Glucocorticoid hormones inhibit food‐induced phase‐shifting of peripheral circadian oscillators

The circadian timing system in mammals is composed of a master pacemaker in the suprachiasmatic nucleus (SCN) of the hypothalamus and slave clocks in most peripheral cell types. The phase of peripheral clocks can be completely uncoupled from the SCN pacemaker by restricted feeding. Thus, feeding time, while not affecting the phase of the SCN pacemaker, is a dominant Zeitgeber for peripheral circadian oscillators. Here we show that the phase resetting in peripheral clocks of nocturnal mice is slow when feeding time is changed from night to day and rapid when switched back from day to night. Unexpectedly, the inertia in daytime feeding‐induced phase resetting of circadian gene expression in liver and kidney is not an intrinsic property of peripheral oscillators, but is caused by glucocorticoid signaling. Thus, glucocorticoid hormones inhibit the uncoupling of peripheral and central circadian oscillators by altered feeding time.

[1]  U. Schibler,et al.  A Serum Shock Induces Circadian Gene Expression in Mammalian Tissue Culture Cells , 1998, Cell.

[2]  C. Kellendonk,et al.  Genetic dissection of glucocorticoid receptor function in mice. , 1998, Current opinion in genetics & development.

[3]  Y Sakaki,et al.  Resetting central and peripheral circadian oscillators in transgenic rats. , 2000, Science.

[4]  K. Yagita,et al.  Forskolin induces circadian gene expression of rPer1, rPer2 and dbp in mammalian rat‐1 fibroblasts , 2000, FEBS letters.

[5]  C. Kellendonk,et al.  Hepatocyte‐specific expression of Cre recombinase , 2000, Genesis.

[6]  Christopher R. Jones,et al.  An hPer2 Phosphorylation Site Mutation in Familial Advanced Sleep Phase Syndrome , 2001, Science.

[7]  U. Schibler,et al.  CLOCK, an essential pacemaker component, controls expression of the circadian transcription factor DBP. , 2000, Genes & development.

[8]  A. Sehgal,et al.  Regulation of CLOCK and MOP4 by Nuclear Hormone Receptors in the Vasculature A Humoral Mechanism to Reset a Peripheral Clock , 2001, Cell.

[9]  Mark J. Zylka,et al.  Two period Homologs: Circadian Expression and Photic Regulation in the Suprachiasmatic Nuclei , 1997, Neuron.

[10]  P. Cheifetz.  The daily rhythm of the secretion of corticotrophin and corticosterone in rats and mice. , 1971, Journal of Endocrinology.

[11]  John B. Hogenesch,et al.  Mop3 Is an Essential Component of the Master Circadian Pacemaker in Mammals , 2000, Cell.

[12]  Jared Rutter,et al.  Regulation of Clock and NPAS2 DNA Binding by the Redox State of NAD Cofactors , 2001, Science.

[13]  F. Fleury-Olela,et al.  Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. , 2000, Genes & development.

[14]  Minoru Tanaka,et al.  Positional Cloning of the Mouse Circadian Clock Gene , 1997, Cell.

[15]  Yoshiyuki Sakaki,et al.  Circadian oscillation of a mammalian homologue of the Drosophila period gene , 1997, Nature.

[16]  E. Nishida,et al.  Involvement of the MAP kinase cascade in resetting of the mammalian circadian clock. , 2000, Genes & development.

[17]  Lily Yan,et al.  Light-Induced Resetting of a Mammalian Circadian Clock Is Associated with Rapid Induction of the mPer1 Transcript , 1997, Cell.

[18]  F. Tamanini,et al.  Molecular Mechanisms of the Biological Clock in Cultured Fibroblasts , 2001, Science.

[19]  F. Ebling.  The role of glutamate in the photic regulation of the suprachiasmatic nucleus , 1996, Progress in Neurobiology.

[20]  G. Wanner,et al.  The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue‐specific expression, but have different target promoter preferences. , 1996, The EMBO journal.

[21]  Steven A. Brown,et al.  Resetting of circadian time in peripheral tissues by glucocorticoid signaling. , 2000, Science.

[22]  Y Sakaki,et al.  Entrainment of the circadian clock in the liver by feeding. , 2001, Science.

[23]  Y Sakaki,et al.  The human and mouse Period1 genes: five well-conserved E-boxes additively contribute to the enhancement of mPer1 transcription. , 2000, Genomics.

[24]  D. V. Leenen,et al.  Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms , 1999, Nature.

[25]  R. Moore,et al.  Glutamate shifts the phase of the circadian neuronal firing rhythm in the rat suprachiasmatic nucleus in vitro , 1994, Neuroscience Letters.

[26]  Gregor Eichele,et al.  A Differential Response of Two Putative Mammalian Circadian Regulators, mper1 and mper2, to Light , 1997, Cell.

[27]  Edouard De Castro,et al.  Olfaction in birds: differential embryonic expression of nine putative odorant receptor genes in the avian olfactory system , 1996, Mechanisms of Development.

[28]  J. Takahashi,et al.  Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. , 2000, Science.

[29]  Mark J. Zylka,et al.  A Molecular Mechanism Regulating Rhythmic Output from the Suprachiasmatic Circadian Clock , 1999, Cell.

[30]  S. Honma,et al.  Ethosecretogram: relation of behavior to plasma corticosterone in freely moving rats. , 1984, The American journal of physiology.

[31]  S Levine,et al.  Ontogeny of the type 2 glucocorticoid receptor in discrete rat brain regions: an immunocytochemical study. , 1988, Brain research.

[32]  S. Kuhlman,et al.  A screen for genes induced in the suprachiasmatic nucleus by light. , 1998, Science.

[33]  U. Schibler,et al.  Circadian regulation of gene expression in animals. , 2001, Current opinion in cell biology.

[34]  V. Viau,et al.  Starvation: early signals, sensors, and sequelae. , 1999, Endocrinology.

[35]  Ueli Schibler,et al.  Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts , 2000, Current Biology.

[36]  Steven M Reppert,et al.  mCRY1 and mCRY2 Are Essential Components of the Negative Limb of the Circadian Clock Feedback Loop , 1999, Cell.

[37]  U. Schibler,et al.  The ins and outs of circadian timekeeping. , 1999, Current opinion in genetics & development.

[38]  D. Virshup,et al.  Phosphorylation and destabilization of human period I clock protein by human casein kinase Iε , 2000, Neuroreport.

[39]  E. Cauter,et al.  Control of circadian and episodic variations of adrenal androgens secretion in man , 1987, Journal of endocrinological investigation.

[40]  S. Reppert,et al.  Molecular analysis of mammalian circadian rhythms. , 2001, Annual review of physiology.

[41]  U. Schibler,et al.  High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. , 1995, Development.

[42]  K Kume,et al.  Interacting molecular loops in the mammalian circadian clock. , 2000, Science.

[43]  G. Eichele,et al.  The mPer2 gene encodes a functional component of the mammalian circadian clock , 1999, Nature.

[44]  Gregor Eichele,et al.  RIGUI, a Putative Mammalian Ortholog of the Drosophila period Gene , 1997, Cell.

[45]  F. Stephan,et al.  Feeding-entrained circadian rhythms in hypophysectomized rats with suprachiasmatic nucleus lesions. , 1999, The American journal of physiology.

[46]  M. Gillette,et al.  Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. , 1994, Science.

[47]  Richard A. Flavell,et al.  All's well that ends dead , 1999 .