Temperature As a Universal Resetting Cue for Mammalian Circadian Oscillators

Overview

Journal Science

Specialty Science

Date 2010 Oct 16

PMID 20947768

Citations 428

Authors

Ethan D Buhr

Seung-Hee Yoo

Joseph S Takahashi

Affiliations

Soon will be listed here.

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.

Citing Articles

Periodic expression of Per1 gene is restored in chipmunk liver during interbout arousal in mammalian hibernation.

Nakamaru E, Seki K, Shirahata Y, Adachi M, Sakabe N, Matsuo T Sci Rep. 2025; 15(1):4403.

PMID: 39948130 PMC: 11825846. DOI: 10.1038/s41598-025-87299-8.

Parameterized resetting model captures dose-dependent entrainment of the mouse circadian clock.

Masuda K, Yoshimoto R, Li R, Sakurai T, Hirano A Nat Commun. 2025; 16(1):1421.

PMID: 39915501 PMC: 11802799. DOI: 10.1038/s41467-025-56792-z.

Delayed feeding disrupts diurnal oscillations in the gut microbiome of a neotropical bat in captivity.

Melville D, Meyer M, Kummerle C, Alvarado-Barrantes K, Wilhelm K, Sommer S FEMS Microbiol Ecol. 2025; 101(2).

PMID: 39844346 PMC: 11783575. DOI: 10.1093/femsec/fiaf012.

Resetting of the Human Circadian Melatonin Rhythm by Ambient Hypoxia.

Post T, De Gioannis R, Schmitz J, Wittkowski M, Schaper T, Wrobeln A J Pineal Res. 2025; 77(1):e70029.

PMID: 39821326 PMC: 11740168. DOI: 10.1111/jpi.70029.

Circadian clock communication during homeostasis and ageing.

Mortimer T, Smith J, Munoz-Canoves P, Benitah S Nat Rev Mol Cell Biol. 2025; .

PMID: 39753699 DOI: 10.1038/s41580-024-00802-3.

References

Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M . Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000; 288(5466):682-5. DOI: 10.1126/science.288.5466.682. View

Stratmann M, Schibler U . Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythms. 2006; 21(6):494-506. DOI: 10.1177/0748730406293889. View

Kornmann B, Schaad O, Bujard H, Takahashi J, Schibler U . System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol. 2007; 5(2):e34. PMC: 1783671. DOI: 10.1371/journal.pbio.0050034. View

Rutter J, Reick M, McKnight S . Metabolism and the control of circadian rhythms. Annu Rev Biochem. 2002; 71:307-31. DOI: 10.1146/annurev.biochem.71.090501.142857. View

Grad I, Picard D . The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol. 2007; 275(1-2):2-12. DOI: 10.1016/j.mce.2007.05.018. View

Lowrey P, Takahashi J . Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet. 2004; 5:407-41. PMC: 3770722. DOI: 10.1146/annurev.genom.5.061903.175925. View

Hoffmann K . . Oecologia. 2017; 3(2):184-206. DOI: 10.1007/BF00416981. View

Yoshida T, Murayama Y, Ito H, Kageyama H, Kondo T . Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle. Proc Natl Acad Sci U S A. 2009; 106(5):1648-53. PMC: 2635835. DOI: 10.1073/pnas.0806741106. View

Yoo S, Yamazaki S, Lowrey P, Shimomura K, Ko C, Buhr E . PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A. 2004; 101(15):5339-46. PMC: 397382. DOI: 10.1073/pnas.0308709101. View

10.

Prolo L, Takahashi J, Herzog E . Circadian rhythm generation and entrainment in astrocytes. J Neurosci. 2005; 25(2):404-8. PMC: 3812245. DOI: 10.1523/JNEUROSCI.4133-04.2005. View

11.

Majercak J, Sidote D, Hardin P, Edery I . How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron. 2000; 24(1):219-30. DOI: 10.1016/s0896-6273(00)80834-x. View

12.

Balsalobre A, Brown S, Marcacci L, Tronche F, Kellendonk C, Reichardt H . Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 2000; 289(5488):2344-7. DOI: 10.1126/science.289.5488.2344. View

13.

Honma S, Yasuda T, Yasui A, van der Horst G, Honma K . Circadian behavioral rhythms in Cry1/Cry2 double-deficient mice induced by methamphetamine. J Biol Rhythms. 2008; 23(1):91-4. DOI: 10.1177/0748730407311124. View

14.

Balsalobre A, Damiola F, Schibler U . A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell. 1998; 93(6):929-37. DOI: 10.1016/s0092-8674(00)81199-x. View

15.

Mosser D, Kotzbauer P, Sarge K, Morimoto R . In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proc Natl Acad Sci U S A. 1990; 87(10):3748-52. PMC: 53980. DOI: 10.1073/pnas.87.10.3748. View

16.

Honma S, Honma K, Shirakawa T, Hiroshige T . Rhythms in behaviors, body temperature and plasma corticosterone in SCN lesioned rats given methamphetamine. Physiol Behav. 1988; 44(2):247-55. DOI: 10.1016/0031-9384(88)90146-1. View

17.

Wadekar S, Li D, Sanchez E . Agonist-activated glucocorticoid receptor inhibits binding of heat shock factor 1 to the heat shock protein 70 promoter in vivo. Mol Endocrinol. 2003; 18(3):500-8. DOI: 10.1210/me.2003-0215. View

18.

Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M . Synchronization of cellular clocks in the suprachiasmatic nucleus. Science. 2003; 302(5649):1408-12. DOI: 10.1126/science.1089287. View

19.

Sehadova H, Glaser F, Gentile C, Simoni A, Giesecke A, Albert J . Temperature entrainment of Drosophila's circadian clock involves the gene nocte and signaling from peripheral sensory tissues to the brain. Neuron. 2009; 64(2):251-66. DOI: 10.1016/j.neuron.2009.08.026. View

20.

Kaushik R, Nawathean P, Busza A, Murad A, Emery P, Rosbash M . PER-TIM interactions with the photoreceptor cryptochrome mediate circadian temperature responses in Drosophila. PLoS Biol. 2007; 5(6):e146. PMC: 1877818. DOI: 10.1371/journal.pbio.0050146. View