Rhythms of Mammalian Body Temperature Can Sustain Peripheral Circadian Clocks
Open accessAbstract
Background Low-amplitude temperature oscillations can entrain the phase of circadian rhythms in several unicellular and multicellular organisms, including Neurospora and Drosophila. Because mammalian body temperature is subject to circadian variations of 1 degrees C-4 degrees C, we wished to determine whether these temperature cycles could serve as a Zeitgeber for circadian gene expression in peripheral cell types.Results In RAT1 fibroblasts cultured in vitro, circadian gene expression could be established by a square wave temperature rhythm with a (Delta)T of 4 degrees C (12 hr 37 degrees C/12 hr 33 degrees C). To examine whether natural body temperature rhythms can also affect circadian gene expression, we first measured core body temperature cycles in the peritoneal cavities of mice by radiotelemetry. We then reproduced these rhythms with high precision in the liquid medium of cultured fibroblasts for several days by means of a homemade computer-driven incubator. While these "in vivo" temperature rhythms were incapable of establishing circadian gene expression de novo, they could maintain previously induced rhythms for multiple days; by contrast, the rhythms of control cells kept at constant temperature rapidly dampened. Moreover, circadian oscillations of environmental temperature could reentrain circadian clocks in the livers of mice, probably via the changes they imposed upon both body temperature and feeding behavior. Interestingly, these changes in ambient temperature did not affect the phase of the central circadian pacemaker in the suprachiasmatic nucleus (SCN) of the hypothalamus.Conclusions We postulate that both endogenous and environmental temperature cycles can participate in the synchronization of peripheral clocks in mammals.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Peripheral oscillators, including those in the brain such as the cerebral cortex, can be entrained by ambient temperature cycles.
“evidence has accumulated over the last decade to indicate that peripheral oscillators, including those in the brain (e.g., cerebral cortex), can be entrained by ambient temperature cycles [8, 9, 28].”
From Sleep, vigilance, and thermosensitivity (2012) · cites this paper as [8]
Cites
Molecular Bases for Circadian Clocks
Dunlap, J. C. (1999) · Cell · doi:10.1016/s0092-8674(00)80566-8 · Cited by 2,900 · see citing works
Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000) · Genes & Development · doi:10.1101/gad.183500 · Cited by 2,394 · see citing works
Self-citationPreitner, N., Damiola, F., Luis-Lopez-Molina, Zakany, J., Duboule, D., Albrecht, U., & Schibler, U. (2002) · Cell · doi:10.1016/s0092-8674(02)00825-5 · Cited by 2,198 · see citing works
Self-citationA Serum Shock Induces Circadian Gene Expression in Mammalian Tissue Culture Cells
Balsalobre, A., Damiola, F., & Schibler, U. (1998) · Cell · doi:10.1016/s0092-8674(00)81199-x · Cited by 2,001 · see citing works
Self-citationEntrainment of the circadian clock in the liver by feeding
Stokkan, K.-A., Yamazaki, S., Tei, H., Sakaki, Y., & Menaker, M. (2001) · Science · doi:10.1126/science.291.5503.490 · Cited by 1,800 · see citing works
Molecular analysis of mammalian circadian rhythms
Reppert, S. M., & Weaver, D. R. (2001) · Annual Review of Physiology · doi:10.1146/annurev.physiol.63.1.647 · Cited by 1,444 · see citing works
Silver, R., LeSauter, J., Tresco, P. A., & Lehman, M. N. (1996) · Nature · doi:10.1038/382810a0 · Cited by 792 · see citing works
Akhtar, R. A., Reddy, A. B., Maywood, E. S., Clayton, J. D., King, V. M., Smith, A. G., Gant, T. W., Hastings, M. H., & Kyriacou, C. P. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00759-5 · Cited by 777 · see citing works
The circadian rhythm of body temperature
Refinetti, R., & Menaker, M. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90188-8 · Cited by 735 · see citing works
Independent Photoreceptive Circadian Clocks Throughout Drosophila
Plautz, J. D., Kaneko, M. A. N., Hall, J. C., & Kay, S. A. (1997) · Science · doi:10.1126/science.278.5343.1632 · Cited by 640 · see citing works
Regulation of Daily Locomotor Activity and Sleep by Hypothalamic EGF Receptor Signaling
Kramer, A., Yang, F.-C., Snodgrass, P., Li, X., Scammell, T. E., Davis, F. C., & Weitz, C. J. (2001) · Science · doi:10.1126/science.1067716 · Cited by 536 · see citing works
Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts
Balsalobre, A., Marcacci, L., & Schibler, U. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00758-2 · Cited by 485 · see citing works
Self-citationLight acts directly on organs and cells in culture to set the vertebrate circadian clock
Whitmore, D., Foulkes, N. S., & Sassone‐Corsi, P. (2000) · Nature · doi:10.1038/35003589 · Cited by 481 · see citing works
Glucocorticoid hormones inhibit food‐induced phase‐shifting of peripheral circadian oscillators
Minh, N. L., Damiola, F., Tronche, F., Schütz, G., & Schibler, U. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.7128 · Cited by 467 · see citing works
Self-citationMolecular Mechanisms of the Biological Clock in Cultured Fibroblasts
Yagita, K., Tamanini, F., van der Horst, G. T. J., & Okamura, H. (2001) · Science · doi:10.1126/science.1059542 · Cited by 464 · see citing works
Regulation of CLOCK and MOP4 by Nuclear Hormone Receptors in the Vasculature
McNamara, P., Seo, S., Rudic, R. D., Sehgal, A., Chakravarti, D., & FitzGerald, G. A. (2001) · Cell · doi:10.1016/s0092-8674(01)00401-9 · Cited by 441 · see citing works
Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators
Whitmore, D., Foulkes, N. S., Strähle, U., & Sassone‐Corsi, P. (1998) · Nature Neuroscience · doi:10.1038/3703 · Cited by 357 · see citing works
Lopez‐Molina, L., Conquet, F., Dubois‐Dauphin, M., & Schibler, U. (1997) · The EMBO Journal · doi:10.1093/emboj/16.22.6762 · Cited by 300 · see citing works
Self-citationNucleus Suprachiasmaticus: The Biological Clock in the Hamster?
Stetson, M. H., & Watson‐Whitmyre, M. (1976) · Science · doi:10.1126/science.942799 · Cited by 278 · see citing works
Forskolin induces circadian gene expression of rPer1, rPer2 and dbp in mammalian rat‐1 fibroblasts
Yagita, K., & Okamura, H. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01724-x · Cited by 258 · see citing works
A new role for cryptochrome in a Drosophila circadian oscillator
Krishnan, B., Levine, J. D., Lynch, M. K. S., Dowse, H. B., Funes, P., Hall, J. C., Hardin, P. E., & Dryer, S. E. (2001) · Nature · doi:10.1038/35077094 · Cited by 239 · see citing works
Assignment of circadian function for the Neurospora clock gene frequency
Merrow, M. W., Brunner, M., & Roenneberg, T. (1999) · Nature · doi:10.1038/21190 · Cited by 227 · see citing works
How Temperature Changes Reset a Circadian Oscillator
Liu, Y., Merrow, M. W., Loros, J., & Dunlap, J. (1998) · Science · doi:10.1126/science.281.5378.825 · Cited by 226 · see citing works
Zimmerman, W. F., Pittendrigh, C. S., & Pavlidis, T. (1968) · Journal of Insect Physiology · doi:10.1016/0022-1910(68)90226-6 · Cited by 216 · see citing works
Roper, T. J. (1999) · Advances in the Study of Behavior · doi:10.1016/s0065-3454(08)60219-3 · Cited by 210 · see citing works
Rapid, small-scale RNA isolation from tissue culture cells.
Xie, W., & Rothblum, L. I. (1991) · PubMed · Cited by 210 · see citing works
Schmidt, E. E., & Schibler, U. (1995) · Development · doi:10.1242/dev.121.8.2373 · Cited by 157 · see citing works
Self-citationTemperature compensation and temperature entrainment of the chick pineal cell circadian clock
Barrett, R. K., & Takahashi, J. S. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05681.1995 · Cited by 111 · see citing works
Ruby, N. F., Burns, D. E., & Heller, H. C. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-19-08630.1999 · Cited by 108 · see citing works
LeSauter, J., & Silver, R. (1998) · Chronobiology International · doi:10.3109/07420529808998706 · Cited by 99 · see citing works
The regulation of circadian clocks by light in fruitflies and mice
Foster, F., & Helfrich‐Förster, C. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0962 · Cited by 98 · see citing works
Underwood, H. A., & Calaban, M. (1987) · Journal of Biological Rhythms · doi:10.1177/074873048700200302 · Cited by 91 · see citing works
Circadian Activity Rhythms in Squirrel Monkeys: Entrainment by Temperature Cycles 1
Aschoff, J., & Tokura, H. (1986) · Journal of Biological Rhythms · doi:10.1177/074873048600100201 · Cited by 87 · see citing works
Nef, S., Allaman, I., Fiumelli, H., de Castro, E., & Nef, P. (1996) · Mechanisms of Development · doi:10.1016/0925-4773(95)00491-2 · Cited by 80 · see citing works
Effects of Temperature Perturbations on Circadian Conidiation in Neurospora
Francis, C. D., & Sargent, M. (1979) · PLANT PHYSIOLOGY · doi:10.1104/pp.64.6.1000 · Cited by 78 · see citing works
Ruby, N. F., Dark, J. G., Burns, D. E., Heller, H. C., & Zucker, I. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00357.2002 · Cited by 75 · see citing works
Invited Review: A neural clockwork for encoding circadian time
Herzog, E. D., & Schwartz, W. J. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00836.2001 · Cited by 71 · see citing works
Relationship of Circadian Temperature and Activity Rhythms in Two Rodent Species
DeCoursey, P. J., PIUS, S., SANDLIN, C., et al. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00187-5 · Cited by 51 · see citing works
Liu, S., Chen, X.-M., Yoda, T., Nagashima, K., Fukuda, Y., & Kanosue, K. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03374-1 · Cited by 41 · see citing works
Pálková, M., Sigmund, L., & Erkert, H. G. (1999) · Chronobiology International · doi:10.3109/07420529909019082 · Cited by 34 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dibner, C., Schibler, U., & Albrecht, U. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135821 · Cited by 2,421 · see citing works
Self-citationCentral and Peripheral Circadian Clocks in Mammals
Mohawk, J. A., Green, C. B., & Takahashi, J. S. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153128 · Cited by 2,265 · see citing works
The genetics of mammalian circadian order and disorder: implications for physiology and disease
Takahashi, J. S., Hong, H.-K., Ko, C. H., & McDearmon, E. L. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2430 · Cited by 1,611 · see citing works
Molecular architecture of the mammalian circadian clock
Partch, C. L., Green, C. B., & Takahashi, J. S. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.07.002 · Cited by 1,449 · see citing works
Suprachiasmatic Nucleus: Cell Autonomy and Network Properties
Welsh, D. K., Takahashi, J. S., & Kay, S. A. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135919 · Cited by 1,216 · see citing works
Circadian rhythm disruption and mental health
Walker, W. H., Walton, J. C., DeVries, A. C., & Nelson, R. J. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0694-0 · Cited by 1,030 · see citing works
Temperature as a Universal Resetting Cue for Mammalian Circadian Oscillators
Buhr, E. D., Yoo, S.-H., & Takahashi, J. S. (2010) · Science · doi:10.1126/science.1195262 · Cited by 917 · see citing works
Molecular components of the mammalian circadian clock
Buhr, E. D., & Takahashi, J. S. (2013) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25950-0_1 · Cited by 738 · see citing works
Welsh, D. K., Yoo, S.-H., Liu, A. C., Takahashi, J. S., & Kay, S. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.11.057 · Cited by 726 · see citing works
Kornmann, B., Schaad, O., Bujard, H., Takahashi, J. S., & Schibler, U. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050034 · Cited by 658 · see citing works
Self-citationCircadian Rhythms: Mechanisms and Therapeutic Implications
Levi, F., & Schibler, U. (2007) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.47.120505.105208 · Cited by 645 · see citing works
Self-citationCrosstalk between components of circadian and metabolic cycles in mammals
Asher, G., & Schibler, U. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.006 · Cited by 601 · see citing works
Self-citationThe human circadian metabolome
Dallmann, R., Viola, A. U., Tarokh, L., Cajochen, C., & Brown, S. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114410109 · Cited by 566 · see citing works
Self-citationThe Functional and Clinical Significance of the 24-Hour Rhythm of Circulating Glucocorticoids
Oster, H., Challet, E., Ott, V., Arvat, E., de Kloet, E. R., Dijk, D.-J., Lightman, S., Vgontzas, A., & Van Cauter, E. (2017) · Endocrine Reviews · doi:10.1210/er.2015-1080 · Cited by 548 · see citing works
Glucocorticoids and the circadian clock
Dickmeis, T. (2009) · Journal of Endocrinology · doi:10.1677/joe-08-0415 · Cited by 494 · see citing works
Role of the circadian system in cardiovascular disease
Thosar, S. S., Butler, M. P., & Shea, S. A. (2018) · Journal of Clinical Investigation · doi:10.1172/jci80590 · Cited by 443 · see citing works
Circadian clocks: regulators of endocrine and metabolic rhythms
Hastings, M., O’Neill, J. S., & Maywood, E. S. (2007) · Journal of Endocrinology · doi:10.1677/joe-07-0378 · Cited by 426 · see citing works
Timing of light exposure affects mood and brain circuits
Bedrosian, T. A., & Nelson, R. J. (2017) · Translational Psychiatry · doi:10.1038/tp.2016.262 · Cited by 356 · see citing works
Exploring phylogeny to find the function of sleep
Anafi, R. C., Kayser, M. S., & Raizen, D. M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0098-9 · Cited by 259 · see citing works
Entrainment of the Human Circadian Clock
Roenneberg, T., & Merrow, M. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.043 · Cited by 272 · see citing works
Molecular insights into human daily behavior
Brown, S. A., Kunz, D., Dumas, A., Westermark, P. O., Vanselow, K., Tilmann-Wahnschaffe, A., Herzel, H., & Kramer, A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707772105 · Cited by 270 · see citing works
Self-citationClocks, metabolism, and the epigenome
Feng, D., & Lazar, M. A. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.06.026 · Cited by 271 · see citing works
“The central clock can entrain the peripheral clocks through neuronal and hormonal signals, as well as body temperature, aligning all clocks with the external light/dark cycle (Balsalobre et al., 2000; Brown et al., 2002; reviewed in Dibner et al., 2010).”
Circadian clocks: setting time by food
Mendoza, J. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01510.x · Cited by 257 · see citing works
Circadian timing of metabolism in animal models and humans
Dibner, C., & Schibler, U. (2015) · Journal of Internal Medicine · doi:10.1111/joim.12347 · Cited by 237 · see citing works
Self-citationDNA microarray analyses of circadian timing: the genomic basis of biological time
Duffield, G. E. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01082.x · Cited by 234 · see citing works
Circadian Rhythms, the Molecular Clock, and Skeletal Muscle
Harfmann, B. D., Schroder, E. A., & Esser, K. A. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730414561638 · Cited by 211 · see citing works
Tahara, Y., & Shibata, S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.049 · Cited by 198 · see citing works
The thermophysiological cascade leading to sleep initiation in relation to phase of entrainment
Kräuchi, K. (2007) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2007.07.001 · Cited by 191 · see citing works
Circadian rhythms – from genes to physiology and disease
Bollinger, T., & Schibler, U. (2014) · Swiss Medical Weekly · doi:10.4414/smw.2014.13984 · Cited by 152 · see citing works
Self-citationCircadian rhythmicity of body temperature and metabolism
Refinetti, R. (2020) · Temperature · doi:10.1080/23328940.2020.1743605 · Cited by 155 · see citing works
Mammalian circadian systems: Organization and modern life challenges
Finger, A., & Kramer, A. (2021) · Acta Physiologica · doi:10.1111/apha.13548 · Cited by 117 · see citing works
Sleep, vigilance, and thermosensitivity
Romeijn, N., Raymann, R. J. E. M., Møst, E., Te Lindert, B., Van Der Meijden, W. P., Fronczek, R., Gomez-Herrero, G., & Van Someren, E. J. W. (2012) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1042-2 · Cited by 105 · see citing works
Chrono-biology, Chrono-pharmacology and Chrono-nutrition
Tahara, Y., & Shibata, S. (2014) · Journal of Pharmacological Sciences · doi:10.1254/jphs.13r06cr · Cited by 94 · see citing works
Metabolic impacts of altering meal frequency and timing - Does when we eat matter
Hutchison, A. T., & Heilbronn, L. K. (2016) · Biochimie · doi:10.1016/j.biochi.2015.07.025 · Cited by 91 · see citing works
Circadian Entrainment to Temperature, But Not Light, in the Isolated Suprachiasmatic Nucleus
Herzog, E. D., & Huckfeldt, R. M. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00129.2003 · Cited by 82 · see citing works
Impact of Chronodisruption during Primate Pregnancy on the Maternal and Newborn Temperature Rhythms
Serón-Ferré, M., Forcelledo, M. L., Torres-Farfan, C., Valenzuela, F. J., Rojas, A., Vergara, M., Rojas-Garcia, P. P., Recabarren, M. P., & Valenzuela, G. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057710 · Cited by 55 · see citing works
Modulation of circadian clocks by nutrients and food factors
Oike, H. (2017) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2017.1281722 · Cited by 53 · see citing works
Correlated Fluctuations of Daytime Skin Temperature and Vigilance
Romeijn, N., & Van Someren, E. J. W. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730410391894 · Cited by 48 · see citing works
When should I eat: A circadian view on food intake and metabolic regulation
Chamorro, R., Jouffe, C., Oster, H., Uhlenhaut, N. H., & Meyhöfer, S. M. (2023) · Acta Physiologica · doi:10.1111/apha.13936 · Cited by 40 · see citing works
The real-world association between digital markers of circadian disruption and mental health risks
Lee, M. P., Kim, D. W., Fang, Y., Kim, R., Bohnert, A. S. B., Sen, S., & Forger, D. B. (2024) · npj Digital Medicine · doi:10.1038/s41746-024-01348-6 · Cited by 29 · see citing works
Warming Up Your Tick-Tock: Temperature-Dependent Regulation of Circadian Clocks
Ki, Y., Ri, H., Lee, H., Yoo, E., Choe, J., & Lim, C. (2015) · The Neuroscientist · doi:10.1177/1073858415577083 · Cited by 24 · see citing works
Impacts of “supermoon” events on the physiology of a wild bird
Portugal, S. J., White, C. R., Frappell, P. B., Green, J. A., & Butler, P. J. (2019) · Ecology and Evolution · doi:10.1002/ece3.5311 · Cited by 23 · see citing works
Temperatures to Communicate By
Edery, I. (2010) · Science · doi:10.1126/science.1197747 · Cited by 14 · see citing works
- Authors
- Brown, S. A., Zumbrunn, G., Fleury-Olela, F., Preitner, N., & Schibler, U.
- Affiliations
- University of Geneva (CH)
- Corresponding author
- Schibler, Ueli
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2002-09
- Volume
- 12
- Issue
- 18
- Pages
- 1574-1583
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2171909239
- Cited by
- 589
- References
- 40
- Citations by year
- 2026: 17 · 2025: 22 · 2024: 23 · 2023: 40 · 2022: 24 · 2021: 45 · 2020: 31 · 2019: 26 · 2018: 21 · 2017: 31 · 2016: 30 · 2015: 28 · 2014: 26 · 2013: 39 · 2012: 24
- FWCI
- 5.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Physical Sciences › Computer Science › Computer Networks and Communications › Nonlinear Dynamics and Pattern Formation
- Keywords
- peripheral circadian clock, circadian gene expression, temperature entrainment, zeitgebers, feeding behavior, suprachiasmatic nucleus, core body temperature, fibroblasts, constant temperature
- MeSH terms
- Animals, Body Temperature, Cell Line, Circadian Rhythm, DNA-Binding Proteins, Fibroblasts, Liver, Mice, Inbred BALB C, Models, Biological, Suprachiasmatic Nucleus, Transcription Factors, Gene Expression, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review