Cross-talk between circadian clocks, sleep-wake cycles, and metabolic networks: Dispelling the darkness

BioEssays

Volumn 38, Issue 4, 2016, Pages 394-405

  Ray, Sandipan ^a   Reddy, Akhilesh B ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

Circadian rhythms; Metabolic networks; Non transcriptional oscillator; Peroxiredoxin; Redox regulation; Sleep wake cycle; Systems biology

Indexed keywords

BIOLOGICAL MARKER; MESSENGER RNA; PEROXIREDOXIN; PROTEOME; SIRTUIN; TRANSCRIPTION FACTOR CLOCK;

ARTICLE; BIOMICS; CELL METABOLISM; CIRCADIAN RHYTHM; CYANOBACTERIUM; FEEDBACK SYSTEM; HUMAN; METABOLISM; NONHUMAN; OSCILLATION; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PROTEIN PROCESSING; PROTEOMICS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SLEEP WAKING CYCLE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; ANIMAL; DROSOPHILA MELANOGASTER; PHOTOPERIODICITY; PHYSIOLOGICAL FEEDBACK; PHYSIOLOGY; SLEEP; SUPRACHIASMATIC NUCLEUS; SYSTEMS BIOLOGY; WAKEFULNESS;

ANIMALS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CLOCK PROTEINS; DROSOPHILA MELANOGASTER; FEEDBACK, PHYSIOLOGICAL; HUMANS; METABOLIC NETWORKS AND PATHWAYS; OXIDATION-REDUCTION; PEROXIREDOXINS; PHOTOPERIOD; SIGNAL TRANSDUCTION; SIRTUINS; SLEEP; SUPRACHIASMATIC NUCLEUS; SYSTEMS BIOLOGY; WAKEFULNESS;

EID: 84961218318     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201500056     Document Type: Article

References (129)

1. Dunlap JC. 1999. Molecular bases for circadian clocks. Cell 96: 271-90.
2. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, et al. 2005. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6: 544-56.
3. Siegel JM. 2005. Clues to the functions of mammalian sleep. Nature 437: 1264-71.
4. Nitz DA, van SB, Tononi G, Greenspan RJ. 2002. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol 12: 1934-40.
5. Maret S, Dorsaz S, Gurcel L, Pradervand S, et al. 2007. Homer1a is a core brain molecular correlate of sleep loss. Proc Natl Acad Sci USA 104: 20090-5.
6. Broussard JL, Ehrmann DA, Van CE, Tasali E, et al. 2012. Impaired insulin signaling in human adipocytes after experimental sleep restriction: a randomized, crossover study. Ann Intern Med 157: 549-57.
7. Saper CB, Scammell TE, Lu J. 2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437: 1257-63.
8. Schwartz JR, Roth T. 2006. Shift work sleep disorder: burden of illness and approaches to management. Drugs 66: 2357-70.
9. Reddy AB, O'Neill JS. 2010. Healthy clocks, healthy body, healthy mind. Trends Cell Biol 20: 36-44.
10. Durgan DJ, Young ME. 2010. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 106: 647-58.
11. Vetter C, Fischer D, Matera JL, Roenneberg T. 2015. Aligning work and circadian time in shift workers improves sleep and reduces circadian disruption. Curr Biol 25: 907-11.
12. Hastings MH, Reddy AB, Maywood ES. 2003. A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 4: 649-61.
13. Wulff K, Gatti S, Wettstein JG, Foster RG. 2010. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat Rev Neurosci 11: 589-99.
14. Sahar S, Sassone-Corsi P. 2009. Metabolism and cancer: the circadian clock connection. Nat Rev Cancer 9: 886-96.
15. Reddy AB, Rey G. 2014. Metabolic and non-transcriptional circadian clocks: eukaryotes. Annu Rev Biochem 83: 165-89.
16. Rey G, Reddy AB. 2013. Physiology. Rhythmic respiration. Science 342: 570-1.
17. Xie L, Kang H, Xu Q, Chen MJ, et al. 2013. Sleep drives metabolite clearance from the adult brain. Science 342: 373-7.
18. Takahashi JS, Hong HK, Ko CH, McDearmon EL. 2008. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9: 764-75.
19. Harmer SL, Panda S, Kay SA. 2001. Molecular bases of circadian rhythms. Annu Rev Cell Dev Biol 17: 215-53.
20. Chen R, Schirmer A, Lee Y, Lee H, et al. 2009. Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol Cell 36: 417-30.
21. Sangoram AM, Saez L, Antoch MP, Gekakis N, et al. 1998. Mammalian circadian autoregulatory loop: a timeless ortholog and mPer1 interact and negatively regulate CLOCK-BMAL1-induced transcription. Neuron 21: 1101-13.
22. Kume K, Zylka MJ, Sriram S, Shearman LP, et al. 1999. MCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98: 193-205.
23. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, et al. 2002. Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12: 540-50.
24. Panda S, Antoch MP, Miller BH, Su AI, et al. 2002. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109: 307-20.
25. Storch KF, Lipan O, Leykin I, Viswanathan N, et al. 2002. Extensive and divergent circadian gene expression in liver and heart. Nature 417: 78-83.
26. Ueda HR, Chen W, Adachi A, Wakamatsu H, et al. 2002. A transcription factor response element for gene expression during circadian night. Nature 418: 534-9.
27. Ueda HR, Hayashi S, Chen W, Sano M, et al. 2005. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37: 187-92.
28. Reddy AB, Karp NA, Maywood ES, Sage EA, et al. 2006. Circadian orchestration of the hepatic proteome. Curr Biol 16: 1107-15.
29. Mauvoisin D, Wang J, Jouffe C, Martin E, et al. 2014. Circadian clock-dependent and -independent rhythmic proteomes implement distinct diurnal functions in mouse liver. Proc Natl Acad Sci USA 111: 167-72.
30. Robles MS, Cox J, Mann M. 2014. In-vivo quantitative proteomics reveals a key contribution of post-transcriptional mechanisms to the circadian regulation of liver metabolism. PLoS Genet 10: e1004047.
31. Nakajima M, Imai K, Ito H, Nishiwaki T, et al. 2005. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308: 414-5.
32. Tomita J, Nakajima M, Kondo T, Iwasaki H. 2005. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307: 251-4.
33. O'Neill JS, van OG, Dixon LE, Troein C, et al. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469: 554-8.
34. O'Neill JS, Reddy AB. 2011. Circadian clocks in human red blood cells. Nature 469: 498-503.
35. Lakin-Thomas PL. 2006. Transcriptional feedback oscillators: maybe, maybe not. J Biol Rhythms 21: 83-92.
36. van OG, Millar AJ. 2012. Non-transcriptional oscillators in circadian timekeeping. Trends Biochem 37: 484-92.
37. Wood TL, Bridwell-Rabb J, Kim YI, Gao T, et al. 2010. The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor. Proc Natl Acad Sci USA 107: 5804-9.
38. Qin X, Byrne M, Mori T, Zou P, et al. 2010. Intermolecular associations determine the dynamics of the circadian KaiABC oscillator. Proc Natl Acad Sci USA 107: 14805-10.
39. Rosbash M. 2009. The implications of multiple circadian clock origins. PLoS Biol 7: e62.
40. Edgar RS, Green EW, Zhao Y, van OG, et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485: 459-64.
41. Copley SD, Novak WR, Babbitt PC. 2004. Divergence of function in the thioredoxin fold suprafamily: evidence for evolution of peroxiredoxins from a thioredoxin-like ancestor. Biochemistry 43: 13981-95.
42. Hall A, Karplus PA, Poole LB. 2009. Typical 2-Cys peroxiredoxins-structures, mechanisms and functions. FEBS J 276: 2469-77.
43. Wood ZA, Poole LB, Karplus PA. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-3.
44. Weerapana E, Wang C, Simon GM, Richter F, et al. 2010. Quantitative reactivity profiling predicts functional cysteines in proteomes. Nature 468: 790-5.
45. 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: 510-4.
46. Wang TA, Yu YV, Govindaiah G, Ye X, et al. 2012. Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337: 839-42.
47. Krishnan N, Davis AJ, Giebultowicz JM. 2008. Circadian regulation of response to oxidative stress in Drosophila melanogaster. Biochem Biophys Res Commun 374: 299-303.
48. Lai AG, Doherty CJ, Mueller-Roeber B, Kay SA, et al. 2012. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc Natl Acad Sci USA 109: 17129-34.
49. Wu L, Reddy AB. 2014. Rethinking the clockwork: redox cycles and non-transcriptional control of circadian rhythms. Biochem Soc Trans 42: 1-0.
50. McDearmon EL, Patel KN, Ko CH, Walisser JA, et al. 2006. Dissecting the functions of the mammalian clock protein BMAL1 by tissue-specific rescue in mice. Science 314: 1304-8.
51. Mohawk JA, Baer ML, Menaker M. 2009. The methamphetamine-sensitive circadian oscillator does not employ canonical clock genes. Proc Natl Acad Sci USA 106: 3519-24.
52. Wijnen H, Young MW. 2006. Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet 40: 409-48.
53. Eckel-Mahan K, Sassone-Corsi P. 2009. Metabolism control by the circadian clock and vice versa. Nat Struct Mol Biol 16: 462-7.
54. Bass J. 2012. Circadian topology of metabolism. Nature 491: 348-56.
55. Masri S, Sassone-Corsi P. 2013. The circadian clock: a framework linking metabolism, epigenetics and neuronal function. Nat Rev Neurosci 14: 69-75.
56. Bass J, Takahashi JS. 2010. Circadian integration of metabolism and energetics. Science 330: 1349-54.
57. Rutter J, Reick M, McKnight SL. 2002. Metabolism and the control of circadian rhythms. Annu Rev Biochem 71: 307-31.
58. Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, et al. 2008. The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134: 329-40.
59. Asher G, Gatfield D, Stratmann M, Reinke H, et al. 2008. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134: 317-28.
60. Nakahata Y, Sahar S, Astarita G, Kaluzova M, et al. 2009. Circadian control of the NAD+ salvage pathway by CLOCK-SI RT1. Science 324: 654-7.
61. Sahar S, Masubuchi S, Eckel-Mahan K, Vollmer S, et al. 2014. Circadian control of fatty acid elongation by SIRT1 protein-mediated deacetylation of acetyl-coenzyme A synthetase 1. J Biol Chem 289: 6091-7.
62. Ramsey KM, Yoshino J, Brace CS, Abrassart D, et al. 2009. Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324: 651-4.
63. Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, et al. 2010. Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142: 943-53.
64. Peek CB, Affinati AH, Ramsey KM, Kuo HY, et al. 2013. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342: 1243417.
65. Asher G, Schibler U. 2011. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab 13: 125-37.
66. Ghosh A, Chance B. 1964. Oscillations of glycolytic intermediates in yeast cells. Biochem Biophys Res Commun 16: 174-81.
67. Bier M, Bakker BM, Westerhoff HV. 2000. How yeast cells synchronize their glycolytic oscillations: a perturbation analytic treatment. Biophys J 78: 1087-93.
68. Kloster A, Olsen LF. 2012. Oscillations in glycolysis in Saccharomyces cerevisiae: the role of autocatalysis and intracellular ATPase activity. Biophys Chem 165-166: 39-47.
69. Zhang EE, Liu Y, Dentin R, Pongsawakul PY, et al. 2010. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat Med 16: 1152-6.
70. Akimoto H, Kinumi T, Ohmiya Y. 2005. Circadian rhythm of a TCA cycle enzyme is apparently regulated at the translational level in the dinoflagellate Lingulodinium polyedrum. J Biol Rhythms 20: 479-89.
71. Guo J, Nguyen AY, Dai Z, Su D, et al. 2014. Proteome-wide light/dark modulation of thiol oxidation in cyanobacteria revealed by quantitative site-specific redox proteomics. Mol Cell Proteomics 13: 3270-85.
72. Masri S, Patel VR, Eckel-Mahan KL, Peleg S, et al. 2013. Circadian acetylome reveals regulation of mitochondrial metabolic pathways. Proc Natl Acad Sci USA 110: 3339-44.
73. Dallmann R, Viola AU, Tarokh L, Cajochen C, et al. 2012. The human circadian metabolome. Proc Natl Acad Sci USA 109: 2625-9.
74. Davies SK, Ang JE, Revell VL, Holmes B, et al. 2014. Effect of sleep deprivation on the human metabolome. Proc Natl Acad Sci USA 111: 10761-6.
75. Martinez-Lozano SP, Tarokh L, Li X, Kohler M, et al. 2014. Circadian variation of the human metabolome captured by real-time breath analysis. PLoS ONE 9: e114422.
76. Yamazaki S, Numano R, Abe M, Hida A, et al. 2000. Resetting central and peripheral circadian oscillators in transgenic rats. Science 288: 682-5.
77. Reppert SM, Weaver DR. 2001. Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63: 647-76.
78. Fuller PM, Gooley JJ, Saper CB. 2006. Neurobiology of the sleep-wake cycle: sleep architecture, circadian regulation, and regulatory feedback. J Biol Rhythms 21: 482-93.
79. Deboer T, Vansteensel MJ, Detari L, Meijer JH. 2003. Sleep states alter activity of suprachiasmatic nucleus neurons. Nat Neurosci 6: 1086-90.
80. Borbely AA. 1982. A two process model of sleep regulation. Hum Neurobiol 1: 195-204.
81. Franken P, Dijk DJ. 2009. Circadian clock genes and sleep homeostasis. Eur J Neurosci 29: 1820-9.
82. Franken P. 2013. A role for clock genes in sleep homeostasis. Curr Opin Neurobiol 23: 864-72.
83. Shaw PJ, Tononi G, Greenspan RJ, Robinson DF. 2002. Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417: 287-91.
84. Wisor JP, Pasumarthi RK, Gerashchenko D, Thompson CL, et al. 2008. Sleep deprivation effects on circadian clock gene expression in the cerebral cortex parallel electroencephalographic differences among mouse strains. J Neurosci 28: 7193-201.
85. Krueger JM, Obal F, Jr. 2003. Sleep function. Front Biosci 8: d511-9.
86. Huber R, Ghilardi MF, Massimini M, Tononi G. 2004. Local sleep and learning. Nature 430: 78-81.
87. Ferrara M, De GL. 2011. Going local: insights from EEG and stereo-EEG studies of the human sleep-wake cycle. Curr Top Med Chem 11: 2423-37.
88. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, et al. 2011. Local sleep in awake rats. Nature 472: 443-7.
89. Krueger JM, Rector DM, Roy S, Van Dongen HP, et al. 2008. Sleep as a fundamental property of neuronal assemblies. Nat Rev Neurosci 9: 910-9.
90. Hinard V, Mikhail C, Pradervand S, Curie T, et al. 2012. Key electrophysiological, molecular, and metabolic signatures of sleep and wakefulness revealed in primary cortical cultures. J Neurosci 32: 12506-17.
91. Cirelli C, Gutierrez CM, Tononi G. 2004. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41: 35-43.
92. Robles MS, Mann M. 2013. Proteomic approaches in circadian biology. Handb Exp Pharmacol 2013: 389-407.
93. Moller M, Sparre T, Bache N, Roepstorff P, et al. 2007. Proteomic analysis of day-night variations in protein levels in the rat pineal gland. Proteomics 7: 2009-18.
94. Deery MJ, Maywood ES, Chesham JE, Sladek M, et al. 2009. Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the suprachiasmatic circadian clock. Curr Biol 19: 2031-6.
95. Ong SE, Mann M. 2005. Mass spectrometry-based proteomics turns quantitative. Nat Chem Biol 1: 252-62.
96. Lee JE, Zamdborg L, Southey BR, Atkin N, Jr., et al. 2013. Quantitative peptidomics for discovery of circadian-related peptides from the rat suprachiasmatic nucleus. J Proteome Res 12: 585-93.
97. Lee JE, Atkins N, Jr., Hatcher NG, Zamdborg L, et al. 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: 285-97.
98. Seo HS, Hirano M, Shibato J, Rakwal R, et al. 2008. Effects of coffee bean aroma on the rat brain stressed by sleep deprivation: a selected transcript- and 2D gel-based proteome analysis. J Agric Food Chem 56: 4665-73.
99. Pawlyk AC, Ferber M, Shah A, Pack AI, et al. 2007. Proteomic analysis of the effects and interactions of sleep deprivation and aging in mouse cerebral cortex. J Neurochem 103: 2301-13.
100. Janich P, Arpat AB, Castelo-Szekely V, Lopes M, et al. 2015. Ribosome profiling reveals the rhythmic liver translatome and circadian clock regulation by upstream open reading frames. Genome Res 25: 1848-59.
101. Jang C, Lahens NF, Hogenesch JB, Sehgal A. 2015. Ribosome profiling reveals an important role for translational control in circadian gene expression. Genome Res 25: 1836-47.
102. Zhou M, Wang W, Karapetyan S, Mwimba M, et al. 2015. Redox rhythm reinforces the circadian clock to gate immune response. Nature 523: 472-6.
103. Yoshida Y, Iigusa H, Wang N, Hasunuma K. 2011. Cross-talk between the cellular redox state and the circadian system in Neurospora. PLoS ONE 6: e28227.
104. Gillette MU, Wang TA. 2014. Brain circadian oscillators and redox regulation in mammals. Antioxid Redox Signal 20: 2955-65.
105. Mann M, Jensen ON. 2003. Proteomic analysis of post-translational modifications. Nat Biotechnol 21: 255-61.
106. Kim EY, Edery I. 2006. Balance between DBT/CKIepsilon kinase and protein phosphatase activities regulate phosphorylation and stability of Drosophila CLOCK protein. Proc Natl Acad Sci USA 103: 6178-83.
107. Hirano A, Yumimoto K, Tsunematsu R, Matsumoto M, et al. 2013. FBXL21 regulates oscillation of the circadian clock through ubiquitination and stabilization of cryptochromes. Cell 152: 1106-18.
108. Cardone L, Hirayama J, Giordano F, Tamaru T, et al. 2005. Circadian clock control by SUMOylation of BM AL1. Science 309: 1390-4.
109. Eckel-Mahan KL, Patel VR, Mohney RP, Vignola KS, et al. 2012. Coordination of the transcriptome and metabolome by the circadian clock. Proc Natl Acad Sci USA 109: 5541-6.
110. Patel VR, Eckel-Mahan K, Sassone-Corsi P, Baldi P. 2012. CircadiOmics: integrating circadian genomics, transcriptomics, proteomics, and metabolomics. Nat Methods 9: 772-3.
111. Zhang R, Lahens NF, Ballance HI, Hughes ME, et al. 2014. A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA 111: 16219-24.
112. Petit JM, Burlet-Godinot S, Magistretti PJ, Allaman I. 2015. Glycogen metabolism and the homeostatic regulation of sleep. Metab Brain Dis 30: 263-79.
113. Benington JH, Heller HC. 1995. Restoration of brain energy metabolism as the function of sleep. Prog Neurobiol 45: 347-60.
114. Van CE, Spiegel K, Tasali E, Leproult R. 2008. Metabolic consequences of sleep and sleep loss. Sleep Med 9: S23-8.
115. Grimaldi B, Bellet MM, Katada S, Astarita G, et al. 2010. PER2 controls lipid metabolism by direct regulation of PPARgamma. Cell Metab 12: 509-20.
116. Van der Horst GT, Muijtjens M, Kobayashi K, Takano R, et al. 1999. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398: 627-30.
117. Zaniolo K, Desnoyers S, Leclerc S, Guerin SL. 2007. Regulation of poly(ADP-ribose) polymerase-1 (PARP-1) gene expression through the post-translational modification of Sp1: a nuclear target protein of PARP-1. BMC Mol Biol 8: 96.
118. Hallows WC, Lee S, Denu JM. 2006. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103: 10230-5.
119. Lamia KA, Sachdeva UM, DiTacchio L, Williams EC, et al. 2009. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326: 437-40.
120. Liu C, Li S, Liu T, Borjigin J, et al. 2007. Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447: 477-81.
121. Rodgers JT, Lerin C, Haas W, Gygi SP, et al. 2005. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434: 113-8.
122. Kaasik K, Lee CC. 2004. Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430: 467-71.
123. Reinke H, Saini C, Fleury-Olela F, Dibner C, et al. 2008. Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev 22: 331-45.
124. O'Neill JS, Maywood ES, Chesham JE, Takahashi JS, et al. 2008. CAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320: 949-53.
125. Lee B, Li A, Hansen KF, Cao R, et al. 2010. CREB influences timing and entrainment of the SCN circadian clock. J Biol Rhythms 25: 410-20.
126. Brunet A, Sweeney LB, Sturgill JF, Chua KF, et al. 2004. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-5.
127. Frescas D, Valenti L, Accili D. 2005. Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J Biol Chem 280: 20589-95.
128. Sato TK, Panda S, Miraglia LJ, Reyes TM, et al. 2004. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 43: 527-37.
129. 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: 345-57.