition to allow and stimulate these cells to further surge generation. The SCN also communicates directly to the RFRP‐3 system, also an E2‐sensitive target, to coordinate the removal of E2 negative feedback during the time of the LH surge.
Figure 3. Figure 3. Reciprocal interactions between the circadian system and the HPA axis. The SCN is synchronized to external time and communicates to the HPA axis to control rhythms in CRH secretion. In addition, autonomic projections to the adrenal lead to rhythms in sensitivity of this gland to ACTH to further influence rhythms in glucocorticoid secretion. Cortisol, in turn, acts to coordinate the phase of peripheral clocks. Created with BioRender.com.
Figure 4. Figure 4. Production of melatonin in humans. Rods and cones and intrinsically photosensitive retinal ganglion cells receive environmental light information that is subsequently communicated to the SCN via a direct retinohypothalamic tract (RHT). In turn, the SCN transmits this information to the pineal gland via a multisynaptic pathway including the paraventricular nuclei (PVN), the intermediolateral column of the spinal cord (IMC), and the superior cervical ganglia (SCG) of the sympathetic branch of the autonomic nervous system. Postganglionic sympathetic fibers stimulate the nocturnal increase of melatonin when disinhibited from SCN activity during the night. Melatonin, in turn, feeds back to the SCN to influence circadian phase. Created with BioRender.com.
Figure 5. Figure 5. Maternal‐fetal rhythm synchronization. The developing fetus is exposed to several time cues from its mother. The main signal is through melatonin secretion from the maternal pineal gland that crosses the placenta. Additional entraining signals include maternal cortisol and feeding times. In addition, the developing embryo is exposed to a rhythmic environment via clock genes that are expressed in maternal reproductive tissues, including the oviduct, uterus, and placenta. This rhythmic environment is likely required for normal fetal and postnatal development. Circadian disruptions that alter maternal endocrine timing signals impair fetal development. Clocks indicate rhythmic expression of clock genes. Created with BioRender.com.
Figure 6. Figure 6. Circadian control of neuroendocrine functioning. A hierarchy of circadian control generates broad rhythms in hormone secretion. The SCN sits at the pinnacle of this hierarchy, communicating via synaptic connectivity to neuroendocrine cells in the CNS. In turn, neuroendocrine cells exhibiting autonomous clockworks that organize their daily transcriptional activity and response to SCN signaling secrete hormones in a rhythmic fashion to act on pituitary cells containing autonomous clocks. These rhythmic patterns of pituitary hormone secretion act on target glands with cellular clockworks that further modify their response to this hormonal cascade, ultimately resulting in daily patterns of hormone activity coordinated across axes. Created with BioRender.com.


Figure 1. The core molecular clockwork. The core intracellular mechanisms responsible for mammalian circadian rhythm generation. The process begins when CLOCK and BMAL1 proteins dimerize to drive the transcription of the Per and Cry genes. Throughout the day, PER and CRY proteins rise within the cell cytoplasm. When levels of PER and CRY reach a threshold, they form heterodimers, feed back to the cell nucleus, and negatively regulate CLOCK: BMAL1‐mediated transcription of their own genes. Levels of PER are regulated by casein kinase 1 epsilon and delta (CK1ϵ/d) which phosphorylates these proteins and marks them for degradation, thereby appropriately delaying negative feedback. AMP kinase (not pictured) similarly phosphorylates CRY proteins. Whereas Clock is constitutively expressed, a secondary feedback loop drives the transcription of Ror and Rev‐Erbα that, in turn, induce rhythms in Bmal1 transcription through stimulatory and inhibitory actions on ROR response elements (RRE) in the Bmal1 promotor, respectively. Clock‐controlled genes are tissue‐specific genes that are produced rhythmically by the CLOCK:BMAL1 complex but are not part of the clockwork mechanism (i.e., do not feed back onto the clockwork), allowing the cellular clock to broadly regulate rhythms in gene transcription required differentially across systems. Created with BioRender.com.


Figure 2. Circadian control of the preovulatory LH surge in spontaneously ovulating rodents. Model depicting SCN communication of kisspeptin and RFRP‐3 cells in the coordinate and E2 positive and negative feedback required for surge generation. In this model, the SCN communicates to AVPV and ARC kp cells as integration sites for circadian and steroid hormone integration. AVPV Kp cells increase activity in response to E2 and astrocyte‐derived P4. These cells receive AVP (and potentially VIP) stimulation from the SCN that initiates the surge in a time‐dependent manner, presumably due to a subordinate clockwork coordinating daily changes in AVP/VIP receptor expression. ARC Kp reduces activity in response to E2, and AVP communication from the SCN via the CSF may release ARC Kp cells from E2 inhibition to allow and stimulate these cells to further surge generation. The SCN also communicates directly to the RFRP‐3 system, also an E2‐sensitive target, to coordinate the removal of E2 negative feedback during the time of the LH surge.


Figure 3. Reciprocal interactions between the circadian system and the HPA axis. The SCN is synchronized to external time and communicates to the HPA axis to control rhythms in CRH secretion. In addition, autonomic projections to the adrenal lead to rhythms in sensitivity of this gland to ACTH to further influence rhythms in glucocorticoid secretion. Cortisol, in turn, acts to coordinate the phase of peripheral clocks. Created with BioRender.com.


Figure 4. Production of melatonin in humans. Rods and cones and intrinsically photosensitive retinal ganglion cells receive environmental light information that is subsequently communicated to the SCN via a direct retinohypothalamic tract (RHT). In turn, the SCN transmits this information to the pineal gland via a multisynaptic pathway including the paraventricular nuclei (PVN), the intermediolateral column of the spinal cord (IMC), and the superior cervical ganglia (SCG) of the sympathetic branch of the autonomic nervous system. Postganglionic sympathetic fibers stimulate the nocturnal increase of melatonin when disinhibited from SCN activity during the night. Melatonin, in turn, feeds back to the SCN to influence circadian phase. Created with BioRender.com.


Figure 5. Maternal‐fetal rhythm synchronization. The developing fetus is exposed to several time cues from its mother. The main signal is through melatonin secretion from the maternal pineal gland that crosses the placenta. Additional entraining signals include maternal cortisol and feeding times. In addition, the developing embryo is exposed to a rhythmic environment via clock genes that are expressed in maternal reproductive tissues, including the oviduct, uterus, and placenta. This rhythmic environment is likely required for normal fetal and postnatal development. Circadian disruptions that alter maternal endocrine timing signals impair fetal development. Clocks indicate rhythmic expression of clock genes. Created with BioRender.com.


Figure 6. Circadian control of neuroendocrine functioning. A hierarchy of circadian control generates broad rhythms in hormone secretion. The SCN sits at the pinnacle of this hierarchy, communicating via synaptic connectivity to neuroendocrine cells in the CNS. In turn, neuroendocrine cells exhibiting autonomous clockworks that organize their daily transcriptional activity and response to SCN signaling secrete hormones in a rhythmic fashion to act on pituitary cells containing autonomous clocks. These rhythmic patterns of pituitary hormone secretion act on target glands with cellular clockworks that further modify their response to this hormonal cascade, ultimately resulting in daily patterns of hormone activity coordinated across axes. Created with BioRender.com.
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Article Title: Circadian Regulation of Hormonal Timing and the Pathophysiology of Circadian Dysregulation
 

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Jacob S. Moeller, Savannah R. Bever, Samantha L. Finn, Chayarndorn Phumsatitpong, Madison F. Browne, Lance J. Kriegsfeld. Circadian Regulation of Hormonal Timing and the Pathophysiology of Circadian Dysregulation. Compr Physiol 2022, 12: 4185-4214. doi: 10.1002/cphy.c220018