Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 330 (6002): 379-385

Copyright © 2010 by the American Association for the Advancement of Science

Temperature as a Universal Resetting Cue for Mammalian Circadian Oscillators

Ethan D. Buhr,1,2 Seung-Hee Yoo,1,2,3 Joseph S. Takahashi1,2,3,4,*

Abstract: Environmental temperature cycles are a universal entraining cue for all circadian systems at the organismal level with the exception of homeothermic vertebrates. We report here that resistance to temperature entrainment is a property of the suprachiasmatic nucleus (SCN) network and is not a cell-autonomous property of mammalian clocks. This differential sensitivity to temperature allows the SCN to drive circadian rhythms in body temperature, which can then act as a universal cue for the entrainment of cell-autonomous oscillators throughout the body. Pharmacological experiments show that network interactions in the SCN are required for temperature resistance and that the heat shock pathway is integral to temperature resetting and temperature compensation in mammalian cells. These results suggest that the evolutionarily ancient temperature resetting response can be used in homeothermic animals to enhance internal circadian synchronization.

1 Department of Neurobiology and Physiology, Northwestern University, Evanston, IL 60208–3520, USA.
2 Center for Functional Genomics, Northwestern University, Evanston, IL 60208–3520, USA.
3 Department of Neuroscience, University of Texas Southwestern Medical Center, Dallas, TX 75390–9111, USA.
4 Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390–9111, USA

* To whom correspondence should be addressed. E-mail: joseph.takahashi{at}utsouthwestern.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
HSP90 Affects the Stability of BMAL1 and Circadian Gene Expression.
R. Schneider, R. M. Linka, and H. Reinke (2014)
J Biol Rhythms 29, 87-96
   Abstract »    Full Text »    PDF »
PNAS Plus: From the Cover: Mistimed sleep disrupts circadian regulation of the human transcriptome.
S. N. Archer, E. E. Laing, C. S. Moller-Levet, D. R. van der Veen, G. Bucca, A. S. Lazar, N. Santhi, A. Slak, R. Kabiljo, M. von Schantz, et al. (2014)
PNAS 111, E682-E691
   Abstract »    Full Text »    PDF »
Interactions between endocrine and circadian systems.
A. H. Tsang, J. L. Barclay, and H. Oster (2014)
J. Mol. Endocrinol. 52, R1-R16
   Abstract »    Full Text »    PDF »
Organ-specific development characterizes circadian clock gene Per2 expression in rats.
S.-y. Nishide, K. Hashimoto, T. Nishio, K.-i. Honma, and S. Honma (2014)
Am J Physiol Regulatory Integrative Comp Physiol 306, R67-R74
   Abstract »    Full Text »    PDF »
Body Temperature Predicts the Direction of Internal Desynchronization in Humans Isolated from Time Cues.
S. Daan, S. Honma, and K.-i. Honma (2013)
J Biol Rhythms 28, 403-411
   Abstract »    Full Text »    PDF »
A neuropeptide speeds circadian entrainment by reducing intercellular synchrony.
S. An, R. Harang, K. Meeker, D. Granados-Fuentes, C. A. Tsai, C. Mazuski, J. Kim, F. J. Doyle III, L. R. Petzold, and E. D. Herzog (2013)
PNAS 110, E4355-E4361
   Abstract »    Full Text »    PDF »
Leptin-sensitive neurons in the arcuate nucleus integrate activity and temperature circadian rhythms and anticipatory responses to food restriction.
M. F. Wiater, A.-J. Li, T. T. Dinh, H. T. Jansen, and S. Ritter (2013)
Am J Physiol Regulatory Integrative Comp Physiol 305, R949-R960
   Abstract »    Full Text »    PDF »
The Pyrexia transient receptor potential channel mediates circadian clock synchronization to low temperature cycles in Drosophila melanogaster.
W. Wolfgang, A. Simoni, C. Gentile, and R. Stanewsky (2013)
Proc R Soc B 280, 20130959
   Abstract »    Full Text »    PDF »
Energy intake and the circadian rhythm of core body temperature in sheep.
S. K. Maloney, L. C. R. Meyer, D. Blache, and A. Fuller (2013)
PHY2 1, e00118
   Abstract »    Full Text »    PDF »
Period Gene Expression in the Brain of a Dual-Phasing Rodent, the Octodon degus.
B. B. Otalora, M. H. Hagenauer, M. A. Rol, J. A. Madrid, and T. M. Lee (2013)
J Biol Rhythms 28, 249-261
   Abstract »    Full Text »    PDF »
Chronic phase advance alters circadian physiological rhythms and peripheral molecular clocks.
G. Wolff, M. J. Duncan, and K. A. Esser (2013)
J Appl Physiol 115, 373-382
   Abstract »    Full Text »    PDF »
Socially synchronized circadian oscillators.
G. Bloch, E. D. Herzog, J. D. Levine, and W. J. Schwartz (2013)
Proc R Soc B 280, 20130035
   Abstract »    Full Text »    PDF »
Real-time recording of circadian liver gene expression in freely moving mice reveals the phase-setting behavior of hepatocyte clocks.
C. Saini, A. Liani, T. Curie, P. Gos, F. Kreppel, Y. Emmenegger, L. Bonacina, J.-P. Wolf, Y.-A. Poget, P. Franken, et al. (2013)
Genes & Dev. 27, 1526-1536
   Abstract »    Full Text »    PDF »
Fibroblast PER2 Circadian Rhythmicity Depends on Cell Density.
T. Noguchi, L. L. Wang, and D. K. Welsh (2013)
J Biol Rhythms 28, 183-192
   Abstract »    Full Text »    PDF »
Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius).
K. E. Allali, M. R. Achaaban, B. Bothorel, M. Piro, H. Bouaouda, M. E. Allouchi, M. Ouassat, A. Malan, and P. Pevet (2013)
Am J Physiol Regulatory Integrative Comp Physiol 304, R1044-R1052
   Abstract »    Full Text »    PDF »
Drosophila TRPA1 Functions in Temperature Control of Circadian Rhythm in Pacemaker Neurons.
Y. Lee and C. Montell (2013)
J. Neurosci. 33, 6716-6725
   Abstract »    Full Text »    PDF »
Wavelet Meets Actogram.
T. L. Leise, P. Indic, M. J. Paul, and W. J. Schwartz (2013)
J Biol Rhythms 28, 62-68
   Abstract »    Full Text »    PDF »
Temperature Integration at the AC Thermosensory Neurons in Drosophila.
X. Tang, M. D. Platt, C. M. Lagnese, J. R. Leslie, and F. N. Hamada (2013)
J. Neurosci. 33, 894-901
   Abstract »    Full Text »    PDF »
Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus.
R. Enoki, S. Kuroda, D. Ono, M. T. Hasan, T. Ueda, S. Honma, and K.-i. Honma (2012)
PNAS 109, 21498-21503
   Abstract »    Full Text »    PDF »
Aging Differentially Affects the Re-entrainment Response of Central and Peripheral Circadian Oscillators.
M. T. Sellix, J. A. Evans, T. L. Leise, O. Castanon-Cervantes, D. D. Hill, P. DeLisser, G. D. Block, M. Menaker, and A. J. Davidson (2012)
J. Neurosci. 32, 16193-16202
   Abstract »    Full Text »    PDF »
Cold-Inducible RNA-Binding Protein Modulates Circadian Gene Expression Posttranscriptionally.
J. Morf, G. Rey, K. Schneider, M. Stratmann, J. Fujita, F. Naef, and U. Schibler (2012)
Science 338, 379-383
   Abstract »    Full Text »    PDF »
Cellular Circadian Clocks in Mood Disorders.
M. J. McCarthy and D. K. Welsh (2012)
J Biol Rhythms 27, 339-352
   Abstract »    Full Text »    PDF »
Crystal Structure of the Heterodimeric CLOCK:BMAL1 Transcriptional Activator Complex.
N. Huang, Y. Chelliah, Y. Shan, C. A. Taylor, S.-H. Yoo, C. Partch, C. B. Green, H. Zhang, and J. S. Takahashi (2012)
Science 337, 189-194
   Abstract »    Full Text »    PDF »
Period Coding of Bmal1 Oscillators in the Suprachiasmatic Nucleus.
J. Myung, S. Hong, F. Hatanaka, Y. Nakajima, E. De Schutter, and T. Takumi (2012)
J. Neurosci. 32, 8900-8918
   Abstract »    Full Text »    PDF »
Period of Irreversible Therapeutic Intervention during Sepsis Correlates with Phase of Innate Immune Dysfunction.
D. M. Cauvi, D. Song, D. E. Vazquez, D. Hawisher, J. A. Bermudez, M. R. Williams, S. Bickler, R. Coimbra, and A. De Maio (2012)
J. Biol. Chem. 287, 19804-19815
   Abstract »    Full Text »    PDF »
Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators.
C. Saini, J. Morf, M. Stratmann, P. Gos, and U. Schibler (2012)
Genes & Dev. 26, 567-580
   Abstract »    Full Text »    PDF »
LACTATION BIOLOGY SYMPOSIUM: Circadian clocks as mediators of the homeorhetic response to lactation.
T. M. Casey and K. Plaut (2012)
J Anim Sci 90, 744-754
   Abstract »    Full Text »    PDF »
Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening.
Z. Chen, S.-H. Yoo, Y.-S. Park, K.-H. Kim, S. Wei, E. Buhr, Z.-Y. Ye, H.-L. Pan, and J. S. Takahashi (2012)
PNAS 109, 101-106
   Abstract »    Full Text »    PDF »
HSP90 functions in the circadian clock through stabilization of the client F-box protein ZEITLUPE.
T.-s. Kim, W. Y. Kim, S. Fujiwara, J. Kim, J.-Y. Cha, J. H. Park, S. Y. Lee, and D. E. Somers (2011)
PNAS 108, 16843-16848
   Abstract »    Full Text »    PDF »
Rethinking Temperature Sensitivity of the Suprachiasmatic Nucleus.
N. F. Ruby (2011)
J Biol Rhythms 26, 368-370
   Abstract »    PDF »
Phase-Resetting Sensitivity of the Suprachiasmatic Nucleus and Oscillator Amplitude: Reply to Letter by Ruby.
E. D. Buhr, S.-H. Yoo, and J. S. Takahashi (2011)
J Biol Rhythms 26, 371-373
   Abstract »    PDF »
The Stress of Protein Misfolding: From Single Cells to Multicellular Organisms.
T. Gidalevitz, V. Prahlad, and R. I. Morimoto (2011)
Cold Spring Harb Perspect Biol 3, a009704
   Abstract »    Full Text »    PDF »
Light-dependent and circadian clock-regulated activation of sterol regulatory element-binding protein, X-box-binding protein 1, and heat shock factor pathways.
M. Hatori, T. Hirota, M. Iitsuka, N. Kurabayashi, S. Haraguchi, K. Kokame, R. Sato, A. Nakai, T. Miyata, K. Tsutsui, et al. (2011)
PNAS 108, 4864-4869
   Abstract »    Full Text »    PDF »
The Mammalian Circadian Timing System: Synchronization of Peripheral Clocks.
C. Saini, D. M. Suter, A. Liani, P. Gos, and U. Schibler (2011)
Cold Spring Harb Symp Quant Biol 76, 39-47
   Abstract »    Full Text »    PDF »
Circadian Integration of Metabolism and Energetics.
J. Bass and J. S. Takahashi (2010)
Science 330, 1349-1354
   Abstract »    Full Text »    PDF »
Temperatures to Communicate By.
I. Edery (2010)
Science 330, 329-330
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882