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Peripheral Circadian Oscillators in Mammals

  • Steven A. BrownEmail author
  • Abdelhalim Azzi
Chapter
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 217)

Abstract

Although circadian rhythms in mammalian physiology and behavior are dependent upon a biological clock in the suprachiasmatic nuclei (SCN) of the hypothalamus, the molecular mechanism of this clock is in fact cell autonomous and conserved in nearly all cells of the body. Thus, the SCN serves in part as a “master clock,” synchronizing “slave” clocks in peripheral tissues, and in part directly orchestrates circadian physiology. In this chapter, we first consider the detailed mechanism of peripheral clocks as compared to clocks in the SCN and how mechanistic differences facilitate their functions. Next, we discuss the different mechanisms by which peripheral tissues can be entrained to the SCN and to the environment. Finally, we look directly at how peripheral oscillators control circadian physiology in cells and tissues.

Keywords

Feeding Fibroblast HPA axis Temperature 

Notes

Acknowledgments

S. A. B. is funded by the Swiss National Science Foundation, the Swiss Cancer League, and the Velux Foundation and receives additional support from the Zurich Neurozentrum (ZNZ) and Molecular Life Sciences Program (MLS). A. A. receives support from the Velux Foundation and the ZNZ. Thanks to Robert Dallmann for critical reading of the manuscript.

References

  1. Abraham U, Granada AE, Westermark PO, Heine M, Kramer A, Herzel H (2010) Coupling governs entrainment range of circadian clocks. Mol Syst Biol 6:438PubMedCrossRefGoogle Scholar
  2. Abrahamson EE, Moore RY (2006) Lesions of suprachiasmatic nucleus efferents selectively affect rest-activity rhythm. Mol Cell Endocrinol 252:46–56PubMedCrossRefGoogle Scholar
  3. Akashi M, Nishida E (2000) Involvement of the MAP kinase cascade in resetting of the mammalian circadian clock. Genes Dev 14:645–649PubMedGoogle Scholar
  4. Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH (2005) A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15:886–893PubMedCrossRefGoogle Scholar
  5. Alvarez JD, Chen D, Storer E, Sehgal A (2003) Non-cyclic and developmental stage-specific expression of circadian clock proteins during murine spermatogenesis. Biol Reprod 69:81–91PubMedCrossRefGoogle Scholar
  6. Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, Kreppel F, Mostoslavsky R, Alt FW, Schibler U (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134:317–328PubMedCrossRefGoogle Scholar
  7. Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, Schibler U (2010) Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142:943–953PubMedCrossRefGoogle Scholar
  8. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML (2001) A neural circuit for circadian regulation of arousal. Nat Neurosci 4:732–738PubMedCrossRefGoogle Scholar
  9. Aton SJ, Colwell CS, Harmar AJ, Waschek J, Herzog ED (2005) Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci 8: 476–483PubMedGoogle Scholar
  10. Balsalobre A, Damiola F, Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929–937PubMedCrossRefGoogle Scholar
  11. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U (2000a) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344–2347PubMedCrossRefGoogle Scholar
  12. Balsalobre A, Marcacci L, Schibler U (2000b) Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr Biol 10:1291–1294PubMedCrossRefGoogle Scholar
  13. Bartness TJ, Song CK, Demas GE (2001) SCN efferents to peripheral tissues: implications for biological rhythms. J Biol Rhythms 16:196–204PubMedGoogle Scholar
  14. Bray MS, Young ME (2009) The role of cell-specific circadian clocks in metabolism and disease. Obes Rev 10(Suppl 2):6–13PubMedCrossRefGoogle Scholar
  15. Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N, Schibler U (2002) Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 12:1574–1583PubMedCrossRefGoogle Scholar
  16. Brown SA, Fleury-Olela F, Nagoshi E, Hauser C, Juge C, Meier CA, Chicheportiche R, Dayer JM, Albrecht U, Schibler U (2005) The period length of fibroblast circadian gene expression varies widely among human individuals. PLoS Biol 3:e338PubMedCrossRefGoogle Scholar
  17. Buhr ED, Takahashi JS (2013) Molecular components of the mammalian circadian clock. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  18. Buhr ED, Yoo SH, Takahashi JS (2010) Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330:379–385PubMedCrossRefGoogle Scholar
  19. Castanon-Cervantes O, Wu M, Ehlen JC, Paul K, Gamble KL, Johnson RL, Besing RC, Menaker M, Gewirtz AT, Davidson AJ (2010) Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol 185:5796–5805PubMedCrossRefGoogle Scholar
  20. Charmandari E, Chrousos GP, Lambrou GI, Pavlaki A, Koide H, Ng SS, Kino T (2011) Peripheral CLOCK regulates target-tissue glucocorticoid receptor transcriptional activity in a circadian fashion in man. PLoS One 6:e25612PubMedCrossRefGoogle Scholar
  21. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY (2002) Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417:405–410PubMedCrossRefGoogle Scholar
  22. Cheng B, Anea CB, Yao L, Chen F, Patel V, Merloiu A, Pati P, Caldwell RW, Fulton DJ, Rudic RD (2011) Tissue-intrinsic dysfunction of circadian clock confers transplant arteriosclerosis. Proc Natl Acad Sci USA 108:17147–17152PubMedCrossRefGoogle Scholar
  23. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM (2012) Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485:123–127PubMedCrossRefGoogle Scholar
  24. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, Hu Z, Liu X, Waschek JA (2003) Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol 285:R939–R949PubMedGoogle Scholar
  25. Cuninkova L, Brown SA (2008) Peripheral circadian oscillators: interesting mechanisms and powerful tools. Ann NY Acad Sci 1129:358–370PubMedCrossRefGoogle Scholar
  26. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961PubMedCrossRefGoogle Scholar
  27. Davidson AJ, Yamazaki S, Arble DM, Menaker M, Block GD (2008) Resetting of central and peripheral circadian oscillators in aged rats. Neurobiol Aging 29:471–477PubMedCrossRefGoogle Scholar
  28. De Bacquer D, Van Risseghem M, Clays E, Kittel F, De Backer G, Braeckman L (2009) Rotating shift work and the metabolic syndrome: a prospective study. Int J Epidemiol 38:848–854PubMedCrossRefGoogle Scholar
  29. Debruyne JP, Noton E, Lambert CM, Maywood ES, Weaver DR, Reppert SM (2006) A clock shock: mouse CLOCK is not required for circadian oscillator function. Neuron 50:465–477PubMedCrossRefGoogle Scholar
  30. DeBruyne JP, Weaver DR, Reppert SM (2007a) CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci 10:543–545PubMedCrossRefGoogle Scholar
  31. DeBruyne JP, Weaver DR, Reppert SM (2007b) Peripheral circadian oscillators require CLOCK. Curr Biol 17:R538–R539PubMedCrossRefGoogle Scholar
  32. Doi M, Takahashi Y, Komatsu R, Yamazaki F, Yamada H, Haraguchi S, Emoto N, Okuno Y, Tsujimoto G, Kanematsu A, Ogawa O, Todo T, Tsutsui K, van der Horst GT, Okamura H (2010) Salt-sensitive hypertension in circadian clock-deficient Cry-null mice involves dysregulated adrenal Hsd3b6. Nat Med 16:67–74PubMedCrossRefGoogle Scholar
  33. Fortier EE, Rooney J, Dardente H, Hardy MP, Labrecque N, Cermakian N (2011) Circadian variation of the response of T cells to antigen. J Immunol 187:6291–6300PubMedCrossRefGoogle Scholar
  34. Gachon F, Firsov D (2010) The role of circadian timing system on drug metabolism and detoxification. Expert Opin Drug Metab Toxicol 7:147–158PubMedCrossRefGoogle Scholar
  35. Gachon F, Nagoshi E, Brown SA, Ripperger J, Schibler U (2004) The mammalian circadian timing system: from gene expression to physiology. Chromosoma 113:103–112PubMedCrossRefGoogle Scholar
  36. Gachon F, Olela FF, Schaad O, Descombes P, Schibler U (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4:25–36PubMedCrossRefGoogle Scholar
  37. Gachon F, Leuenberger N, Claudel T, Gos P, Jouffe C, Fleury Olela F, De Mollerat du Jeu X, Wahli W, Schibler U (2011) Proline- and acidic amino acid-rich basic leucine zipper proteins modulate peroxisome proliferator-activated receptor alpha (PPARalpha) activity. Proc Natl Acad Sci USA 108:4794–4799PubMedCrossRefGoogle Scholar
  38. Georg B, Hannibal J, Fahrenkrug J (2007) Lack of the PAC1 receptor alters the circadian expression of VIP mRNA in the suprachiasmatic nucleus of mice. Brain Res 1135:52–57PubMedCrossRefGoogle Scholar
  39. Gibbs JE, Blaikley J, Beesley S, Matthews L, Simpson KD, Boyce SH, Farrow SN, Else KJ, Singh D, Ray DW, Loudon AS (2012) The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA 109:582–587PubMedCrossRefGoogle Scholar
  40. Hardeland R, Cardinali DP, Srinivasan V, Spence DW, Brown GM, Pandi-Perumal SR (2011) Melatonin–a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 93:350–384PubMedCrossRefGoogle Scholar
  41. Hardin PE, Hall JC, Rosbash M (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343:536–540PubMedCrossRefGoogle Scholar
  42. Hatanaka F, Matsubara C, Myung J, Yoritaka T, Kamimura N, Tsutsumi S, Kanai A, Suzuki Y, Sassone-Corsi P, Aburatani H, Sugano S, Takumi T (2010) Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism. Mol Cell Biol 30: 5636–5648PubMedCrossRefGoogle Scholar
  43. Hirota T, Okano T, Kokame K, Shirotani-Ikejima H, Miyata T, Fukada Y (2002) Glucose down-regulates Per1 and Per2 mRNA levels and induces circadian gene expression in cultured Rat-1 fibroblasts. J Biol Chem 277:44244–44251PubMedCrossRefGoogle Scholar
  44. Ishida A, Mutoh T, Ueyama T, Bando H, Masubuchi S, Nakahara D, Tsujimoto G, Okamura H (2005) Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab 2:297–307PubMedCrossRefGoogle Scholar
  45. Izumo M, Sato TR, Straume M, Johnson CH (2006) Quantitative analyses of circadian gene expression in mammalian cell cultures. PLoS Comput Biol 2:e136PubMedCrossRefGoogle Scholar
  46. Janik DS, Pickard GE, Menaker M (1990) Circadian locomotor rhythms in the desert iguana. II. Effects of electrolytic lesions to the hypothalamus. J Comp Physiol A 166:811–816PubMedGoogle Scholar
  47. Kalsbeek A, Fliers E (2013) Dialy regulation of hormone profiles. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  48. Kalsbeek A, Garidou ML, Palm IF, Van Der Vliet J, Simonneaux V, Pevet P, Buijs RM (2000) Melatonin sees the light: blocking GABA-ergic transmission in the paraventricular nucleus induces daytime secretion of melatonin. Eur J Neurosci 12:3146–3154PubMedCrossRefGoogle Scholar
  49. Kalsbeek A, La Fleur S, Van Heijningen C, Buijs RM (2004) Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J Neurosci 24:7604–7613PubMedCrossRefGoogle Scholar
  50. Kawamura H, Ibuka N (1978) The search for circadian rhythm pacemakers in the light of lesion experiments. Chronobiologia 5:69–88PubMedGoogle Scholar
  51. Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk HD, Kramer A, Maier B (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci USA 106:21407–21412PubMedCrossRefGoogle Scholar
  52. Ko ML, Shi L, Tsai JY, Young ME, Neuendorff N, Earnest DJ, Ko GY (2011) Cardiac-specific mutation of Clock alters the quantitative measurements of physical activities without changing behavioral circadian rhythms. J Biol Rhythms 26:412–422PubMedCrossRefGoogle Scholar
  53. Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338: 349–354PubMedCrossRefGoogle Scholar
  54. Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U (2007) System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 5:e34PubMedCrossRefGoogle Scholar
  55. Kramer A, Yang FC, Snodgrass P, Li X, Scammell TE, Davis FC, Weitz CJ (2001) Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 294: 2511–2515PubMedCrossRefGoogle Scholar
  56. Lamia KA, Storch KF, Weitz CJ (2008) Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA 105:15172–15177PubMedCrossRefGoogle Scholar
  57. Lamia KA, Sachdeva UM, DiTacchio L, Williams EC, Alvarez JG, Egan DF, Vasquez DS, Juguilon H, Panda S, Shaw RJ, Thompson CB, Evans RM (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326:437–440PubMedCrossRefGoogle Scholar
  58. Lamia KA, Papp SJ, Yu RT, Barish GD, Uhlenhaut NH, Jonker JW, Downes M, Evans RM (2011) Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480: 552–556PubMedGoogle Scholar
  59. Le Minh N, Damiola F, Tronche F, Schutz G, Schibler U (2001) Glucocorticoid hormones inhibit food-induced phase-shifting of peripheral circadian oscillators. EMBO J 20:7128–7136PubMedCrossRefGoogle Scholar
  60. Lee JE, Atkins N Jr, Hatcher NG, Zamdborg L, Gillette MU, Sweedler JV, Kelleher NL (2010) Endogenous peptide discovery of the rat circadian clock: a focused study of the suprachiasmatic nucleus by ultrahigh performance tandem mass spectrometry. Mol Cell Proteomics 9:285–297PubMedCrossRefGoogle Scholar
  61. LeSauter J, Hoque N, Weintraub M, Pfaff DW, Silver R (2009) Stomach ghrelin-secreting cells as food-entrainable circadian clocks. Proc Natl Acad Sci USA 106:13582–13587PubMedCrossRefGoogle Scholar
  62. Li XM, Delaunay F, Dulong S, Claustrat B, Zampera S, Fujii Y, Teboul M, Beau J, Levi F (2010) Cancer inhibition through circadian reprogramming of tumor transcriptome with meal timing. Cancer Res 70:3351–3360PubMedCrossRefGoogle Scholar
  63. Liu X, Lorenz L, Yu QN, Hall JC, Rosbash M (1988) Spatial and temporal expression of the period gene in Drosophila melanogaster. Genes Dev 2:228–238PubMedCrossRefGoogle Scholar
  64. Liu AC, Welsh DK, Ko CH, Tran HG, Zhang EE, Priest AA, Buhr ED, Singer O, Meeker K, Verma IM, Doyle FJ 3rd, Takahashi JS, Kay SA (2007) Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129:605–616PubMedCrossRefGoogle Scholar
  65. Long MA, Jutras MJ, Connors BW, Burwell RD (2005) Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat Neurosci 8:61–66PubMedCrossRefGoogle Scholar
  66. Mahoney CE, Brewer D, Costello MK, Brewer JM, Bittman EL (2010) Lateralization of the central circadian pacemaker output: a test of neural control of peripheral oscillator phase. Am J Physiol Regul Integr Comp Physiol 299:R751–R761PubMedCrossRefGoogle Scholar
  67. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH, Lopez JP, Philipson LH, Bradfield CA, Crosby SD, JeBailey L, Wang X, Takahashi JS, Bass J (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466:627–631PubMedCrossRefGoogle Scholar
  68. Marcheva B, Ramsey KM, Peek CB, Affinati A, Maury E, Bass J (2013) Circadian clocks and metabolism. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  69. Maret S, Dorsaz S, Gurcel L, Pradervand S, Petit B, Pfister C, Hagenbuchle O, O’Hara BF, Franken P, Tafti M (2007) Homer1a is a core brain molecular correlate of sleep loss. Proc Natl Acad Sci USA 104:20090–20095PubMedCrossRefGoogle Scholar
  70. Maywood ES, Chesham JE, O’Brien JA, Hastings MH (2011) A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc Natl Acad Sci USA 108:14306–14311PubMedCrossRefGoogle Scholar
  71. McGlincy NJ, Valomon A, Chesham JE, Maywood ES, Hastings MH, Ule J (2012) Regulation of alternative splicing by the circadian clock and food related cues. Genome Biol 13:R54PubMedCrossRefGoogle Scholar
  72. Minami Y, Ode KL, Ueda HR (2013) Mammalian circadian clock; the roles of transcriptional repression and delay. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  73. Minors DS, Waterhouse JM (1982) Circadian rhythms of urinary excretion: the relationship between the amount excreted and the circadian changes. J Physiol 327:39–51PubMedGoogle Scholar
  74. Morf J, Rey G, Schneider K, Stratmann M, Fujita J, Naef F, Schibler U (2012) Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally. Science 338: 379–383PubMedCrossRefGoogle Scholar
  75. Nagoshi E, Saini C, Bauer C, Laroche T, Naef F, Schibler U (2004) Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 119:693–705PubMedCrossRefGoogle Scholar
  76. Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, Guarente LP, Sassone-Corsi P (2008) The NAD+−dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134:329–340PubMedCrossRefGoogle Scholar
  77. Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324:654–657PubMedCrossRefGoogle Scholar
  78. O’Neill JS, Reddy AB (2010) Circadian clocks in human red blood cells. Nature 469:498–503CrossRefGoogle Scholar
  79. O’Neill JS, Maywood ES, Hastings MH (2013) Cellular mechanisms of circadian pacemaking: beyond transcriptional loops. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  80. Padmanabhan K, Robles MS, Westerling T, Weitz CJ (2012) Feedback regulation of transcriptional termination by the mammalian circadian clock PERIOD complex. Science 337:599–602PubMedCrossRefGoogle Scholar
  81. Pagani L, Semenova EA, Moriggi E, Revell VL, Hack LM, Lockley SW, Arendt J, Skene DJ, Meier F, Izakovic J, Wirz-Justice A, Cajochen C, Sergeeva OJ, Cheresiz SV, Danilenko KV, Eckert A, Brown SA (2010) The physiological period length of the human circadian clock in vivo is directly proportional to period in human fibroblasts. PLoS One 5:e13376PubMedCrossRefGoogle Scholar
  82. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320PubMedCrossRefGoogle Scholar
  83. Pendergast JS, Niswender KD, Yamazaki S (2011) Tissue-specific function of period3 in circadian rhythmicity. PloS one 7:e30254CrossRefGoogle Scholar
  84. Pendergast JS, Niswender KD, Yamazaki S (2012) Tissue-specific function of period3 in circadian rhythmicity. PLoS One 7:e30254PubMedCrossRefGoogle Scholar
  85. Perreau-Lenz S, Kalsbeek A, Garidou ML, Wortel J, van der Vliet J, van Heijningen C, Simonneaux V, Pevet P, Buijs RM (2003) Suprachiasmatic control of melatonin synthesis in rats: inhibitory and stimulatory mechanisms. Eur J Neurosci 17:221–228PubMedCrossRefGoogle Scholar
  86. Plautz JD, Kaneko M, Hall JC, Kay SA (1997) Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632–1635PubMedCrossRefGoogle Scholar
  87. Reddy AB (2013) Genome-wide analyses of circadian systems. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  88. Reddy AB, Karp NA, Maywood ES, Sage EA, Deery M, O’Neill JS, Wong GK, Chesham J, Odell M, Lilley KS, Kyriacou CP, Hastings MH (2006) Circadian orchestration of the hepatic proteome. Curr Biol 16:1107–1115PubMedCrossRefGoogle Scholar
  89. Reddy AB, Maywood ES, Karp NA, King VM, Inoue Y, Gonzalez FJ, Lilley KS, Kyriacou CP, Hastings MH (2007) Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45:1478–1488PubMedCrossRefGoogle Scholar
  90. Reick M, Garcia JA, Dudley C, McKnight SL (2001) NPAS2: an analog of clock operative in the mammalian forebrain. Science 293:506–509PubMedCrossRefGoogle Scholar
  91. Reinke H, Saini C, Fleury-Olela F, Dibner C, Benjamin IJ, Schibler U (2008) Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev 22:331–345PubMedCrossRefGoogle Scholar
  92. Rey G, Cesbron F, Rougemont J, Reinke H, Brunner M, Naef F (2011) Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol 9:e1000595PubMedCrossRefGoogle Scholar
  93. Ripperger JA, Shearman LP, Reppert SM, Schibler U (2000) CLOCK, an essential pacemaker component, controls expression of the circadian transcription factor DBP. Genes Dev 14: 679–689PubMedGoogle Scholar
  94. Roenneberg T, Kantermann T, Juda M, Vetter C, Allebrandt KV (2013) Light and the human circadian clock. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  95. Rutter J, Reick M, Wu LC, McKnight SL (2001) Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293:510–514PubMedCrossRefGoogle Scholar
  96. Scheer FA, Ter Horst GJ, van Der Vliet J, Buijs RM (2001) Physiological and anatomic evidence for regulation of the heart by suprachiasmatic nucleus in rats. Am J Physiol Heart Circ Physiol 280:H1391–H1399PubMedGoogle Scholar
  97. Schmutz I, Ripperger JA, Baeriswyl-Aebischer S, Albrecht U (2010) The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev 24:345–357PubMedCrossRefGoogle Scholar
  98. Shearman LP, Jin X, Lee C, Reppert SM, Weaver DR (2000) Targeted disruption of the mPer3 gene: subtle effects on circadian clock function. Mol Cell Biol 20:6269–6275PubMedCrossRefGoogle Scholar
  99. Shinohara K, Funabashi T, Mitushima D, Kimura F (2000) Effects of gap junction blocker on vasopressin and vasoactive intestinal polypeptide rhythms in the rat suprachiasmatic nucleus in vitro. Neurosci Res 38:43–47PubMedCrossRefGoogle Scholar
  100. Silver R, LeSauter J, Tresco PA, Lehman MN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382: 810–813PubMedCrossRefGoogle Scholar
  101. Slat E, Freeman GM, Herzog ED (2013) The clock in the brain: neurons, glia and networks in daily rhythms. In: Kramer A, Merrow M (eds) Circadian clocks, vol 217, Handbook of experimental pharmacology. Springer, HeidelbergCrossRefGoogle Scholar
  102. Son GH, Chung S, Choe HK, Kim HD, Baik SM, Lee H, Lee HW, Choi S, Sun W, Kim H, Cho S, Lee KH, Kim K (2008) Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc Natl Acad Sci USA 105: 20970–20975PubMedCrossRefGoogle Scholar
  103. Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69:1583–1586PubMedCrossRefGoogle Scholar
  104. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490–493PubMedCrossRefGoogle Scholar
  105. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83PubMedCrossRefGoogle Scholar
  106. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ (2007) Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130:730–741PubMedCrossRefGoogle Scholar
  107. Takahashi JS, Menaker M (1979) Physiology of avian circadian pacemakers. Fed Proc 38: 2583–2588PubMedGoogle Scholar
  108. Teboul M, Grechez-Cassiau A, Guillaumond F, Delaunay F (2009) How nuclear receptors tell time. J Appl Physiol 107:1965–1971PubMedCrossRefGoogle Scholar
  109. Tosini G, Menaker M (1996) Circadian rhythms in cultured mammalian retina. Science 272: 419–421PubMedCrossRefGoogle Scholar
  110. Trudel E, Bourque CW (2012) Circadian modulation of osmoregulated firing in rat supraoptic nucleus neurons. J Neuroendocrinol 24:577–586PubMedCrossRefGoogle Scholar
  111. Tsai JY, Kienesberger PC, Pulinilkunnil T, Sailors MH, Durgan DJ, Villegas-Montoya C, Jahoor A, Gonzalez R, Garvey ME, Boland B, Blasier Z, McElfresh TA, Nannegari V, Chow CW, Heird WC, Chandler MP, Dyck JR, Bray MS, Young ME (2010) Direct regulation of myocardial triglyceride metabolism by the cardiomyocyte circadian clock. J Biol Chem 285:2918–2929PubMedCrossRefGoogle Scholar
  112. Tsuchiya Y, Minami I, Kadotani H, Nishida E (2005) Resetting of peripheral circadian clock by prostaglandin E2. EMBO Rep 6:256–261PubMedCrossRefGoogle Scholar
  113. Ueda HR, Hayashi S, Chen W, Sano M, Machida M, Shigeyoshi Y, Iino M, Hashimoto S (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37:187–192PubMedCrossRefGoogle Scholar
  114. Um JH, Pendergast JS, Springer DA, Foretz M, Viollet B, Brown A, Kim MK, Yamazaki S, Chung JH (2011) AMPK regulates circadian rhythms in a tissue- and isoform-specific manner. PLoS One 6:e18450PubMedCrossRefGoogle Scholar
  115. Urbanski HF (2011) Role of circadian neuroendocrine rhythms in the control of behavior and physiology. Neuroendocrinology 93:211–222PubMedCrossRefGoogle Scholar
  116. Valnegri P, Khelfaoui M, Dorseuil O, Bassani S, Lagneaux C, Gianfelice A, Benfante R, Chelly J, Billuart P, Sala C, Passafaro M (2011) A circadian clock in hippocampus is regulated by interaction between oligophrenin-1 and Rev-erbalpha. Nat Neurosci 14:1293–1301PubMedCrossRefGoogle Scholar
  117. Vollmers C, Gill S, DiTacchio L, Pulivarthy SR, Le HD, Panda S (2009) Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc Natl Acad Sci USA 106:21453–21458PubMedCrossRefGoogle Scholar
  118. Webb AB, Angelo N, Huettner JE, Herzog ED (2009) Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc Natl Acad Sci USA 106:16493–16498PubMedCrossRefGoogle Scholar
  119. Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697–706PubMedCrossRefGoogle Scholar
  120. Welsh DK, Yoo SH, Liu AC, Takahashi JS, Kay SA (2004) Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr Biol 14:2289–2295PubMedCrossRefGoogle Scholar
  121. Westgate EJ, Cheng Y, Reilly DF, Price TS, Walisser JA, Bradfield CA, FitzGerald GA (2008) Genetic components of the circadian clock regulate thrombogenesis in vivo. Circulation 117:2087–2095PubMedCrossRefGoogle Scholar
  122. Yagita K, Okamura H (2000) Forskolin induces circadian gene expression of rPer1, rPer2 and dbp in mammalian rat-1 fibroblasts. FEBS Lett 465:79–82PubMedCrossRefGoogle Scholar
  123. Yagita K, Tamanini F, van Der Horst GT, Okamura H (2001) Molecular mechanisms of the biological clock in cultured fibroblasts. Science 292:278–281PubMedCrossRefGoogle Scholar
  124. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682–685PubMedCrossRefGoogle Scholar
  125. Yannielli PC, Molyneux PC, Harrington ME, Golombek DA (2007) Ghrelin effects on the circadian system of mice. J Neurosci 27:2890–2895PubMedCrossRefGoogle Scholar
  126. Yi CX, Challet E, Pevet P, Kalsbeek A, Escobar C, Buijs RM (2008) A circulating ghrelin mimetic attenuates light-induced phase delay of mice and light-induced Fos expression in the suprachiasmatic nucleus of rats. Eur J Neurosci 27:1965–1972PubMedCrossRefGoogle Scholar
  127. Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, Menaker M, Takahashi JS (2004) PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 101:5339–5346PubMedCrossRefGoogle Scholar
  128. Zuber AM, Centeno G, Pradervand S, Nikolaeva S, Maquelin L, Cardinaux L, Bonny O, Firsov D (2009) Molecular clock is involved in predictive circadian adjustment of renal function. Proc Natl Acad Sci USA 106:16523–16528PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Institute of Pharmacology and ToxicologyZürichSwitzerland

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