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First published October 2004

It’s All in the Timing: Many Clocks, Many Outputs

Abstract

It is thought that circadian regulation of physiology and behavior imparts survival advantages to organisms that use clocks. In mammals, a master clock resident in the SCN synchronizes other central and peripheral oscillators to evoke this regulation. This master oscillator consists of interlocking transcriptional-translational feedback loops, and it regulates both core clock genes necessary for oscillator maintenance as well as specific output genes that directly or indirectly mediate physiology under circadian control. It is now clear that both neuroanatomic and molecular outputs of the clock are necessary for proper circadian clock function. Recent technology has improved our understanding of these processes, elucidating the anatomic outputs of the SCN, as well as the molecular outputs of both central and peripheral oscillators that mediate observed physiological changes.

References

Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, Sakaki Y, Menaker M, and Block GD (2002) Circadian rhythms in isolated brain regions. J Neurosci 22:350-356.
Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH, and Kyriacou CP (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12:540-550.
Baggs JE and Green CB (2003) Nocturnin, a deadenylase in Xenopus laevis retina: A mechanism for posttranscriptional control of circadian-related mRNA. Curr Biol 13:189-198.
Berendse HW and Groenewegen HJ (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299:187-228.
Boer GJ, van Esseveldt KE, van der Geest BA, Duindam H, and Rietveld WJ (1999) Vasopressin-deficient suprachiasmatic nucleus grafts re-instate circadian rhythmicity in suprachiasmatic nucleus-lesioned arrhythmic rats. Neuroscience 89:375-385.
Buijs RM, Hermes MH, and Kalsbeek A (1998) The suprachiasmatic nucleus-paraventricular nucleus interactions: A bridge to the neuroendocrine and autonomic nervous system. Prog Brain Res 119:365-382.
Buijs RM, van Eden CG, Goncharuk VD, and Kalsbeek A (2003) The biological clock tunes the organs of the body: Timing by hormones and the autonomic nervous system. J Endocrinol 177:17-26.
Buijs RM, Wortel J, Van Heerikhuize JJ, Feenstra MG, Ter Horst GJ, Romijn HJ, and Kalsbeek A (1999) Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci 11:1535-1544.
Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, and Kay SA (2002) Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 22:9305-9319.
Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, and Zhou QY (2002) Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417:405-410.
Colwell CS and Michel S (2003) Sleep and circadian rhythms: Do sleep centers talk back to the clock? Nat Neurosci 6:1005-1006.
Coon SL, Roseboom PH, Baler R, Weller JL, Namboodiri MA, Koonin EV, and Klein DC (1995) Pineal serotonin N-acetyltransferase: Expression cloning and molecular analysis. Science 270:1681-1683.
Davidson AJ, Yamazaki S, and Menaker M (2003) SCN: Ringmaster of the circadian circus or conductor of the circadian orchestra? Novartis Found Symp 253:110-121; discussion 121-125, 281-284.
de la Iglesia HO, Blaustein JD, and Bittman EL (1995) The suprachiasmatic area in the female hamster projects to neurons containing estrogen receptors and GnRH. Neuroreport 6:1715-1722.
Ditty JL, Williams SB, and Golden SS (2003) A cyanobacterial circadian timing mechanism. Annu Rev Genet 37:513-543.
Duffield GE (2003) DNA microarray analyses of circadian timing: The genomic basis of biological time. J Neuroendocrinol 15:991-1002.
Duffield GE, Best JD, Meurers BH, Bittner A, Loros JJ, and Dunlap JC (2002) Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr Biol 12:551-557.
Etchegaray JP, Lee C, Wade PA, and Reppert SM (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421:177-182.
Evans DA, van der Kleij AA, Sonnemans MA, Burbach JP, and van Leeuwen FW (1994) Frameshift mutations at two hotspots in vasopressin transcripts in post-mitotic neurons. Proc Natl Acad Sci U S A 91:6059-6063.
Fonjallaz P, Ossipow V, Wanner G, and Schibler U (1996) The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue-specific expression, but have different target promoter preferences. EMBO J 15:351-362.
Franken P, Lopez-Molina L, Marcacci L, Schibler U, and Tafti M (2000) The transcription factor DBP affects circadian sleep consolidation and rhythmic EEG activity. J Neurosci 20:617-625.
Grechez-Cassiau A, Panda S, Lacoche S, Teboul M, Azmi S, Laudet V, Hogenesch JB, Taneja R, and Delaunay F (2004) The transcriptional repressor STRA13 regulates a subset of peripheral circadian outputs. J Biol Chem 279:1141-1150.
Green CB and Besharse JC (1996) Identification of a novel vertebrate circadian clock-regulated gene encoding the protein nocturnin. Proc Natl Acad Sci U S A 93:14884-14888.
Grundschober C, Delaunay F, Puhlhofer A, Triqueneaux G, Laudet V, Bartfai T, and Nef P (2001) Circadian regulation of diverse gene products revealed by mRNA expression profiling of synchronized fibroblasts. J Biol Chem 276:46751-46758.
Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, and Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110-2113.
Hermes ML, Coderre EM, Buijs RM, and Renaud LP (1996) GABA and glutamate mediate rapid neurotransmission from suprachiasmatic nucleus to hypothalamic paraventricular nucleus in rat. J Physiol 496:749-757.
Herzog ED, Takahashi JS, and Block GD (1998) Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat Neurosci 1:708-713.
Huang LE, Arany Z, Livingston DM, and Bunn HF (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 271:32253-32259.
Jin X, Shearman LP, Weaver DR, Zylka MJ, de Vries GJ, and Reppert SM (1999) A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell 96:57-68.
Kapfhamer D, Valladares O, Sun Y, Nolan PM, Rux JJ, Arnold SE, Veasey SC, and Bucan M (2002) Mutations in Rab3a alter circadian period and homeostatic response to sleep loss in the mouse. Nat Genet 32:290-295.
Klein DC and Weller JL (1970) Indole metabolism in the pineal gland: A circadian rhythm in N-acetyltransferase. Science 169:1093-1095.
Kornmann B, Preitner N, Rifat D, Fleury-Olela F, and Schibler U (2001) Analysis of circadian liver gene expression by ADDER, a highly sensitive method for the display of differentially expressed mRNAs. Nucleic Acids Res 29:E51.
Kramer A, Yang FC, Snodgrass P, Li X, Scammell TE, Davis FC, and Weitz CJ (2001) Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 294:2511-2515.
Kruisbrink J, Mirmiran M, Van der Woude TP, and Boer GJ (1987) Effects of enhanced cerebrospinal fluid levels of vasopressin, vasopressin antagonist or vasoactive intestinal polypeptide on circadian sleep-wake rhythm in the rat. Brain Res 419:76-86.
Lavery DJ, Lopez-Molina L, Margueron R, Fleury-Olela F, Conquet F, Schibler U, and Bonfils C (1999) Circadian expression of the steroid 15 alpha-hydroxylase (Cyp2a4) and coumarin 7-hydroxylase (Cyp2a5) genes in mouse liver is regulated by the PAR leucine zipper transcription factor DBP. Mol Cell Biol 19:6488-6499.
Lavery DJ and Schibler U (1993) Circadian transcription of the cholesterol 7 alpha hydroxylase gene may involve the liver-enriched bZIP protein DBP. Genes Dev 7:1871-1884.
Lee YH, Alberta JA, Gonzalez FJ, and Waxman DJ (1994) Multiple, functional DBP sites on the promoter of the cholesterol 7 alpha-hydroxylase P450 gene, CYP7: Proposed role in diurnal regulation of liver gene expression. J Biol Chem 269:14681-14689.
Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV, Golden SS, Ishiura M, and Kondo T (1995) Circadian orchestration of gene expression in cyanobacteria. Genes Dev 9:1469-1478.
Lucas RJ, Stirland JA, Darrow JM, Menaker M, and Loudon AS (1999) Free running circadian rhythms of melatonin, luteinizing hormone, and cortisol in Syrian hamsters bearing the circadian tau mutation. Endocrinology 140:758-764.
Michael TP and McClung CR (2003) Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol 132:629-639.
Moore RY (1983) Organization and function of a central nervous system circadian oscillator: The suprachiasmatic hypothalamic nucleus. Fed Proc 42:2783-2789.
Moore RY (1993) Organization of the primate circadian system. J Biol Rhythms 8:S3-S9.
Moore RY (1996) Entrainment pathways and the functional organization of the circadian system. Prog Brain Res 111:103-119.
Moore RY and Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201-206.
Oishi K, Miyazaki K, Kadota K, Kikuno R, Nagase T, Atsumi G, Ohkura N, Azama T, Mesaki M, Yukimasa S, et al. (2003) Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J Biol Chem 278:41519-41527.
Ouyang Y, Andersson CR, Kondo T, Golden SS, and Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A 95:8660-8664.
Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, and Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307-320.
Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, and Schibler U (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251-260.
Ralph MR, Foster RG, Davis FC, and Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975-978.
Reppert SM and Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935-941.
Rutter J, Reick M, Wu LC, and McKnight SL (2001) Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293:510-514.
Schibler U and Sassone-Corsi P (2002) A web of circadian pacemakers. Cell 111:919-922.
Seite R and Pebusque MJ (1985) Chronobiological studies on the nucleolus. Chronobiol Int 2:69-91.
Sherman TG, McKelvy JF, and Watson SJ (1986) Vasopressin mRNA regulation in individual hypothalamic nuclei: A northern and in situ hybridization analysis. J Neurosci 6:1685-1694.
Silver R, LeSauter J, Tresco PA, and Lehman MN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382:810-813.
Silver R, Sookhoo AI, LeSauter J, Stevens P, Jansen HT, and Lehman MN (1999) Multiple regulatory elements result in regional specificity in circadian rhythms of neuro-peptide expression in mouse SCN. Neuroreport 10:3165-3174.
Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490-493.
Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, and Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78-83.
Straume M (2004) DNA microarray time series analysis: Automated statistical assessment of circadian rhythms in gene expression patterning. Methods Enzymol 383:149-166.
Tosini G and Menaker M (1996) Circadian rhythms in cultured mammalian retina. Science 272:419-421.
Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, et al. (2002) A transcription factor response element for gene expression during circadian night. Nature 418:534-539.
van den Pol AN and Tsujimoto KL (1985) Neurotransmitters of the hypothalamic suprachiasmatic nucleus: Immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15:1049-1086.
Van der Beek EM, Horvath TL, Wiegant VM, Van den Hurk R, and Buijs RM (1997) Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: Combined tracing and light and electron microscopic immunocytochemical studies. J Comp Neurol 384:569-579.
van Esseveldt KE, Lehman MN, and Boer GJ (2000) The suprachiasmatic nucleus and the circadian time-keeping system revisited. Brain Res Brain Res Rev 33:34-77.
Welsh DK, Logothetis DE, Meister M, and Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697-706.
Wuarin J, Falvey E, Lavery D, Talbot D, Schmidt E, Ossipow V, Fonjallaz P, and Schibler U (1992) The role of the transcriptional activator protein DBP in circadian liver gene expression. J Cell Sci Suppl 16:123-127.
Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, et al. (2004) PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 101:5339-5346.

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Article first published: October 2004
Issue published: October 2004

Keywords

  1. suprachiasmatic nucleus
  2. circadian clock
  3. transcription
  4. neuroanatomic
  5. circadian output

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PubMed: 15534318

Authors

Affiliations

Satchidananda Panda
Genomics Institute of Novartis Research Foundation
John B. Hogenesch
Genomics Institute of Novartis Research Foundation, Department of Neuropharmacology, Scripps Research Institute, [email protected]

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