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The Meter of Metabolism
Open accessAbstract
The circadian system orchestrates the temporal organization of many aspects of physiology, including metabolism, in synchrony with the 24 hr rotation of the Earth. Like the metabolic system, the circadian system is a complex feedback network that involves interactions between the central nervous system and peripheral tissues. Emerging evidence suggests that circadian regulation is intimately linked to metabolic homeostasis and that dysregulation of circadian rhythms can contribute to disease. Conversely, metabolic signals also feed back into the circadian system, modulating circadian gene expression and behavior. Here, we review the relationship between the circadian and metabolic systems and the implications for cardiovascular disease, obesity, and diabetes.
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“The term chrono-nutrition was introduced in 1986 by Delabois (10) but was not much used beyond its application in weight loss diets.”
From Meal irregularity and cardiometabolic consequences: results from observational and intervention studies (2016) · cites this paper as [10]
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“Each endpoint was adjusted for age and regularly updated information throughout follow-up on: alcohol consumption, physical exercise, multivitamin use, menopausal status and postmenopausal hormone use, physical examination in the past 2 years, healthy eating score37 (without components of multivitamin and alcohol, which were adjusted individually), smoking status, pack-years, and BMI.”
From Total and Cause-Specific Mortality of U.S. Nurses Working Rotating Night Shifts (2015) · cites this paper as [37]
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“The circadian system and its prime marker, melatonin, are considered to have antitumor effects through multiple pathways, including antioxidant activity, anti-inflammatory effects, and immune enhancement.33-37”
From Total and Cause-Specific Mortality of U.S. Nurses Working Rotating Night Shifts (2015) · cites this paper as [37]
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Self-citationPinealectomy interferes with the circadian clock genes expression in white adipose tissue
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Chemotherapeutic Effect of SR9009, a REV-ERB Agonist, on the Human Glioblastoma T98G Cells
Wagner, P. M., Monjes, N. M., & Guido, M. E. (2019) · ASN NEURO · doi:10.1177/1759091419892713 · Cited by 63
Role of Intestinal Circadian Genes in Alcohol-Induced Gut Leakiness
Swanson, G. R., Forsyth, C. B., Tang, Y., Shaikh, M. W., Zhang, L., Turek, F. W., & Keshavarzian, A. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01466.x · Cited by 63
“…and metabolic fields as to the intersections at the behavioral, tissue, and molecular levels of the circadian clock and metabolic systems, and has led to major mechanistic discoveries of these interactions (Green et al., 2008; Laposky et al., 2008b; Nakahata et al., 2008; Ramsey et al., 2009).”
InfluentialNon‐alcoholic fatty liver disease: the role of nuclear receptors and circadian rhythmicity
Mazzoccoli, G., Vinciguerra, M., Oben, J. A., Tarquini, R., & Cosmo, S. D. (2014) · Liver International · doi:10.1111/liv.12534 · Cited by 66
Circadian Rhythms and Obesity in Mammals
Froy, O. (2012) · ISRN Obesity · doi:10.5402/2012/437198 · Cited by 66
“The transcription factor CLOCK dimerizes with BMAL1 to activate transcription upon binding to E-box (5′-CACGTG-3′) promoter elements [11].”
Diurnal Rhythms Spatially and Temporally Organize Autophagy
Ryzhikov, M., Ehlers, A., Steinberg, D. F., Xie, W.-F., Oberlander, E., Brown, S., Erdmann-Gilmore, P., Townsend, R., Lane, W. S., Dolinay, T., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.072 · Cited by 67
“Circadian rhythms are daily variations in biological function that depend upon a group of conserved transcription factors called clock genes (Green et al., 2008).”
Circadian clock disruption improves the efficacy of chemotherapy through p73-mediated apoptosis
Lee, J. H., & Sancar, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106284108 · Cited by 65
“13 Thus, the circadian clock system regulates physiology, behavior, and metabolism through periodic activation and repression of the set of clock-controlled genes (CCGs) that are involved in a remarkably wide variety of cellular pathways (Green et al., 2008; Sahar and Sassone-Corsi, 2009; Schibler and Sassone-Corsi, 2…”
Glycemic control is impaired in the evening in prediabetes through multiple diurnal rhythms
Sonnier, T. J., Rood, J., Gimble, J. M., & Peterson, C. M. (2014) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2014.04.001 · Cited by 62
Liu, C., Wu, Y., Li, H., Qi, Q., Langenberg, C., Loos, R. J. F., & Xu, L. (2010) · BMC Medical Genetics · doi:10.1186/1471-2350-11-59 · Cited by 62
“Background There is growing evidence suggesting that circadian rhythms are closely linked to metabolic regulation, and dysregulation of circadian rhythms may increase diabetes risk [1].”
Computational and experimental insights into the circadian effects of SIRT1
Foteinou, P. T., Venkataraman, A., Francey, L. J., Anafi, R. C., Hogenesch, J. B., & Doyle, F. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803410115 · Cited by 66
Diurnal Variation in Urodynamics of Rat
Herrera, G. M., & Meredith, A. L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012298 · Cited by 61
“Physiological function is phaselocked to the day-night cycle to ensure optimal performance of a system at the appropriate time of day, for example, an upregulation of metabolic pathways during the period of expected food consumption [1,2].”
Rhythm of digestion: keeping time in the gastrointestinal tract
Bron, R., & Furness, J. B. (2009) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2009.05254.x · Cited by 60
“Evidence that these alternating episodes are under the control of circadian feedback loops involving clock genes has snowballed in recent years (for a review, see Green et al.8).”
Tong, X., Buelow, K. L., Guha, A., Rausch, R., & Yin, L. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.340786 · Cited by 66
Kinnaird, J. H., Weir, W., Durrani, Z., Pillai, S. S., Baird, M., & Shiels, B. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066833 · Cited by 62
“CLOCK (Circadian Locomotor Output Kaput), is a transcription factor involved in regulation of circadian rhythm and is now understood to be important in control of metabolic homeostasis [67].”
Dietary proanthocyanidins modulate BMAL1 acetylation, Nampt expression and NAD levels in rat liver
Ribas‐Latre, A., Baselga‐Escudero, L., Casanova, E., Arola‐Arnal, A., Salvadó, M. J., Bladé, C., & Arola, L. (2015) · Scientific Reports · doi:10.1038/srep10954 · Cited by 63
“…heterodimer enhances the transcription of metabolic genes, such as nicotinamide phosphoribosyltransferase ( Nampt ), which are implicated in many aspects of metabolism and biochemical processes, therefore supporting the tight relation between the clock system and metabolism or physiology 8,9 .”
Circadian regulation of adipose function
Shostak, A., Husse, J., & Oster, H. (2013) · Adipocyte · doi:10.4161/adip.26007 · Cited by 63
“Nonetheless many of these cyclic genes represent ccgs, which harbor in their promoters circadian transcription factor binding elements (E-boxes, RREs—see above) and are, thus, direct targets of the circadian clock.(31) Identification of genuine (i.”
A Small Molecule Modulates Circadian Rhythms through Phosphorylation of the Period Protein
Lee, J. W., Hirota, T., Peters, E. C., Garcia, M. E., Gonzalez, R., Cho, C. Y., Wu, X., Schultz, P. G., & Kay, S. A. (2011) · Angewandte Chemie International Edition · doi:10.1002/anie.201103915 · Cited by 62
Mi, Y., Qi, G., Gao, Y.-Q., Li, R., Wang, Y., Li, X., Huang, S., & Liu, X. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700440 · Cited by 60
Liu, Y., Guo, Y., Zhang, L., Pei, Y., Yu, N., Yu, P., Papasian, C. J., & Deng, H. (2010) · Obesity · doi:10.1038/oby.2010.83 · Cited by 59
“Emerging evidence shows that circadian regulation is intimately linked to metabolic homeostasis and that dysregulation of circadian rhythms can contribute to disease such as obesity (26).”
Ribas‐Latre, A., Bas-Prior, J. M. D., Baselga‐Escudero, L., Casanova, E., Arola‐Arnal, A., Salvadó, M. J., Arola, L., & Bladé, C. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400571 · Cited by 63
Puszynska, A. M., & O’Shea, E. K. (2017) · eLife · doi:10.7554/elife.23210 · Cited by 59
“This tight coupling between circadian machinery and metabolism is coming to light as a universal feature across kingdoms of life (Green et al., 2008; Dodd et al., 2015).”
The Relationship between Circadian Rhythm and Cancer Disease
Munteanu, C., Turti, S., Achim, L., Muresan, R., Souca, M., Prifti, E., Mârza, S. M., & Papuc, I. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115846 · Cited by 65
“Clock-regulated genes express themselves rhythmically, coordinating cellular functions with the daily cycle of light and dark to maximize physiological reactions to external stimuli [51].”
Skeletal aging and the adipocyte program
Lecka‐Czernik, B., Rosen, C. J., & Kawai, M. (2010) · Cell Cycle · doi:10.4161/cc.9.18.13046 · Cited by 57
Metabolic Compensation and Circadian Resilience in Prokaryotic Cyanobacteria
Johnson, C. H., & Egli, M. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060713-035632 · Cited by 58
The circadian rhythm in intervertebral disc degeneration: an autophagy connection
Zhang, T., Li, Z., Dong, J., & Jiang, L. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0372-6 · Cited by 61
Wang, Z., Akamatsu, T., Wang, K., & Wang, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097907 · Cited by 57
“Mounting evidence from studies of circadian rhythms has shown that a wide variety of taxa tend to switch from nocturnal to diurnal activity patterns to adapt to metabolic demands (for a review, see [25]) and/or their physical and social environment (see [26] for a review).”
Cycling Transcriptional Networks Optimize Energy Utilization on a Genome Scale
Wang, G.-Z., Hickey, S. L., Shi, L., Huang, H.-C., Nakashe, P., Koike, N., Tu, B. P., Takahashi, J. S., & Konopka, G. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.10.043 · Cited by 59
“It is possible that cost is not as relevant for directing cyclical expression of genes that are core components of the regulatory network of cycling behavior and biosynthetic pathways, such as Bmal1, Clock, Cry, Dbp, Per, and Nampt (Green et al., 2008).”
InfluentialSelf-citationKim, H., Zheng, Z., Walker, P. D., Kapatos, G., & Zhang, K. (2017) · Molecular and Cellular Biology · doi:10.1128/mcb.00048-17 · Cited by 59
“The liver is a major metabolic organ that plays primary roles in maintaining energy homeostasis across the circadian cycle (1, 2).”
Wilson, K. A., Chamoli, M., Hilsabeck, T. A. U., Pandey, M., Bansal, S., Chawla, G., & Kapahi, P. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.08.018 · Cited by 57
“Circadian clock regulators—The circadian clock is an internal time-keeping system that helps maintain a 24-h rhythmic oscillation in behavior, physiology, and metabolism and is present across animals of different taxa (Green et al., 2008).”
Matsumoto, E., Ishihara, A., Tamai, S., Nemoto, A., Iwase, K., Hiwasa, T., Shibata, S., & Takiguchi, M. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.089391 · Cited by 53
General Characteristics and Risk Factors of Cardiovascular Disease among Interstate Bus Drivers
Hirata, R. P., Sampaio, L. M. M., Filho, F. S. L., Braghiroli, A., Balbi, B., Romano, S., Insalaco, G., & de Oliveira, L. V. F. (2012) · The Scientific World JOURNAL · doi:10.1100/2012/216702 · Cited by 55
“The work shift is also a risk factor of chronic disease, including cardiovascular disease and metabolic disorders, due to the altered circadian rhythm, changes in lifestyle, tension, and stress at work [54–56].”
Time-restricted feeding protects the blood pressure circadian rhythm in diabetic mice
Hou, T., Su, W., Duncan, M. J., Vsevolozhskaya, O. A., Guo, Z., & Gong, M. C. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2015873118 · Cited by 60
“BP circadian rhythms are controlled at the molecular level by interacting transcriptional–translational feedback loops composed of a set of clock genes, which are expressed in cells throughout the body (31, 32).”
Metadata
- Authors
- Green, C. B., Takahashi, J. S., & Bass, J.
- Affiliations
- University of Virginia (US)
- Northwestern University (US)
- Corresponding author
- Takahashi, Joseph S.
- Bass, Joseph
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 134
- Issue
- 5
- Pages
- 728-742
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3760165
- OpenAlex
- W2063946784
- Cited by
- 902
- References
- 145
- Citations by year
- 2026: 22 · 2025: 29 · 2024: 29 · 2023: 33 · 2022: 51 · 2021: 49 · 2020: 36 · 2019: 44 · 2018: 35 · 2017: 52 · 2016: 56 · 2015: 51 · 2014: 65 · 2013: 61 · 2012: 74
- FWCI
- 7.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- Amylin Pharmaceuticals
- National Institutes of Health (5p50mh074924-05)
- National Institute on Aging (P01AG011412)
- National Heart, Lung, and Blood Institute (R01HL075029)
- National Institute of Mental Health (P50 MH-074924, R01MH078024)
- National Institute of General Medical Sciences (R01GM076626)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Health Sciences › Medicine › Physiology (medical) › Dietary Effects on Health
- Keywords
- circadian rhythm, metabolism, circadian regulation, metabolic homeostasis, circadian gene expression, central nervous system, peripheral tissues, cardiovascular disease, obesity, diabetes mellitus
- MeSH terms
- Animals, Biological Clocks, Circadian Rhythm, Feeding Behavior, Humans, Metabolic Networks and Pathways
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