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Glucocorticoid regulation of the circadian clock modulates glucose homeostasis
Open accessAbstract
Circadian clock genes are regulated by glucocorticoids; however, whether this regulation is a direct or secondary effect and the physiological consequences of this regulation were unknown. Here, we identified glucocorticoid response elements (GREs) at multiple clock genes and showed that 3 were directly regulated by the glucocorticoid receptor. We determined that a GRE within the core clock gene Per2 was continuously occupied during rhythmic expression and essential for glucocorticoid regulation of that gene in vivo. We further demonstrated that mice with a genomic deletion spanning this GRE expressed elevated leptin levels and were protected from glucose intolerance and insulin resistance on glucocorticoid treatment but not from muscle wasting. We conclude that Per2 is an integral component of a particular glucocorticoid regulatory pathway and that glucocorticoid regulation of the peripheral clock is selectively required for some actions of glucocorticoids.
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“Resetting of the peripheral clock occurs through well-defined molecular mechanisms that involve direct interaction of glucocorticoids, glucocorticoid response elements and the regulatory regions of core clock genes Bmal1, Cry1, Per1 and Per2 [63, 64].”
From Sleep, testosterone and cortisol balance, and ageing men (2022) · cites this paper as [64]
Experimental — accuracy not yet measuredIn the citing paper
“Per2 null mice exhibit no glucocorticoid oscillations, indicating that PER2 may also impact glucocorticoid receptor (GR)-dependent glucose metabolism [24,25].”
From Circadian control of glucose metabolism (2014) · cites this paper as [24]
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“In response to glucocorticoids, GR binds to GREs in PER1 and PER2 genes to regulate their rhythmic expression (So et al. 2009).”
BackgroundAdrenal and Glucocorticoid Effects on the Circadian Rhythm of Murine Intraocular Pressure
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“Glucocorticoids bind and activate GRs to bind to glucocorticoid response elements in DNA, which are located in the promoter regions of clock genes, such as Per1 and Per2, and modulate gene transcription.(25) Additionally, circadian clock components such as CLOCK and CRY proteins can interact with the GRs and inhibit t…”
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Epilepsy, gut microbiota, and circadian rhythm
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“68 In agreement with this finding, exposure of murine and human mesenchymal stem cells from bone marrow to dexamethasone triggers oscillatory expression of clock-related genes.”
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“Indeed, while Per1 carries a canonical GRE, Per2 has an intronic binding sequence that confers GR responsiveness to the gene (So et al., 2009).”
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“Glucose and lipid metabolism in the liver and adipose tissue exhibit circadian variations due, at least in part, to circadian expression of key enzymes in these pathways (Lamia et al., 2008; Panda et al., 2002; So et al., 2009; Zvonic et al., 2006).”
BackgroundResetting the Aging Clock: Implications for Managing Age-Related Diseases
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“P values for the rhythmicity of DBP, PER2, and BMAL1 were determined by a cosinor analysis with p = 0.04, p = 0.12, and p < 0.01 in U2OS cells; p = 0.02, p = 0.35, and p = 0.43 in hiPSCs; and p < 0.01, p < 0.01, and p < 0.01 in MEF.”
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Core clock regulators in dexamethasone-treated HEK 293T cells at 4 h intervals
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“Moreover, it has been reported that CLOCK is relatively unresponsive to glucocorticoid clock resetting [16].”
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“50 At the Kcnh2 locus, motif analysis identified 2 GR binding sites, and we observed significant ChIP enrichment for the conserved site located +1.2 kb from the transcription start site (Figure 2E, left).”
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“(Balsalobre et al. 2000; Chen et al. 2017; Nagoshi et al. 2004; So et al. 2009), and light is known to generate robust oscillations of core clock genes in the”
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“This interaction is bidirectional, as the “clock” genes (e.g., PER1, PER2, TIMELESS, NPAS2) that generate circadian rhythms are shown to be regulated by stress hormones like cortisol (Segall et al., 2009; So et al., 2009).”
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“Maladaptive alterations to hormone signaling that is prevalent in BCa result in dysregulated expression of hormone-regulated clock genes, cascading onto the entire circadian molecular network owing to its interdependent nature [10, 11, 56, 59].”
BackgroundMethodRigid Cooperation of Per1 and Per2 proteins
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“GR has been shown to regulate E4BP4 transcription via a GR binding sequence (GBS) located ~5kb upstream of the transcription start site [28, 29].”
BackgroundChronic stress, gut microbiota, and immunity: interconnections and implications for health
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“identified glucocorticoid response elements in the molecular circadian clock and found that PER2 was an integral component of the glucocorticoid regulatory pathway and was directly regulated by the glucocorticoid receptor [40].”
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“, corticosteroids, shift the phase of the molecular oscillator through regulation of clock protein (PER and REVERBα) expression (13).”
Modulation of the circadian clock by glucocorticoid receptor isoforms in the H295R cell line
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BackgroundInduced Torpor as a Countermeasure for Low Dose Radiation Exposure in a Zebrafish Model
Cahill, T., da Silveira, W. A., Renaud, L., Williamson, T., Wang, H., Chung, D., Overton, I. M., Chan, S. S. L., & Hardiman, G. (2021) · Cells · doi:10.3390/cells10040906 · Cited by 11
Circadian Regulation of Hormonal Timing and the Pathophysiology of Circadian Dysregulation
Moeller, J., Bever, S. R., Finn, S. L., Phumsatitpong, C., Browne, M. F., & Kriegsfeld, L. J. (2022) · Comprehensive physiology · doi:10.1002/cphy.c220018 · Cited by 21
“As mentioned previously, some clock genes have a GRE in their promoter region (447) and, in peripheral tissues, clock gene expression can be entrained by glucocorticoid treatment (26, 380) (Figure 3).”
Gomez, A. M., Wu, Y., Zhang, C., Boyd, L., Wee, T.-L., Gewolb, J., Amor, C., Cheadle, L., & Borniger, J. C. (2025) · Neuron · doi:10.1016/j.neuron.2025.11.019 · Cited by 17
Maskal, J. M., Brito, L. F., Duttlinger, A. W., Kpodo, K. R., McConn, B. R., Byrd, C. J., Richert, B. T., Marchant, J. N., Lay, D. C., Jr., Perry, S. D., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-01889-w · Cited by 10
The importance of the circadian trough in glucocorticoid signaling: a variation on B-flat
Meijer, O. C., Kooijman, S., Kroon, J., & Winter, E. M. (2023) · Stress · doi:10.1080/10253890.2023.2275210 · Cited by 10
“…function, but GR also affects the molecular clock. this includes GRe-mediated transcriptional regulation of the Per1 gene (Balsalobre et al., 2000; So et al., 2009), but also regulation of many other genes, as evidence by prednisolone-induced effects in the rat hippocampus (Birnie et al., 2023).…”
BackgroundSumová, A., & Sládek, M. (2024) · Physiological Research · doi:10.33549/physiolres.935304 · Cited by 12
Xydous, M., Sekeri‐Pataryas, K. E., Prombona, A., & Sourlingas, T. G. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.03.001 · Cited by 10
“Unlike mper1, the mper2 gene does not include a glucocorticoid response element upstream of the transcription start site and does not exhibit an “acute response” to dexamethasone, as first shown by Balsalobre et al., 2000 [9], despite the presence of a strong GRE element downstream of the TSS [42].”
Joo, J., Cox, C., Kindred, E. D., Lashinger, L. M., Young, M. E., & Bray, M. S. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.80 · Cited by 10
Phase-Dependent Shifting of the Adrenal Clock by Acute Stress-Induced ACTH
Engeland, W. C., Yoder, J. M., Karsten, C. A., & Kofuji, P. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00081 · Cited by 10
“Activation of glucocorticoid receptors by dexamethasone can entrain other peripheral clocks (14, 15).”
BackgroundGlucocorticoid receptor epigenetic activity in the heart
Akinborewa, O., & Quattrocelli, M. (2025) · Epigenetics · doi:10.1080/15592294.2025.2468113 · Cited by 10
“It is well-known that glucocorticoids follow a strong circadian rhythm in their secretion, peaking at the beginning of the feeding phase – early night in rodents and early morning in humans [91–95].”
Xie, Z., Ahmad, I. M., Zuo, L., Xiao, F., Wang, Y., & Li, D. (2021) · Integrative Zoology · doi:10.1111/1749-4877.12613 · Cited by 11
Xydous, M., Prombona, A., & Sourlingas, T. G. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.07.011 · Cited by 12
Soto-Rivera, C. L., & Majzoub, J. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804169-7.00003-9 · Cited by 9
Corticosteroids and circadian rhythms in the cardiovascular system
Kanki, M., & Young, M. J. (2020) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2020.10.007 · Cited by 9
The trophoblast clock controls transport across placenta in mice
Demarez, C., de Assis, L. V. M., Krohn, M., Ramella, N. A., Schwaninger, M., Oster, H., & Astiz, M. (2021) · Development · doi:10.1242/dev.197673 · Cited by 9
“The SCN perceives time of day via direct photic input from the retina and subsequently relays temporal information to peripheral clocks, present in almost all cells in the body, by humoral and neuronal pathways (Dibner et al., 2010; Husse et al., 2015; Schibler et al., 2003; So et al., 2009).”
BackgroundKong, X., Ota, S. M., Suchecki, D., Lan, A., Peereboom, A. I., Hut, R. A., & Meerlo, P. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304211065336 · Cited by 9
“Glucocorticoids such as CORT bind with GR’s, which then can modulate the transcription of many genes, including Per2 and other clock genes, by binding to glucocorticoid responsive elements (GRE) in the promoter region (Balsalobre et al., 2000; So et al., 2009; Cheon et al., 2013; Dickmeis et al., 2013; Oster et al., 2…”
BackgroundChen, K. Y., Angulo, A. D., Guo, X., More, A., Ochsner, S. A., Lopez, E., Saul, D., Pang, W., Sun, Y., McKenna, N. J., et al. (2022) · Frontiers in Aging · doi:10.3389/fragi.2021.803482 · Cited by 8
Input integration by the circadian clock exhibits nonadditivity and fold-change detection
Manella, G., Bolshette, N. B., Golik, M., & Asher, G. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2209933119 · Cited by 8
Nobiletin Stimulates Adrenal Hormones and Modulates the Circadian Clock in Mice
Ryan, C., Tahara, Y., Haraguchi, A., Lu, Y., & Shibata, S. (2024) · Nutrients · doi:10.3390/nu16101491 · Cited by 8
“Corticosterone regulates Per1 and Per2 expression via glucocorticoid receptors and adrenaline via the cAMP-CREB pathway [17].”
BackgroundProtective Effects and Mechanisms of Melatonin on Stress Myocardial Injury in Rats
Chen, J.-Y., Li, T., Wang, J.-L., Wang, Z.-L., Zhang, Y., & Zang, L. (2022) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000001312 · Cited by 8
Zhu, L., Yu, J., Zhang, W., XIE, B., & Zhu, Y. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2559 · Cited by 8
“The CRF/arginine-vasopressin immunoreactive neuronal projection to the hypothalamic paraventricular nucleus causes hypothalamic CRF release and leads to activation of the HPA axis, inducing rhythmic release of glucocorticoids in the adrenal gland (41-43) (Fig.”
Expression of Clock Genes in Human Subcutaneous and Visceral Adipose Tissues
Zanquetta, M. M., Corrêa‐Giannella, M. L., Giannella‐Neto, D., Alonso, P. A., Guimaraes, L. M. M. V., Meyer, A., & Villares, S. M. (2012) · Chronobiology International · doi:10.3109/07420528.2012.657319 · Cited by 8
“…female subjects occurs as a cause or as a consequence of weight gain, as well as the relationship to hormonal (glucocorticoids, leptin) and metabolic (glycemia, ethanol consumption) variables known to affect the expression of these genes (Ando et al., 2010a; Mendoza et al., 2011; So et al., 2009).”
BackgroundLovdel, A., Suchacki, K. J., Roberts, F. L., Sulston, R. J., Wallace, R. J., Thomas, B. J., Bell, R. M. B., Cervera, I. P., Macpherson, G. J., Morton, N. M., et al. (2024) · Journal of Endocrinology · doi:10.1530/joe-24-0072 · Cited by 7
“…so, we used qPCR to measure the expression of the glucocorticoid target genes Fkbp5, Tsc22d3 (also known as Gilz ), and Per1 ( D’Adamio et al. 1997, So et al. 2009, Lee et al. 2011, Reddy et al. 2012, Suarez et al. 2012, Pereira et al. 2014) in BM and WAT from the same mice that had undergone LC–…”
MethodMehranfard, N., Ghasemi, M., & Saboory, E. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70065 · Cited by 7
Sládek, M., Lužná, V., Houdek, P., & Sumová, A. (2025) · Acta Physiologica · doi:10.1111/apha.70138 · Cited by 7
Kusunose, N., Matsunaga, N., Kimoto, K., Akamine, T., Hamamura, K., Koyanagi, S., Ohdo, S., & Kubota, T. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.09.086 · Cited by 7
Conserved immunomodulatory transcriptional networks underlie antipsychotic-induced weight gain
Zapata, R. C., Chaudry, B. S., Valencia, M. L., Zhang, D., Ochsner, S. A., McKenna, N. J., & Osborn, O. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01528-y · Cited by 7
“Given the wealth of studies connecting circadian rhythms and metabolic dysfunction, and our recent observations of the importance of circadian rhythms in AIWG [41], we were interested to note significant intersections of the AIWG-P gene set with HCTs of several transcription factors with characterized roles in circadi…”
BackgroundBuurstede, J. C., Umeoka, E. H. D. L., da Silva, M. S., Krugers, H. J., Joëls, M., & Meijer, O. C. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109186 · Cited by 8
“This is not trivial, since in mice such an approach has been possible only on a single occasion, based on a fortuitous naturally occurring deletion in the mouse genome (So et al., 2009).”
BackgroundYang, D., Oike, H., Furuse, M., & Yasuo, S. (2021) · Chronobiology International · doi:10.1080/07420528.2021.1977654 · Cited by 7
“After the binding of glucocorticoids to the receptors, ligand-receptor complexes translocate to the nucleus and bind to the glucocorticoid response elements (GREs) present on the promoters of core clock genes, such as Per1 and Per2 (Cheon et al. 2013; So et al. 2009).”
BackgroundFasting during the ramadan: a challenge for patients with adrenal insufficiency
Debono, M. (2017) · Endocrine · doi:10.1007/s12020-017-1329-y · Cited by 7
“The cortisol rhythm regulates other bodily rhythms and acts as a secondary messenger between the central clock and peripheral clocks in different tissues and cells [3].”
BackgroundHansen, S. B., Frederiksen, J. S. S., Lodberg, A., Poulsen, M. F., Andersen, C. B. F., Oster, H., Jessen, N., & Jørgensen, J. O. L. (2025) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaf564 · Cited by 5
Metadata
- Authors
- So, A. Y.-L., Bernal, T. U., Pillsbury, M. L., Yamamoto, K. R., & Feldman, B. J.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-10-13
- Volume
- 106
- Issue
- 41
- Pages
- 17582-17587
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2757402
- OpenAlex
- W1998522501
- Cited by
- 431
- References
- 51
- Citations by year
- 2026: 15 · 2025: 26 · 2024: 37 · 2023: 19 · 2022: 36 · 2021: 28 · 2020: 32 · 2019: 28 · 2018: 22 · 2017: 28 · 2016: 33 · 2015: 23 · 2014: 25 · 2013: 20 · 2012: 18
- FWCI
- 8.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- University of California, San Francisco
- National Cancer Institute (CA20535, R01CA020535, R37CA020535)
- National Institute of General Medical Sciences (R25GM056847, GM 56847)
- National Institute of Diabetes and Digestive and Kidney Diseases (K08DK073697, DK73697)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- glucocorticoids, circadian clock, clock genes, glucocorticoid response element, glucocorticoid receptor, Per2, glucose homeostasis, insulin resistance, impaired glucose tolerance, leptin, muscle atrophy, peripheral clocks
- MeSH terms
- Animals, Circadian Rhythm, Gene Expression Regulation, Glucocorticoids, Glucose, Homeostasis, Nuclear Proteins, Transcription Factors, Transcription, Genetic, Polymerase Chain Reaction, Cell Cycle Proteins, Leptin, Mice, Period Circadian Proteins, Mesenchymal Stem Cells
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